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Exposure to nitrogen does not eliminate N2 fixation in the feather moss Pleurozium schreberi (Brid.) Mitt
Abstract
Background and aims
The feather moss Pleurozium schreberi (Brid.) Mitt. is colonized by cyanobacteria, which fix substantial amounts of atmospheric nitrogen (N) in pristine and N-poor ecosystems. Cyanobacterial N2 fixation is inhibited by N deposition. However, the threshold of N input that leads to the inhibition of N2 fixation has not been adequately investigated. Further, the ability of N2 fixation to recover in mosses from high N deposition areas has not been studied to date.
Methods
We conducted two laboratory studies in which we (1) applied a range of concentrations of N as NH4NO3 to mosses from low N-deposition areas, and (2) we deprived mosses from a high N-deposition area of N to test their ability to recover N2 fixation.
Results
Higher addition rates (up to 10 kg N ha−1) did not systematically inhibit N2 fixation in P. schreberi. Conversely, upon weeks of N deprivation of mosses from a high N environment, N2 fixation rates increased.
Conclusions
The threshold of total N deposition above which N2 fixation in P. schreberi is inhibited is likely to be > 10 kg N ha−1. Further, cyanobacteria are able to recover from high N inputs and are able to fix atmospheric N2 after a period of N deprivation.
Supplementary resource (1)
... Multiple studies have shown that N deposition affects diazotrophic activity in a dose-dependent way. Recently, Rousk et al. (2013b) showed that N 2 fixation rates in the forest moss Pleurozium schreberi, mainly colonized by cyanobacteria, were not sensitive to N amendments up to 10 kg N ha −1 year −1 . This result was similar to the upper limit of N deposition that Sphagnum mosses could adsorb before N compounds started to leach into deeper peat layers, as calculated in Lamers et al. (2000). ...
... This result was similar to the upper limit of N deposition that Sphagnum mosses could adsorb before N compounds started to leach into deeper peat layers, as calculated in Lamers et al. (2000). However, when the Pleurozium mosses were experimentally deprived of N, after having been exposed to high N deposition rates, their microbial community reacted with an increase in N 2 fixation rates (Rousk et al. 2013b). Similarly, along a natural gradient of N deposition levels, the diazotrophic activity (mainly of cyanobacteria) associated with the forest mosses Hylocomium splendens and P. schreberi was shown to decrease with increasing N deposition levels (Leppänen et al. 2013). ...
... Studies on the effect of N fertilization on S. fuscum and S. angustifolium-associated diazotrophs in a pristine peat bog showed that the diazotrophic activity was negatively affected by high N input, although moss productivity did not change (Vile et al. 2014). The difference in response pattern to N deposition between the study of Rousk et al. (2013b) and the others indicates that increased N deposition may not have a uniform effect on diazotrophs in all moss species. Rather, it suggests that the response may be influenced by diazotrophic community composition, as well as by differential plant-microbe interactions. ...
Background and aims
In pristine ombrotrophic Sphagnum-dominated peatland ecosystems nitrogen (N) is often a limiting nutrient, which is replenished by biological N2 fixation and atmospheric N deposition. It is, however, unclear which impact long-term N deposition has on microbial N2 fixing activity and diazotrophic diversity, and whether phosphorus (P) modulates the response. Therefore, we studied the impact of increased N deposition and N depletion on microbial N2 fixation and diazotrophic diversity associated with the peat moss Sphagnum magellanicum, and their interaction with P availability.
Methods
Nitrogenase activities of S. magellanicum-associated microorganisms were determined by acetylene reduction assays (ARA) and 15N2 tracer methods on mosses from two geographically distinct locations with different N deposition histories, high or low N deposition, and in samples depleted in N (grown 3 years in the greenhouse) versus recent field samples. The short-term response to increased N deposition was tested for mosses differing in N and P fertilization histories. In addition, diversity of diazotrophic microorganisms was assessed by nifH gene amplicon sequencing of N-depleted mosses.
Results
We showed distinct and persistent differences in diazotrophic communities and their activities associated with S. magellanicum from sites with high versus low N deposition. Initially, diazotrophic activity was six times higher for the low N site. During incubation and repeated ARA, however, this activity strongly decreased, while it remained stable for the high N site. Activity for the high N site could not be increased by long-term experimental N deprivation. Short-term, experimental N application had an inhibitory effect on N2 fixation for both sites, which was not observed in mosses with high indirect P availability.
Conclusions
We conclude that although N deposition negatively affects N2 fixation as also shown in previous studies, long-term effects of N deprivation on the diazotrophic activity and community are more complex. Furthermore, our results indicated that P availability might be an important factor in modulating the response of Sphagnum-associated diazotrophs to N deposition.
... 8,10). And other studies have demonstrated a recovery from N stress upon removal of the stressor [13]. Yet, the potential ability of N 2 fixation in mosses to acclimatize to high N loads, that is, to grow less sensitive to the stressor, has not been investigated so far. ...
... Surprisingly, N 2 fixation in P. schreberi was also found to be inhibited by only 3 kg N ha -1 yr -1 additions in a different field study by the same authors [8], indicating that pre-sampling conditions [16] and site characteristics like throughfall N [10] and horizontal N deposition [15,17] might have fundamental effects on nitrogenase activity. On the other hand, in a laboratory set-up [13], the authors found no inhibition of N 2 fixation in P. schreberi at additions of 10 kg N, contrasting the results reported by [8], and [10] showing moss associated N 2 fixation to be inhibited by road-derived N deposition of 4 kg N ha -1 yr -1 in boreal forests. Thus, although N input can impede N 2 fixation in mosses, the threshold of N input above which N 2 fixation is inhibited is not well defined. ...
... While the applied solutions might have been quickly washed through the moss, solid N fertilizers used in other addition experiments likely lead to a slow and constant N release to moss and associated N 2 fixers [8]. Further, laboratory incubations exclude any background N deposition rates including atmospheric N, throughfall N and horizontal N deposition, which could add more than 6 kg N ha -1 yr -1 [10,27], leading to a total N input to pristine ecosystems that can be above 10 kg N ha -1 yr -1 [13]. ...
Nitrogen (N2) fixation is a major source of available N in ecosystems that receive low amounts of atmospheric N deposition. In boreal forest and subarctic tundra, the feather moss Hylocomium splendens is colonized by N2 fixing cyanobacteria that could contribute fundamentally to increase the N pool in these ecosystems. However, N2 fixation in mosses is inhibited by N input. Although this has been shown previously, the ability of N2 fixation to grow less sensitive towards repeated, increased N inputs remains unknown. Here, we tested if N2 fixation in H. splendens can recover from increased N input depending on the N load (0, 5, 20, 80, 320 kg N ha-1 yr-1) after a period of N deprivation, and if sensitivity towards increased N input can decrease after repeated N additions. Nitrogen fixation in the moss was inhibited by the highest N addition, but was promoted by adding 5 kg N ha-1 yr-1, and increased in all treatments during a short period of N deprivation. The sensitivity of N2 fixation towards repeated N additions seem to decrease in the 20 and 80 kg N additions, but increased in the highest N addition (320 kg N ha-1 yr-1). Recovery of N in leachate samples increased with increasing N loads, suggesting low retention capabilities of mosses if N input is above 5 kg N ha-1 yr-1. Our results demonstrate that the sensitivity towards repeated N additions is likely to decrease if N input does not exceed a certain threshold.
... Most of the studies on moss-associated biological N 2 fixation (BNF) have been conducted in N-poor environments such as arctic and boreal peatlands or forests (Knorr et al., 2015;Porada et al., 2014; Christina Groß and Shakhawat Hossen share the first authorship. Rousk et al., 2014a) whereas little is known about BNF in mosses that are common in N-rich temperate forests. ...
... Diazotrophs may switch their energy-intense BNF activity when sufficient ammonium or nitrate is available (Dynarski & Houlton, 2018;Norman & Friesen, 2017). Most N-fertilization experiments showed decreasing BNF rates in several moss species (Gundale et al., 2011;Kox et al., 2016;Wang et al., 2022), but some studies also reported no effect on BNF following moderate N additions to mosses (Rousk et al., 2014a;van den Elzen et al., 2018). A decrease in BNF due to the addition of reactive N was yet not reported for mosses from temperate forests, which may have higher N need or greater tolerance against high N availability than boreal mosses. ...
Many moss species are associated with nitrogen (N)‐fixing bacteria (diazotrophs) that support the N supply of mosses. Our knowledge relates primarily to pristine ecosystems with low atmospheric N input, but knowledge of biological N fixation (BNF) and diazotrophic communities in mosses in temperate forests with high N deposition is limited. We measured BNF rates using the direct stable isotope method and studied the total and potentially active diazotrophic communities in two abundant mosses, Brachythecium rutabulum and Hypnum cupressiforme , both growing on lying deadwood trunks in 25 temperate forest sites. BNF rates in both mosses were similar to those observed in moss species of pristine ecosystems. H. cupressiforme fixed three times more N 2 and exhibited lower diazotrophic richness than B. rutabulum . Frankia was the most prominent diazotroph followed by cyanobacteria Nostoc. Manganese, iron, and molybdenum contents in mosses were positively correlated with BNF and diazotrophic communities. Frankia maintained high BNF rates in H. cupressiforme and B. rutabulum even under high chronic N deposition in Central European forests. Moss N concentration and ¹⁵ N abundance indicate a rather minor contribution of BNF to the N nutrition of these mosses.
... In October 2016, total precipitation in Forks, WA (closest NOAA weather station located to the Hoh Rainforest) and Seattle was 59.99 cm and 26.16 cm, respectively (NOWData 2017). Previous studies have observed a positive relationship between rainfall frequency and N 2 fixation rates in boreal ecosystems (DeLuca et al. 2002;Zielke et al. 2002;Gundale et al. 2009Gundale et al. , 2012Rousk et al. 2014). In this case there was no apparent moisture limitation in October (based on the NOAA precipitation data), but perhaps samples collected in October 2016 exceeded the optimum moisture requirement to facilitate N 2 fixation (see Rousk et al. 2017). ...
... However, it remains unclear how N fixed through cyanobacteria associations enters the soil for plant uptake. Because mosses are efficient in retaining nutrients (Oechel and Van Cleve 1986;Aldous 2002), the rate at which fixed N is transferred to soil and plants is expected to be slow (Rousk et al. 2014;DeLuca et al 2022). In A. macrophyllum canopies, fixed N may enter the environment by accumulating in canopy soil. ...
Purpose
Old-growth forests in the Pacific Northwest host a variety of epiphytes on their branches and stem. Given the common and often large epiphytic biomass associated with Acer macrophyllum (Pursh) in this region, we evaluated how seasonal weather changes and urbanization (metal and nitrogen deposition), affect canopy epiphytic N2 fixation in the Hoh Rainforest of the Olympic Peninsula and in urban parks and forests in Seattle.
Methods
We collected Isothecium stoloniferum (Brid.) samples from both the Hoh Rainforest and Seattle at four periods from April 2016 through January 2017. Moss-associated N2 fixation rates were measured in the laboratory using the acetylene reduction assay and trace metal concentrations in the moss were analyzed using NO3 + H2O2 digestion.
Results
We found levels of N2 fixation were highest during the spring sampling period. Elevated levels of heavy metals were observed in I. stoloniferum samples collected in the urban canopies in Seattle where N2 fixation rates were low, suggesting N2 fixation is sensitive to the bioaccumulation of heavy metals. In A. macrophyllum canopies, I. stoloniferum was found to yield 0.1130 g N m⁻² yr⁻¹ in canopy branches within the Hoh Rainforest and only 0.0009 g N m⁻² yr⁻¹ on branches in Seattle.
Conclusions
These results highlight a rarely explored source of biological N2-fixation in temperate rainforests and suggest that epiphytic N2-fixation may contribute bio-available nitrogen in A. macrophyllum stands. N2-fixation in canopy bryophytes was found to be highly sensitive to urban pollution, possibly due to bioaccumulation of heavy metals in bryophyte tissue.
... Though N 2 fixation can be inhibited by N inputs, moss-cyanobacteria associations can show resilience towards increased N enrichment. For instance, negative effects of high N inputs (> 12 kg N ha −1 year −1 ) on moss-associated N 2 fixation disappeared quickly after N input ceased (within 2 weeks) (Rousk et al. 2014a) and no effects on N 2 fixation in mosses by long-term N additions (0-50 kg N ha −1 year −1 ) were found (Gundale et al. 2013). Recovery of moss-associated N 2 fixation has even been found after adding very high N inputs (5-320 kg N ha −1 year −1 ), providing only 2 weeks of recovery (Rousk & Michelsen 2016). ...
... Previous studies have shown that recovery from high N inputs needs a longer time or N needs to be actively removed via e.g. rinsing (Rousk et al. 2014a;Rousk and Michelsen 2016). Therefore, recovery from N inputs is possible, if N input remains below a certain threshold. ...
Moss-associated nitrogen (N2) fixation is one of the main inputs of new N in pristine ecosystems that are characterized by low N availability. Previous studies have shown that N2 fixation is inhibited by inorganic N (IN) inputs, but if N2 fixation in mosses is similarly affected by organic N (ON) remains unknown. Here, we assessed N2 fixation in two dominant mosses in boreal forests (Pleurozium schreberi and Sphagnum capillifolium) in response to different levels of N, simulating realistic (up to 4 kg N ha⁻¹ year⁻¹) and extreme N addition rates in pristine ecosystems (up to 20 kg N ha⁻¹ year⁻¹) of IN (ammonium nitrate) and ON (alanine and urea). We also assessed if N2 fixation can recover from the N additions. In the realistic scenario, N2 fixation was inhibited by increasing NH4NO3 additions in P. schreberi but not in S. capillifolium, and alanine and urea stimulated N2 fixation in both moss species. In contrast, in the extreme N additions, increasing N inputs inhibited N2 fixation in both moss species and all N forms. Nitrogen fixation was more sensitive to N inputs in P. schreberi than in S. capillifolium and was higher in the recovery phase after the realistic compared to the extreme N additions. These results demonstrate that N2 fixation in mosses is less sensitive to organic than inorganic N inputs and highlight the importance of considering different N forms and species-specific responses when estimating the impact of N inputs on ecosystem functions such as moss-associated N2 fixation.
... In this study, the nitrogenase activity of bryophytes showed a highly positive correlation with the degree of cyanobacterial colonization (Fig. 4), which is consistent with previous studies (DeLuca et al., 2007;Lindo and Whiteley, 2011;Rousk et al., 2014a;Jean et al., 2020). On a global level, the current research on biological N fixation in mosses is mainly focused on boreal forests. ...
... Subsequently, Zackrisson et al. (2004) showed that the number of symbiotic cyanobacteria limited N fixation rate of P. schreberi at the early stage of secondary succession. Rousk et al. (2014a) studied the effects of N deposition on the N-fixing ability of P. schreberi in the coniferous forests of northern Sweden, and showed that the acetylene reduction after N deprivation was positively related to cyanobacterial colonization (r = 0.94; P < 0.001). Another study conducted in the coastal temperate rain forest of North America demonstrated a significant positive correlation between the N fixation rate and the total number of cyanobacteria (R 2 = 0.268; P < 0.001) (Lindo and Whiteley, 2011). ...
Water changes are predicted to regulate physiological activities of bryophytes characterized by poikilohydric gametophytes. In montane forest ecosystems, nitrogen(N)–fixing bryophyte–cyanobacteria associations are main N resources. The aim of this study was to assess how bryophyte–associated microbiomes and their nitrogenase activity response to instant or long-term water content changes. We investigated the cyanobacterial colonization and nitrogenase activity of four epiphytic bryophyte species in a subtropical montane cloud forest during the dry and rainy seasons in Ailao Mountains, Yunnan, southwestern China. We also evaluated the nitrogenase activity of bryophyte–cyanobacteria associations in response to different water contents in laboratory experiment. The degree of cyanobacterial colonization was evaluated using ultraviolet fluorescence microscopy, and nitrogenase activity of bryophyte–cyanobacteria associations were measured using the acetylene reduction assay (ARA). Cyanobacteria showed an association with all four bryophyte species, with 1.04–3.37% area colonized of the shoot and 10.16–20.21 nmol C2H4·g⁻¹·h⁻¹ average nitrogenase activity. Nitrogenase activity was positively related to cyanobacterial colonization (R = 0.742; P = 0.0349). The relationship between water content and nitrogenase activity was unimodal, and both water surplus and shortage inhibited N fixation. Furthermore, long–term drought conditions reduced the degree of cyanobacteria colonization on bryophyte shoots, resulting in decreased nitrogenase activity in the dry season. These results indicate that different response strategies of N fixation operate in bryophyte–cyanobacteria associations to cope with instant and long–term changes in water availability. Our data suggest that both extreme precipitation and drought have a negative impact on N fixation of cyanobacteria–bryophyte associations.
... These phototrophic diazotrophs provide N to their host in exchange for C compounds (Bay et al., 2013;Leppänen et al., 2013), a process that we refer to as a direct mutualism, with reference to the direct transfer of chemicals between host and symbiont (Ho and Bodelier, 2015). In these moss symbioses, as well as in vascular plant symbioses, application of high rates of inorganic N were found to decrease N 2 fixation rates, with the host plant shifting to the use of this readily available inorganic N source (Gundale et al., 2011;Zackrisson et al., 2004;Rousk et al., 2014). There may also be a different, indirect type of interaction in which Sphagnum receives a flow of nutrients from dead and lysed microorganisms. ...
... This is on the same order of magnitude as the range of 12-25 kg ha −1 y −1 reported for pristine boreal bogs, although their growing season only lasts 140 days per year (Vile et al., 2014). Furthermore, similar to Markham (2009), we found Sphagnum-associated N 2 fixation rates to be at least 5 times higher than those found in feather mosses, which are around 1.5-3 kg ha −1 yr −1 (Rousk et al., 2014;DeLuca et al., 2002;Zackrisson et al., 2009;Leppänen et al., 2013). This could be due to morphological differences between the moss species (including hyaline cells of Sphagnum providing additional space and protection to microorganisms) and differences in microbial communities resulting from differences in habitat conditions and resources, i.e., availability of inorganic and organic nitrogen and carbon compounds, moisture content and presence of oxygen. ...
In pristine Sphagnum-dominated peatlands, (di)nitrogen (N2)
fixing (diazotrophic) microbial communities associated with Sphagnum
mosses contribute substantially to the total nitrogen input, increasing
carbon sequestration. The rates of symbiotic nitrogen fixation reported for
Sphagnum peatlands, are, however, highly variable, and experimental
work on regulating factors that can mechanistically explain this variation is
largely lacking. For two common fen species (Sphagnum palustre and
S. squarrosum) from a high nitrogen deposition area
(25 kg N ha−1 yr−1), we found that diazotrophic activity (as
measured by 15 − 15N2 labeling) was still present at a rate of
40 nmol N gDW−1 h−1. This was surprising, given that nitrogen
fixation is a costly process. We tested the effects of phosphorus
availability and buffering capacity by bicarbonate-rich water, mimicking a
field situation in fens with stronger groundwater or surface water influence,
as potential regulators of nitrogen fixation rates and Sphagnum
performance. We expected that the addition of phosphorus, being a limiting
nutrient, would stimulate both diazotrophic activity and Sphagnum
growth. We indeed found that nitrogen fixation rates were doubled. Plant
performance, in contrast, did not increase. Raised bicarbonate levels also
enhanced nitrogen fixation, but had a strong negative impact on
Sphagnum performance. These results explain the higher nitrogen
fixation rates reported for minerotrophic and more nutrient-rich peatlands.
In addition, nitrogen fixation was found to strongly depend on light, with
rates 10 times higher in light conditions suggesting high reliance on
phototrophic organisms for carbon. The contrasting effects of phosphorus and
bicarbonate on Sphagnum spp. and their diazotrophic communities
reveal strong differences in the optimal niche for both partners with respect
to conditions and resources. This suggests a trade-off for the symbiosis of
nitrogen fixing microorganisms with their Sphagnum hosts, in which a
sheltered environment apparently outweighs the less favorable environmental
conditions. We conclude that microbial activity is still nitrogen limited
under eutrophic conditions because dissolved nitrogen is being monopolized by
Sphagnum. Moreover, the fact that diazotrophic activity can
significantly be upregulated by increased phosphorus addition and acid
buffering, while Sphagnum spp. do not benefit, reveals remarkable
differences in optimal conditions for both symbiotic partners and calls into
question the regulation of nitrogen fixation by Sphagnum under these
eutrophic conditions. The high nitrogen fixation rates result in high
additional nitrogen loading of 6 kg ha−1 yr−1 on top of the
high nitrogen deposition in these ecosystems.
... It has been shown that N 2 fixation rates in H. splendens and P. schreberi commonly decreases with increasing N deposition (Rousk et al. 2023), and can be suppressed at N deposition rates as low as 3 kg ha − 1 year − 1 (Salemaa et al., 2019). However, N 2 fixation on mosses can recover from N stress after removal of the stressor (Rousk et al., 2014a;Wang et al., 2022). ...
... Nodulation and N fixation are adversely affected by the addition of NO 3 À or NH 4 + fertilizers (Zahran 1999). Addition of 10 kg N ha À1 depressed acetylene reduction in feather moss (Rousk et al. 2014). Inorganic N addition tends to stimulate nitrogenase activity in cowpea at the vegetative stage (Hassan 2017). ...
Climate has a substantial impact on human health, livelihood, food, and infrastructure. However, rapid shifts in climatic conditions threaten the survival of all living creatures. The current abnormalities in precipitation and temperature are leading to nonprofitable agricultural production, food insecurity, and depletion of natural genetic resources. The changing trends towards diversified diets have posed greater challenges for producers in meeting the consumers’ demands, necessitating a consistent and reliable food supply. Unfortunately, the current scenario of climatic variation has made it hard to put enough food on the table. Because of flooding, droughts, and salinity stress, a large number of staple crops and their by-products get wasted. Similarly, low production of cash crops also lowers the import–export values and affects the national economy. A few preventive measures could be taken to address the challenges of climatic irregularities. Examples include the use of elite genotypes, changing harvest dates, sowing either late or early, and cultivating new crops rather than just the usual ones. It is compulsory to test, validate, and devise a climate-resilient cropping system. In contrast, growers must participate in different activities to determine adoption-related barriers and generate alternative options. These approaches will minimize insect pest infestation, prevent diseases, improve soil fertility, increase water use efficiency, and, above all, help in developing defense mechanisms against climate change. The yields of major crops have been declining, so efforts have been put into converting marginal lands into agricultural lands to compensate for this. However, this practice ultimately degrades the land and threatens the existence of biodiversity in both domestic and wild species. This could affect future attempts to address climate risk. Recently, efforts have been made to improve the operating system at farms by modifying the percentage of pesticide and fertilizer usage, their method of application (foliar/ground), the introduction of the sprinkler irrigation technique, and the use of certified seeds to improve both plant growth and soil fertility. By adhering to these practices, farmers are hoping to be able to deal with climatic variations in a significantly more effective manner. In addition, decision-makers establishing appropriate policies and interventions for climate-smart agricultural production approaches and methods must carefully examine the macroeconomic, social, and ecological interventions. At the same time, policies that encourage unsustainable production and aggravate environmental issues must also be abolished. Moreover, more funding for research, notably action research, is required to deal with forthcoming climate-related threats.
... Nodulation and N fixation are adversely affected by the addition of NO 3 À or NH 4 + fertilizers (Zahran 1999). Addition of 10 kg N ha À1 depressed acetylene reduction in feather moss (Rousk et al. 2014). Inorganic N addition tends to stimulate nitrogenase activity in cowpea at the vegetative stage (Hassan 2017). ...
Malnutrition affects about 1.8 billion people worldwide and is significantly attributed to micronutrient deficiencies, notably in developing countries. Humans receive their nutrients mainly from agriculture, but this sector is under pressure due to population growth and reducing arable land areas, especially in developing and underdeveloped regions. These countries are turning to farming practices to boost crop yields and address food and nutrient shortage issues. The vital microelements zinc and iron are required for both plant and human growth, however, it is commonly known that approximately one-third of the world’s population suffers from a shortage of these nutrients. Crops must either have better nutritional properties or be biofortified to counteract micronutrient deficiencies. In order to provide critical nutrients, a number of biofortification projects using conventional breeding, biotechnological, and agronomic approaches have been launched with varying degrees of success, particularly in developing and underdeveloped countries. Utilizing nanoparticle fertilizers is an agronomic biofortification technique to boost crop production and nutrients, soil micronutrient availability, and plant parts assimilation. It is important to use eco-friendly and secure technologies like nanobiofortification to reduce the reliance on large quantities of chemical fertilizers. A viable strategy for enhancing the sustainability of present agricultural methods and for biofortifying food crop production by key micronutrients, resulting in better nutritional quality, is the use of nanoparticles as nano fertilizers. In order to maximize the sustainable application, this chapter evaluates the existing usage of Zn and Fe-NPs for biofortification in various food crops while addressing valuable information gaps and challenges.
... Nodulation and N fixation are adversely affected by the addition of NO 3 À or NH 4 + fertilizers (Zahran 1999). Addition of 10 kg N ha À1 depressed acetylene reduction in feather moss (Rousk et al. 2014). Inorganic N addition tends to stimulate nitrogenase activity in cowpea at the vegetative stage (Hassan 2017). ...
A score of pedo-environmental factors serves as limiting elements for the biological nitrogen fixation (BNF) process in root nodules of leguminous plants. Since the advent of the green revolution, pesticides have been considered indispensable for keeping crop pests below the economic threshold level to ensure sustainable production of field crops for the rapidly increasing world population. However, pesticide application has also been associated with adverse effects on plant growth and development besides causing a detrimental reduction in microbial community dynamics. Rhizobium strains that are host-specific are no exception to this threat and are negatively influenced by different pesticides, especially fungicides, which seriously affect the functioning of the nitrogen (N) fixation process. Pesticides containing different synthetic chemicals affect symbiotic nitrogen fixation (SNF), and consequently, the amount of N fixed. This leads to reliance on crop plants primarily on N available in soil solution. Ultimately, reduced soil fertility leads to deteriorated crop productivity and poor nutritional quality of the produce. The objective of this review has been to synthesize, explore and critically analyze the effects of pesticide applications and their physiological impacts on BNF in legumes for sustainable crop production to strengthen food security for the increasing world population. Our review elucidates that indiscriminate use of agrochemicals could result in an undesirable environment for the healthy survival of symbiotic and symbiotic organisms leading to a corresponding reduction in exopolysaccharide (EPS) synthesis leading to poor atmospheric N fixation and thus affecting the whole agroecosystems. Therefore, by giving due consideration to the harmful effects of pesticides, farmers’ awareness about the safe usage of agrochemicals might be among the top priorities to conserve the environment besides harmonically preserving living organisms.
... Previous studies showed that recovery from high N loads needs a longer time or N needs to be actively removed via e.g. rinsing (Rousk et al. 2014a;Rousk & Michelsen 2016). Therefore, recovery from N loads is possible, if N input remains below a certain threshold. ...
Moss-associated nitrogen (N 2 ) fixation is one of the main inputs of new N in pristine ecosystems that receive low amounts of atmospheric N deposition. Previous studies have shown that N 2 fixation is inhibited by inorganic N (IN) inputs, but if N 2 fixation in mosses is similarly affected by organic N (ON) remains unknown. Here, we assessed N 2 fixation in two dominant mosses in boreal forests ( Pleurozium schreberi and Sphagnum capillifolium ) in response to different levels of N, simulating realistic (up to 4 kg N ha ⁻¹ yr ⁻¹ ) and extreme N deposition rates in pristine ecosystems (up to 20 kg N ha ⁻¹ yr ⁻¹ ) of IN (NH 4 NO 3 ) and ON (alanine and urea). We also assessed if N 2 fixation can recover from the N additions. In the realistic scenario, N 2 fixation was inhibited by increasing NH 4 NO 3 additions in P. schreberi but not in S. capillifolium , and alanine and urea stimulated N 2 fixation in both moss species. In contrast, in the extreme N additions, increasing N inputs inhibited N 2 fixation in both moss species and all N forms. Nitrogen fixation was more sensitive to N inputs in P. schreberi than in S. capillifolium and was higher in the recovery phase after the realistic compared to the extreme N additions. These results demonstrate that N 2 fixation in mosses is less sensitive to organic than inorganic N inputs and highlight the importance of considering different N forms and species-specific responses when estimating the impact of N inputs on ecosystem functions such as moss-associated N 2 fixation.
... The complete elimination of free-living BNF in soil and litter due to increased tropical N deposition, as suggested by Dynarski and Houlton (2018), however, seems unlikely as even after 3 years of adding 125 kg N ha −1 yr −1 BNF remained an active process in both forest sites. Also, in other ecosystems, such as boreal forests (Rousk et al., 2014), the addition of N did not eliminate BNF entirely. While N deposition could potentially replace the loss of N from fixation, the long-term consequences of the suppression of free-living N fixers on terrestrial nutrient cycles and plant productivity remain unknown (Dynarski & Houlton, 2018). ...
In tropical forests, free‐living Biological nitrogen (N) fixation (BNF) in soil and litter tends to decrease when substrate N concentrations increase, whereas increasing phosphorus (P) and molybdenum (Mo) soil and litter concentrations have been shown to stimulate free‐living BNF rates. Yet, very few studies explored the effects of adding N, P, and Mo together in a single large‐scale fertilization experiment, which would teach us which of these elements constrain or limit BNF activities. At two distinct forest sites in French Guiana, we performed a 3‐year in situ nutrient addition study to explore the effects of N, P, and Mo additions on leaf litter and soil BNF. Additionally, we conducted a short‐term laboratory study with the same nutrient addition treatments (+N, +N+P, +P, +Mo, and +P+Mo). We found that N additions alone suppressed litter free‐living BNF in the field, but not in the short‐term laboratory study, while litter free‐living BNF remained unchanged in response to N+P additions. Additionally, we found that P and P+Mo additions stimulated BNF in leaf litter, both in the field and in the lab, while Mo alone yielded no changes. Soil BNF increased with P and P+Mo additions in only one of the field sites, while in the other site soil BNF increased with Mo and P+Mo additions. We concluded that increased substrate N concentrations suppress BNF. Moreover, both P and Mo have the potential to limit free‐living BNF in these tropical forests, but the balance between P versus Mo limitation is determined by site‐specific characteristics of nutrient supply and demand.
... Lower N 2 fixation rates in nostocalean cyanobacteria are a known consequence of higher ammonium availability, triggering a negative feedback for the differentiation of vegetative cells into heterocytes (Flores et al., 2019). This can also be observed in moss-associated communities under both field and laboratory conditions, which can, however, recover their previous rates once N becomes a limiting factor again (Rousk et al., 2014b;Rousk and Michelsen, 2016). ...
Mosses can be responsible for up to 100% of net primary production in arctic and subarctic tundra, and their associations with diazotrophic cyanobacteria have an important role in increasing nitrogen (N) availability in these pristine ecosystems. Predictions about the consequences of climate change in subarctic environments point to increased N mineralization in soil and higher litter deposition due to warming. It is not clear yet how these indirect climate change effects impact moss-cyanobacteria associations and N2 fixation. This work aimed to evaluate the effects of increased N and litter input on biological N2 fixation rates associated with the feathermoss Hylocomium splendens from a tundra heath. H. splendens samples were collected near Abisko, northern Sweden, from a field experiment with annual additions of ammonium chloride and dried birch litter and the combination of both for three years. Samples were analyzed for N2 fixation, cyanobacterial colonization, C and N content and pH. Despite the high N additions, no significant differences in moss N content were found. However, differences between treatments were observed in N2 fixation rates, cyanobacterial colonization and pH, with the combined ammonium+litter treatment causing a significant reduction in the number of branch-colonizing cyanobacteria and N2 fixation, and ammonium additions significantly lowering moss pH. A significant, positive relationship was found between N2 fixation rates, moss colonization by cyanobacteria and pH levels, showing a clear drop in N2 fixation rates at lower pH levels even if larger cyanobacterial populations were present. These results suggest that increased N availability and litter deposition resulting from climate change not only interferes with N2 fixation directly, but also acidifies moss microhabitats and reduces the abundance of associated cyanobacteria, which could eventually impact the N cycle in the Subarctic.
... On the contrary, total N in mosses decreased with increasing distance from the metal source of pollution. Yet, again, the effects of N on N 2 fixation depends on the level of N deposited (Rousk et al. 2014;Rousk and Michelsen 2016), and may have not been high enough along our study sites. The higher moss-N content in samples closest to the metal source of pollution could also reflect higher N 2 fixation activity by colonizing cyanobacteria, fuelled by higher Fe availability. ...
Nitrogen (N 2) fixation by moss-associated cyanobacteria is one of the main sources of new N input in pristine ecosystems such as boreal forests and arctic tundra. Given the non-vascular physiology of mosses, they are especially sensitive to e.g. increased N input and heavy metal deposition. While the effects of increased N input on moss-associated N 2 fixation has been comprehensively assessed, hardly any reports exist on the effects of increased heavy metal load on this key ecosystem function. To address this knowledge gap, we made use of an extreme metal pollution gradient in boreal forests of Northern Sweden originating from a metal mine and its associated smelters. We collected the common moss Pleurozium schreberi, known to host cyanobacteria, along a distance gradient away from the metal source of pollution and measured moss-metal content (Fe, Cu, Zn, Pb) as well as N 2 fixation. We found a strong distance gradient in moss-metal content for all investigated metals: a sharp decline in metal content with distance away from the metal pollution source. However, we found a similarly steep gradient in moss-associated N 2 fixation, with highest activity closest to the metal source of pollution. Hence, while mosses may be sensitive to increased heavy metal inputs, the activity of colonising cyanobacteria seem to be unaffected by heavy metals, and consequently, ecosystem function may not be compromised by elevated metal input.
... Nonetheless, decreases in N 2 fixation rates at N loadings above 3.1 kg NÁha À1 Áyr À1 are indicative of a suppression of biological N 2 fixation with increasing N addition. Inhibition of N 2 fixation by high N availability and/or deposition has been demonstrated in boreal feathermosses (Pleurozium schreberi and Hylocomium splendens) where the N 2 fixers are predominantly cyanobacteria (Gundale et al. 2011, Ackermann et al. 2012, Rousk et al. 2014) and in Sphagnum mosses, where the N 2 fixers may be predominantly methanotrophs (Vile et al. 2014, Kox et al. 2016). The inhibition of N 2 fixation that we observed at Mariana Lake Bog is nearly equivalent to the increase in N loading through experimental N addition. ...
Bogs and fens cover 6% and 21%, respectively, of the 140,329 km² Oil Sands Administrative Area in northern Alberta. Development of the oil sands has led to increasing atmospheric N deposition, with values as high as 17 kg N·ha⁻¹·yr⁻¹; regional background deposition is <2 kg N·ha⁻¹·yr⁻¹. Bogs, being ombrotrophic, may be especially susceptible to increasing N deposition. To examine responses to N deposition, over five years, we experimentally applied N (as NH4NO3) to a bog near Mariana Lake, Alberta, unaffected by oil sands activities, at rates of 0, 5, 10, 15, 20, and 25 kg N·ha⁻¹·yr⁻¹, plus controls (no water or N addition). Increasing N addition: (1) stimulated N2 fixation at deposition <3.1 kg N·ha⁻¹·yr⁻¹, and progressively inhibited N2 fixation as N deposition increased above this level; (2) had no effect on Sphagnum fuscum net primary production (NPP) in years 1, 2, and 4, but inhibited S. fuscum NPP in years 3 and 5; (3) stimulated dominant shrub and Picea mariana NPP; (4) led to increased root biomass and production; (5) changed Sphagnum species relative abundance (decrease in S. fuscum, increase in S. magellanicum, no effect on S. angustifolium); (6) led to increasing abundance of Rhododendron groenlandicum and Andromeda polifolia, and to vascular plants in general; (7) led to increasing shrub leaf N concentrations in Andromeda polifolia, Chamaedaphne calyculata, Vaccinium oxycoccos, V. vitis‐idaea, and Picea mariana; (8) stimulated cellulose decomposition, with no effect on S. fuscum peat or mixed vascular plant litter decomposition; (9) had no effect on net N mineralization rates or on porewater NH4⁺‐N, NO3⁻‐N, or DON concentrations; and (10) had minimal effects on peat microbial community composition. Increasing experimental N addition led to a switch from new N being taken up primarily by Sphagnum to being taken up primarily by shrubs. As shrub growth and cover increase, Sphagnum abundance and NPP decrease. Because inhibition of N2 fixation by increasing N deposition plays a key role in bog structural and functional responses, we recommend a N deposition critical load of 3 kg N·ha⁻¹·yr⁻¹ for northern Alberta bogs.
... or when N inputs do not exceed demands(Rousk, Jones, DeLuca, 2014). Another type of nutrient is phosphorus (P; e.g., P fertilizer and 88 deposited P), which often enhances BNF due to the importance of this nutrient to cell 89 metabolism(Burns & Hardy, 1975). ...
Biological nitrogen (N) fixation (BNF), an important source of N in terrestrial ecosystems, plays a critical role in terrestrial nutrient cycling and net primary productivity. Currently, large uncertainty exists regarding how nutrient availability regulates terrestrial BNF and the drivers responsible for this process. We conducted a global meta‐analysis of terrestrial BNF in response to N, phosphorus (P), and micronutrient (Micro) addition across different biomes (i.e., tropical/subtropical forest, savanna, temperate forest, grassland, boreal forest, and tundra) and explored whether the BNF responses were affected by fertilization regimes (nutrient‐addition rates, duration, and total load) and environmental factors (mean annual temperature (MAT), mean annual precipitation (MAP), and N deposition). The results showed that N addition inhibited terrestrial BNF (by 19.0% [95% confidence interval (CI): 17.7–20.3%]; hereafter), Micro addition stimulated terrestrial BNF (30.4% [25.7–35.3%]), and P addition had an inconsistent effect on terrestrial BNF (i.e., inhibiting free‐living N fixation (7.5% [4.4–10.6%]) and stimulating symbiotic N fixation (85.5% [25.8–158.7%])). Furthermore, the response ratios (i.e., effect sizes) of BNF to nutrient addition were smaller in low‐latitude (<30°) biomes (8.5–36.9%) than in mid‐/high‐latitude (≥30°) biomes (32.9–61.3%), and the sensitivity (defined as the absolute value of response ratios) of BNF to nutrients in mid‐/high‐latitude biomes decreased with decreasing latitude (p≤0.009; linear/logarithmic regression models). Fertilization regimes did not affect this phenomenon (p>0.05), but environmental factors did affect it (p<0.001) because MAT, MAP, and N deposition accounted for 5–14%, 10–32%, and 7–18% of the variance in the BNF response ratios in cold (MAT<15°C), low‐rainfall (MAP<2500 mm), and low‐N‐deposition (<7 kg ha−1 yr−1) biomes, respectively. Overall, our meta‐analysis depicts a global pattern of nutrient impacts on terrestrial BNF and indicates that certain types of global change (i.e., warming, elevated precipitation and N deposition) may reduce the sensitivity of BNF in response to nutrient enrichment in mid‐/high‐latitude biomes. This article is protected by copyright. All rights reserved.
... Several studies have demonstrated incomplete downregulation of the N 2 -fixation activity at sites receiving elevated amounts of anthropogenic N r (Kox et al., 2016;Larmola et al., 2014;Rousk & Michelsen, 2016;Rousk, Jones, & DeLuca, 2014;van den Elzen et al., 2017van den Elzen et al., , 2018. We are not aware of any study thus far that has focused on N inventories in vertical peat profiles through polluted peatlands. ...
Microbial N2‐fixation helps to sustain carbon accumulation in pristine peatlands and to remove CO2 from the atmosphere. Recent work in minerotrophic fens has provided evidence that this energetically costly process is not completely downregulated at sites with higher availability of reactive nitrogen (Nr). We suggest that biological N2‐fixation also contributes to the N soil reservoir in rain‐fed, atmospherically polluted peat bogs of Central Europe. At five sites, receiving up to 21 kg Nr ha⁻¹ yr⁻¹, we compared total N accumulation in peat and cumulative Nr deposition since 1950 and 1900. We took advantage of detailed inventories of historical NH4⁺ and NO3‐ emissions, and quantified the role of horizontal Nr deposition via fog interception and dry deposition. Eleven peat cores were ²¹⁰Pb‐dated. At all sites, the amount of N accumulated in peat exceeded the cumulative atmospheric Nr input. At one site in the industrially polluted north of the Czech Republic, atmospheric Nr input explained only 41% of N accumulation in peat. We concluded that the “excess” N in peat was partly a result of N2‐fixation, which subsequently was supported by ¹⁵N/¹⁴N isotope systematics. The δ¹⁵N values of Sphagnum (mean of ‐4.2 ‰) were higher than the δ¹⁵N values of deposited NH4⁺ and NO3‐ (mean of ‐12.3 ‰), converging to the δ¹⁵N value of atmospheric N2 (0.0 ‰) as an alternative N source. These two lines of indirect evidence for N2‐fixation were corroborated by direct measurements of N2‐fixation rates using a ¹⁵N2 labelling assay. During laboratory incubation, δ¹⁵N values of Sphagnum significantly increased, but could explain only part of the “excess” N in peat. Our findings indicate that biological N2‐fixation should be given greater consideration as an input of N not only to pristine peatlands, but also to peatlands located in polluted regions of the globe.
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... The absence of an N loading effect on net total N accumulation in the mesocosms could be a reflection of a down regulation of moss-associated biological N 2 -fixation with increased N loading (cf. Gundale et al. 2011;Ackermann et al. 2012;Rousk et al. 2014;Vile et al. 2014;Kox et al. 2016), although we were unable to discern a statistically significant effect of N loading on the unaccounted N source in the mesocosms (Table 2). Nonetheless, in locations where N 2 fixation represents the dominant source of new N to Sphagnum-dominated bogs, as in northern Alberta, increasing atmospheric N deposition may have a minimal effect on overall net N accumulation in peat. ...
To evaluate the effects of increasing atmospheric N deposition on net C and N accumulation in Sphagnum-dominated bogs, we conducted a laboratory mesocosm experiment. Following 45 days of watering with N-free rainwater, mesocosms were exposed to simulated atmospheric N deposition values of 0, 4.14, 8.18, and 12.42 mg N m⁻² da⁻¹ over a 108 day period. We quantified N retention from leachate N concentrations and from changes in N contents of the Sphagnum/peat mesocosms. As N loading of simulated atmospheric N deposition increased, so did the net retention of simulated atmospherically deposited N. Our hypothesis of a decrease in N retention efficiency with increasing N loading was not observed. Further, for each N loading treatment, rates of retention of simulated atmospherically deposited N remained constant over time. We did not observe a threshold N deposition below which N would be retained in mesocosms and above which N passed through the mesocosms. Substantially more N was retained in mesocosms that was added in simulated atmospheric N deposition, suggesting an unaccounted for N source, most likely biological N2 fixation. In locations where N2 fixation represents a much greater source of new N to Sphagnum-dominated bogs, as in northern Alberta, Canada, increasing atmospheric N deposition may have a minimal effect on overall net N accumulation in peat.
... Thus, most studies have found that an increase in nitrogen would reduce the richness and diversity of diazotrophs. (Zhang et al., 2013;Rousk et al., 2014). However, some studies found that the nitrogen addition increased, rather than decreased, the diversity of diazotrophs Ning et al., 2015). ...
Nitrogen is a macronutrient which plays an important role in the net primary productivity of terrestrial ecosystems, and is critical to understand how nitrogen addition affects above- and below-ground organisms. However, direct and indirect interactions between microbial species response to nitrogen addition for wheat growth are still unclear. In this study, arbuscular mycorrhizal fungi (AMF) and diazotrophs (nifH gene) were selected as two groups of key functional microbes in wheat soil to investigate the comprehensive impact of diversity and community structures between them on wheat yield under a nitrogen gradient. Nitrogen addition resulted in a significant shift in AMF and nifH phylogenetic diversity and community structure. The interactions among AMF and nifH species were diminished in high N-treated soils compared to those in low N-treated soils. Structural equation model analysis showed that AMF community structure affected wheat yield directly, however, which was influenced by AMF diversity, diazotrophic diversity and community structure indirectly. The comprehensive effects of AMF and diazotrophs on wheat productivity indicated the importance of soil functional microbes as drivers for farmland ecosystem and plant growth. These results could be useful in understanding soil nutrient cycling and may help improve the mechanistic understanding of the tripartite interaction among nitrogen addition, microbes and wheat productivity.
... Thus, most studies have found that an increase in nitrogen would reduce the richness and diversity of diazotrophs. ( Zhang et al., 2013;Rousk et al., 2014). However, some studies found that the nitrogen addition increased, rather than decreased, the diversity of diazotrophs ( Huang et al., 2016;Ning et al., 2015). ...
... In addition, our findings of widely suppressive effects of N additions on free-living N fixation suggest that increases in anthropogenic N deposition could reduce or eliminate this key microbial functional group from ecosystems. N fixation by mossassociated cyanobacteria has previously been shown to decline in response to anthropogenic N deposition, although N fixation recovers when N deposition ceases (Rousk et al., 2013). While N deposition could replace the loss of N from fixation, the longterm consequences of the loss of free-living N-fixers on terrestrial nutrient cycles and plant productivity remain unknown. ...
Nitrogen (N) fixation by free‐living bacteria is a primary N input pathway in many ecosystems and sustains global plant productivity. Uncertainty exists over the importance of N, phosphorus (P) and molybdenum (Mo) availability in controlling free‐living N fixation rates. Here, we investigate the geographic occurrence and variability of nutrient constraints to free‐living N fixation in the terrestrial biosphere.
We compiled data from studies measuring free‐living N fixation in response to N, P and Mo fertilizers. We used meta‐analysis to quantitatively determine the extent to which N, P and Mo stimulate or suppress N fixation, and if environmental variables influence the degree of nutrient limitation of N fixation.
Across our compiled dataset, free‐living N fixation is suppressed by N fertilization and stimulated by Mo fertilization. Additionally, free‐living N fixation is stimulated by P additions in tropical forests.
These findings suggest that nutrient limitation is an intrinsic property of the biochemical demands of N fixation, constraining free‐living N fixation in the terrestrial biosphere. These findings have implications for understanding the causes and consequences of N limitation in coupled nutrient cycles, as well as modeling and forecasting nutrient controls over carbon–climate feedbacks.
... Surprisingly, given the theoretical suppression of N 2 fixation by high N availability, we found no effect of the N deposition load of 32 kg ha −1 y −1 in either form in any of the moss species. Similar results were found in short-term N addition experiments for Sphagnum magellanicum from a low N deposition (b0.5 kg N ha −1 y −1 ) site with addition of 200 kg N ha − 1 y − 1 (Kox et al., 2016) and in Pleurozium schreberi with N additions b 10 kg ha −1 y −1 (Rousk et al., 2014). Longterm field studies in boreal forests showed no difference in N 2 fixation rates of Pleurozium schreberi for N deposition loads between 3 and 12 kg ha − 1 y − 1 (Gundale et al., 2011), but higher N 2 fixation rates were found at N deposition loads between 0 and 3 kg ha − 1 y − 1 (Gundale et al., 2011;Leppänen et al., 2013). ...
Pristine bogs, peatlands in which vegetation is exclusively fed by rainwater (ombrotrophic), typically have a low atmospheric deposition of reactive nitrogen (N) (<0.5kgha(-1)y(-1)). An important additional N source is N2 fixation by symbiotic microorganisms (diazotrophs) in peat and mosses. Although the effects of increased total airborne N by anthropogenic emissions on bog vegetation are well documented, the important question remains how different N forms (ammonium, NH4(+), versus nitrate, NO3(-)) affect N cycling, as their relative contribution to the total load strongly varies among regions globally. Here, we studied the effects of 11years of experimentally increased deposition (32 versus 8kgNha(-1)y(-1)) of either NH4(+) or NO3(-) on N accumulation in three moss and one lichen species (Sphagnum capillifolium, S. papillosum, Pleurozium schreberi and Cladonia portentosa), N2 fixation rates of their symbionts, and potential N losses to peat soil and atmosphere, in a bog in Scotland. Increased input of both N forms led to 15-90% increase in N content for all moss species, without affecting their cover. The keystone species S. capillifolium showed 4 times higher N allocation into free amino acids, indicating N stress, but only in response to increased NH4(+). In contrast, NO3(-) addition resulted in enhanced peat N mineralization linked to microbial NO3(-) reduction, increasing soil pH, N concentrations and N losses via denitrification. Unexpectedly, increased deposition from 8 to 32kgha(-1)y(-1) in both N forms did not affect N2 fixation rates for any of the moss species and corresponded to an additional input of 5kgNha(-1)y(-1) with a 100% S. capillifolium cover. Since both N forms clearly show differential effects on living Sphagnum and biogeochemical processes in the underlying peat, N form should be included in the assessment of the effects of N pollution on peatlands.
... In addition to the dependence of BNF and diazotroph (N 2fixing bacteria) abundance on nutrient input and availability (Rousk et al., 2014b), moss-associated BNF shows a strong dependence on moisture and temperature, which fluctuate significantly throughout the growing season . Thus, it is crucial to test whether P and Mo limitation of BNF shift temporally to affect ecosystem productivity. ...
Biological nitrogen fixation ( BNF ) performed by moss‐associated cyanobacteria is one of the main sources of new nitrogen (N) input in pristine, high‐latitude ecosystems. Yet, the nutrients that limit BNF remain elusive. Here, we tested whether this important ecosystem function is limited by the availability of molybdenum (Mo), phosphorus (P), or both.
BNF in dominant mosses was measured with the acetylene reduction assay ( ARA ) at different time intervals following Mo and P additions, in both laboratory microcosms with mosses from a boreal spruce forest and field plots in subarctic tundra. We further used a ¹⁵ N 2 tracer technique to assess the ARA to N 2 fixation conversion ratios at our subarctic site.
BNF was up to four‐fold higher shortly after the addition of Mo, in both the laboratory and field experiments. A similar positive response to Mo was found in moss colonizing cyanobacterial biomass. As the growing season progressed, nitrogenase activity became progressively more P limited. The ARA : ¹⁵ N 2 ratios increased with increasing Mo additions.
These findings show that N 2 fixation activity as well as cyanobacterial biomass in dominant feather mosses from boreal forests and subarctic tundra are limited by Mo availability.
... Ethylene generated in the headspace by the cyanobacterial nitrogenase enzyme was measured by gas chromatography equipped with a flame ionization detector (Varian, Santa Clara, USA) using an automatic headspace sampler (Quma, Wuppertal, Germany). Data are represented as cumulative AR in nmol g −1 DW, as total AR in μmol m −2 or as AR rates in μmol m −2 h −1 where 10 moss shoots of P. schreberi represent an area of 2.8 cm 2 (Rousk et al. 2013). ...
Background and aims
Nitrogen (N2) fixation in feather moss-cyanobacteria associations is a major source of N for boreal ecosystems. However, mosses experience significant shifts in their moisture status due to daily and yearly fluctuations in sunlight, temperature and precipitation. While the effects of drying and rewetting on nutrient leaching and photosynthesis in mosses have been studied, no attempt has been made to assess the consequences for N2 fixation in feather mosses.
Methods
We conducted an experiment in which we dried (3 day at 28 °C; <9 % of field moisture) and rewetted samples of the feather moss Pleurozium schreberi (Brid.) Mitt. that is colonized by N2-fixing-cyanobacteria to assess the influence on N2 fixation. Further, we tested how long it takes for N2 fixation to recover from a drying-rewetting cycle. In addition, we assessed how N2 fixation changes with incubation time with acetylene (2–65 h).
Results
A drying period of 3 days almost completely eliminated N2 fixation (<0.2 μmol m−2 h−1) in the moss. However, rates slowly recovered after rewetting, reaching N2 fixation levels of moist (non-water stressed) moss 5 days after rewetting. Nitrogen fixation increased significantly with incubation time with acetylene (0 μmol m−2 h−1 at 2 h vs. 26 μmol m−2 h−1 at 65 h incubation).
Conclusions
Although N2 fixation recommenced upon rewetting, the recovery was slow. Thus, recurrent drying and rewetting cycles could reduce total N2 fixation in moss-cyanobacteria associations over time, leading to reduced total N input to the system.
Climate change is resulting in accelerated retreat of glaciers worldwide and much nitrogen-poor debris is left after glacier retreats. Asymbiotic dinitrogen (N2) fixation (ANF) can be considered a 'hidden' source of nitrogen (N) for non-nodulating plants in N limited environments; however, seasonal variation and its relative importance in ecosystem N budgets, especially when compared with nodulating symbiotic N2-fixation (SNF), is not well-understood. In this study, seasonal and successional variations in nodulating SNF and non-nodulating ANF rates (nitrogenase activity) were compared along a glacial retreat chronosequence on the eastern edge of the Tibetan Plateau. Key factors regulating the N2-fixation rates as well as the contribution of ANF and SNF to ecosystem N budget were also examined. Significantly greater nitrogenase activity was observed in nodulating species (0.4-17,820.8 umol C2H4 g-1 d-1) compared to non-nodulating species (0.0-9.9 umol C2H4 g-1 d-1) and both peaked in June or July. Seasonal variation in acetylene reduction activity (ARA) rate in plant nodules (nodulating species) and roots (non-nodulating species) was correlated with soil temperature and moisture while ARA in non-nodulating leaves and twigs was correlated with air temperature and humidity. Stand age was not found to be a significant determinant of ARA rates in nodulating or non-nodulating plants. ANF and SNF contributed 0.3-51.5 % and 10.1-77.8 %, respectively, of total ecosystem N input in the successional chronosequence. In this instance, ANF exhibited an increasing trend with successional age while SNF increased only at stages younger than 29 yr and then decreased as succession proceeded. These findings help improve our understanding of ANF activity in non-nodulating plants and N budgets in post glacial primary succession.
Purpose : Old-growth forests in the Pacific Northwest host a variety of epiphytes on their branches and stem. Given the common and often large epiphytic biomass associated with Acer macrophyllum (Pursh ) in this region, we evaluated how seasonal weather changes and urbanization (metal and nitrogen deposition), affect canopy epiphytic N2 fixation in the Hoh Rainforest of the Olympic Peninsula and in urban parks and forests in Seattle.
Methods : We collected Isothecium stoloniferum (Brid.) samples from both the Hoh Rainforest and Seattle at four periods from April 2016 through January 2017. Moss-associated N2 fixation rates were measured in the laboratory using the acetylene reduction assay and trace metal concentrations in the moss were analyzed using NO3 + H2O2 digestion.
Results : We found levels of N2 fixation were highest during the spring sampling period. Elevated levels of heavy metals were observed in I. stoloniferum samples collected in the urban canopies in Seattle, suggesting N2 fixation is sensitive to the bioaccumulation of heavy metals. In A. macrophyllum canopies, I. stoloniferum was found to yield 1.13 kg N ha⁻¹ yr⁻¹ in the Hoh Rainforest and only 0.009 kg N ha⁻¹ yr⁻¹ in Seattle.
Conclusions : These results highlight a rarely explored source of biological N2-fixation in temperate rainforests and suggest that epiphytic N2-fixation may contribute bio-available nitrogen in secondary successional A. macrophyllum stands.
AimsWe investigated N2-fixation by moss-cyanobacterial associations in a North American prairie ecosystem, identifying cyanobacteria associated with moss species, and evaluating spatio-temporal dynamics in N2-fixation rates.Methods
We confirmed the presence and abundance of N2-fixing cyanobacteria on three moss species (Pleurozium schreberi (Brid.) Mitt., Racomitrium elongatum Frisvoll, Rhytidiadelphus triquetrus (Hedw) Warnst.) using epi-fluorescence light microscopy. To estimate monthly N2-fixation rates on mosses from three sites, we conducted laboratory-based acetylene reduction assays with constant incubation temperatures and natural daylight. We evaluated the relationship between daylength and N2-fixation, and daylength and weather variables.ResultsN2-fixation rates varied by species, site, and month. R. elongatum exhibited the highest rates and P. schreberi had the lowest. Rates for R. elongatum and R. triquetrus were positively correlated with daylength, with peaks occurring at 13–14 h daylight, suggesting spring and fall conditions support N2-fixation in this system. Annual median N2-fixation for R. elongatum and R. triquetrus ranged from 0.008–0.124 kg N ha−1 yr−1 based on cover of 11–100%.Conclusions
Our results highlight a previously undescribed source of biological N2-fixation in temperate grasslands. Changes in the distribution or activity of N2-fixing moss-cyanobacterial associations due to management practices and climate change could impact future stand-level nitrogen dynamics.
Symbiosis is the ‘living together’ of two or more organisms, often involving specialized structures. In its broadest sense, symbiotic associations include parasitic and commensal as well as mutually beneficial partnerships. It is common in the ecophysiological literature, however, to use the term symbiosis in a narrow sense to refer to mutually beneficial associations between plants and microorganisms. Mutual benefits may not always be easy to determine, particularly for the microsymbiont. In this chapter, benefits for the macrosymbiont (‘host’) are often expressed in terms of amount of accumulated biomass or acquired resources. In an ecological context, benefits in terms of ‘fitness’ may be more relevant, but these are rarely documented. In the mutually beneficial associations we discuss in this chapter, nutrients or specific products of the partners are shared between two or three partners; the macrosymbiont and the microsymbiont(s). Parasitic associations between plants are dealt with in Chap. 10.1007/978-3-030-29639-1_15; parasitic associations between microorganisms and plants are discussed briefly in this chapter, and more elaborately in Chap. 10.1007/978-3-030-29639-1_14.
Epilithic mosses (EM) and organic substrates (OS) constitute a special ecosystem developing on rocks and a critical interface regulating rock-atmosphere interactions and biological weathering. Carbon (C) and nitrogen (N) are critical elements influencing biotic-abiotic interactions in EM-OS systems. However, the dynamics of C and N in EM-OS systems and their differences among rock types remain unclear. This study investigated contents ([C], [N]) of C and N and their isotope compositions (δ¹³C, δ¹⁵N) in EM and OS layers on limestones and sandstones in Huanjiang karst observatory of Guangxi, China. Significant higher [C]EM (by ca. 5.0%) and lower δ¹³CEM values (by ca. 3.0‰) on sandstones than on limestones might reflect a lower water use efficiency in mosses on sandstones. Differences in δ¹³C values between EM and OS correlated positively with those in C contents, elucidating increasing ¹³C discriminations with the C decomposition in substrates. The δ¹⁵NEM and δ¹⁵NOS values were correlated positively, indicating mosses as a major contributor of organic N in OS. The [N]EM did not differ between two rock types, but significant lower [N]OS and higher δ¹⁵NOS values (by ca. 0.2% and 1.5‰, respectively) occurred on limestones than on sandstones, suggesting larger N losses and ¹⁵N enrichments in OS on limestones. These results underscore that elemental and isotopic signatures can elucidate different C and N dynamics in the EM-OS ecosystems as a function of rock types.
Biological fixation of atmospheric nitrogen (N2) by bryophyte-associated cyanobacteria is an important source of plant-available N in the boreal biome. Information on the factors that drive biological N2 fixation (BNF) rates is needed in order to understand the N dynamics of forests under a changing climate. We assessed the potential of several cryptogam species (the feather mosses Hylocomium splendens and Pleurozium schreberi, a group of Dicranum bryophytes, two liverworts, and Cladina lichens) to serve as associates of cyanobacteria or other N2-fixing bacteria (diazotrophs) using acetylene reduction assay (ARA). We tested the hypotheses that the legacy of chronic atmospheric N deposition reduces BNF in the three bryophyte species, sampled from 12 coniferous forests located at latitudes 60–68° N in Finland. In addition, we tested the effect of moisture and temperature on BNF. All species studied showed a BNF signal in the north, with the highest rates in feather mosses. In moss samples taken along the north–south gradient with an increasing N bulk deposition from 0.8 to 4.4 kg ha⁻¹ year⁻¹, we found a clear decrease in BNF in both feather mosses and Dicranum group. BNF turned off at N deposition of 3–4 kg ha⁻¹ year⁻¹. Inorganic N (NH4-N + NO3-N) best predicted the BNF rate among regression models with different forms of N deposition as explanatory variables. However, in southern spruce stands, tree canopies modified the N in throughfall so that dissolved organic N (DON) leached from canopies compensated for inorganic N retained therein. Here, both DON and inorganic N negatively affected BNF in H. splendens. In laboratory experiments, BNF increased with increasing temperature and moisture. Our results suggest that even relatively low N deposition suppresses BNF in bryophyte-associated diazotrophs. Further, BNF could increase in northern low-deposition areas, especially if climate warming leads to moister conditions, as predicted.
A pre-requisite for denitrification and nitrification is the availability of inorganic nitrogen (N). In many natural ecosystems, atmospheric N deposition as well as moss-associated N2 fixation are the main sources of ‘new’ N to the ecosystem N pool and could provide inorganic N to sustain N2O production. While a link between N2 fixation and N2O emissions is plausible, hardly any attempts have been undertaken to test this link in areas with a moss-dominated understory. Here, we report results from a combined field and laboratory study in which we assessed N2 fixation, net N2O emission under different conditions, and potential nitrification and denitrification in three moss species from a Sphagnum-moss dominated, temperate bog. The three moss species were chosen to represent a gradient of N2 fixation activity. Sphagnum mosses emitted less N2O than the other two moss species (Pleurozium schreberi, Hypnum cupressiforme), but at the same time, showed the highest N2 fixation activity. The lack of a link between N2 fixation and net N2O emissions in three abundant and common moss species indicates that N transformation processes may be decoupled within the moss carpet. This raises new questions on N supply for N2O production and the fate of fixed N2 in moss-dominated systems.
Biological nitrogen (N2) fixation is one of the main sources of available N for pristine ecosystems such as subarctic and arctic tundra. Although this has been acknowledged more than a decade ago, few attempts have been undertaken to identify the foremost driver of N2 fixation in the high Arctic. Here, we report results from in situ measurements of N2 fixation throughout the main growing period (June–August) in high arctic tundra, Greenland, in climate change treatments, shading and warming, and control. Nitrogen fixation was also measured in cores that received additional water prior to the measurements. The climate change field treatments did not lead to significant changes in any measured parameters; however, N2 fixation was promoted by adding water, and moisture was the most important factor influencing N2 fixation in all climate change field treatments. Maximum N2 fixation rates were measured below 14°C soil temperature, which is much lower than the theoretical and previously reported temperature optimum for the nitrogenase enzyme. Diazotroph (N2 fixing bacteria) communities are adapted to low temperatures in high arctic settings, and increased temperature in a future climate may lead to decreased N2 fixation rates, or to a shift in diazotroph communities.
Nitrogen (N) fixation in moss-cyanobacteria associations is one of the main sources of ‘new’ N in pristine ecosystems like subarctic and arctic tundra. This fundamental ecosystem process is driven by temperature as well as by moisture. Yet, the effects of temperature and moisture stress on N2 fixation in mosses under controlled conditions have rarely been investigated separately, rendering the interactive effects of the two climatic factors on N2 fixation unknown. Here, we tested the interactive effects of temperature and moisture on N2 fixation in the two most dominant moss species in a temperate heath, subarctic tundra and arctic tundra: Pleurozium schreberi and Tomentypnum nitens. Mosses with different moisture levels (25, 50, 100%) were kept at different temperatures (10, 20, 30 °C) and N2 fixation was measured at different times after exposure to these conditions. T. nitens had the highest nitrogenase activity and this increased with moisture content, while effects were moderate for P. schreberi. Nitrogenase activity increased with temperature in all mosses, and the temperature optimum (Topt) was between 20 °C and 30 °C for all mosses. Quick acclimatization towards higher temperatures occurred. Our results suggest that the contemporary and not the historical climate govern the response of moss-associated N2 fixation to changes in the abiotic environment. Thus, climate change will have substantial impacts on N2 fixation in dominant mosses in temperate, subarctic and arctic habitats.
In pristine Sphagnum dominated peatlands, (di)nitrogen (N2) fixing (diazotrophic) microbial communities associated with Sphagnum mosses contribute substantially to the total nitrogen input, increasing carbon sequestration. The rates of symbiotic nitrogen fixation reported for Sphagnum peatlands, are, however, highly variable and experimental work on regulating factors that can mechanistically explain this variation is largely lacking. For two common fen species (Sphagnum palustre and S. squarrosum) from a high nitrogen deposition area (25 kg N ha−1 y−1), we found that diazotrophic activity (as measured by 15–15/>N2 labeling) was still present. This was surprising, given that nitrogen fixation is a costly process. We tested the effects of phosphorus availability and buffering capacity by bicarbonate rich water, mimicking a field situation in fens with stronger groundwater or surface water influence, as potential regulators of nitrogen fixation rates and Sphagnum performance. We expected that the addition of phosphorus, being a limiting nutrient, would stimulate both diazotrophic activity and Sphagnum growth. We indeed found that nitrogen fixation rates were doubled. Plant performance, in contrast, did not increase. Raised bicarbonate levels also enhanced nitrogen fixation, but had a strong negative impact on Sphagnum performance. These results explain the higher nitrogen fixation rates reported for minerotrophic and more nutrient-rich peatlands. The contrasting effects of phosphorus and bicarbonate on Sphagnum spp and their diazotrophic communities reveal strong differences in optimal niche for both partners with respect to conditions and resources. This suggests a trade-off for the symbiosis of nitrogen fixing microorganisms with their Sphagnum hosts, in which a sheltered environment apparently outweighs the less favorable environmental conditions. We conclude that microbial activity is still nitrogen limited under eutrophic conditions because dissolved nitrogen is being monopolized by Sphagnum. Moreover, the fact that diazotrophic activity can significantly be upregulated by increased phosphorus addition and acid buffering, while Sphagnum spp do not benefit, reveals remarkable differences in optimal conditions for both symbiotic partners and questions the concept of a direct mutualism.
Nitrogen (N) fixation in the feather moss–cyanobacteria association represents a major N source in boreal forests which experience low levels of N deposition; however, little is known about the effects of anthropogenic N inputs on the rate of fixation of atmospheric N2 in mosses and the succeeding effects on soil nutrient concentrations and microbial community composition. We collected soil samples and moss shoots of Pleurozium schreberi at six distances along busy and remote roads in northern Sweden to assess the influence of road-derived N inputs on N2 fixation in moss, soil nutrient concentrations and microbial communities. Soil nutrients were similar between busy and remote roads; N2 fixation was higher in mosses along the remote roads than along the busy roads and increased with increasing distance from busy roads up to rates of N2 fixation similar to remote roads. Throughfall N was higher in sites adjacent to the busy roads but showed no distance effect. Soil microbial phospholipid fatty acid (PLFA) composition exhibited a weak pattern regarding road type. Concentrations of bacterial and total PLFAs decreased with increasing distance from busy roads, whereas fungal PLFAs showed no distance effect. Our results show that N2 fixation in feather mosses is highly affected by N deposition, here derived from roads in northern Sweden. Moreover, as other measured factors showed only weak differences between the road types, atmospheric N2 fixation in feather mosses represents a highly sensitive indicator for increased N loads to natural systems.
The fertilization responses of six tundra species belonging to three plant growth forms were compared to test the hypothesis that species of the same plant growth form are more similar to one another than to other growth forms in their response to a controlled perturbation. The controlled perturbation was a complete factorial NPK fertilization experiment in tussock tundra at Eagle Creek, Alaska, USA. We compared deciduous shrubs, evergreen shrubs, and functionally deciduous graminoids in terms of mineral and total nonstructural carbohydrate (TNC) concentrations, and annual production per stem or tiller.
Nitrogen inputs via biological N2-fixation are important in arctic environments where N often limits plant productivity. An understanding of the direct and
indirect theoretical causal relationships between key intercorrelated variables that drive the process of N2-fixation is essential to understanding N input. An exploratory multi-group Structural Equation Modeling (SEM) approach was
used to examine the direct and indirect effects of soil moisture, plant community functional composition, and bryophyte and
lichen abundance on rates of nitrogen fixation at a low arctic ecosystem, two high arctic oases and a high arctic polar desert
in the Canadian Arctic. Increasing soil moisture was strongly associated with an increasing presence of bryophytes and increasing
bryophyte abundance was a major factor determining higher N2-fixation rates at all sites. Shrubs had a negative effect on bryophyte abundance at all sites with the exception of the polar
desert site at Alexandra Fjord highland. The importance of competition from vascular plants appears to be greater in more
productive sites and may increase at lower latitudes. Moisture availability may have an indirect effect on ecosystem development
by affecting N input into the system with bryophyte-cyanobacterial associations playing an important intermediary role in
the process.
Human activities have clearly caused dramatic alterations of the terrestrial nitrogen cycle, and analyses of the extent and effects of such changes are now common in the scientific literature. However, any attempt to evaluate N cycling processes within ecosystems, as well as anthropogenic influences on the N cycle, requires an understanding of the magnitude of inputs via biological nitrogen fixation (BNF). Although there have been many studies addressing the microbiology, physiology, and magnitude of N fixation at local scales, there are very few estimates of BNF over large scales. We utilized >100 preexisting published estimates of BNF to generate biome- and global-level estimates of biological N fixation. We also used net primary productivity (NPP) and evapotranspiration (ET) estimates from the Century terrestrial ecosystem model to examine global relationships between these variables and BNF as well as to compare observed and Century-modeled BNF. Our data-based estimates showed a strong positive relationship between ecosystem ET and BNF, and our analyses suggest that while the model's simple relationships for BNF predict broad scale patterns, they do not capture much of the variability or magnitude of published rates. Patterns of BNF were also similar to patterns of ecosystem NPP. Our ``best estimate'' of potential nitrogen fixation by natural ecosystem is ~195 TgNyr-1, with a range of 100-290 TgNyr-1. Although these estimates do not account for the decrease in natural N fixation due to cultivation, this would not dramatically alter our estimate, as the greatest reductions in area have occurred in systems characterized by relatively low rates of N fixation (e.g., grasslands). Although our estimate of BNF in natural ecosystems is similar to previously published estimates of terrestrial BNF, we believe that this study provides a more documented, constrained estimate of this important flux.
A significant fraction of the Earth's land surface is dominated by bryophytes. Research on carbon and nitrogen budgets of tundra, boreal, and peatland ecosystems has demonstrated the important role of mosses in understanding global change. Bryo-phytes are also habitat to a highly diverse micro-biota that plays a key role in the function of these ecosystems. Here we define the term bryosphere to emphasize the combined role of mosses and their associated organisms in the functioning of ecosys-tems from local to global scales. In this minireview, we emphasize the value of the bryosphere as a spatially bounded, whole ecosystem that integrates aboveground and belowground processes, and we highlight the potential of the bryosphere as a nat-ural model system (NMS) to assist in the study of environmental change on biodiversity and ecosys-tem functioning. We propose a formal definition of the bryosphere, attempt to summarize the current state of knowledge of the bryosphere, and discuss how the bryosphere can be a complex yet tractable system under an NMS framework. Recent use of the bryosphere as an NMS has shown how altera-tions in food web structure can affect ecosystem function in a manner that, although predicted by theory, has remained largely untested by experi-ment. An understanding of the biodiversity, eco-system functioning, and adaptation of the bryosphere can be advanced by manipulative experiments coupled with a blend of techniques in molecular, physiological, community, and ecosys-tem ecology. Although studies described herein have demonstrated the utility of the bryosphere NMS for addressing ecological theory, the bryo-sphere is an underutilized system with exceptional promise.
Cyanobacteria are an ancient and morphologically diverse group of photosynthetic prokaryotes, which were the first to evolve
oxygenic photosynthesis. Cyanobacteria are widely distributed in diversed environments. In the case of members of the orders
Nostocales and Stigonematales, their persistence and success were attributed to their ability to form specialized cells: heterocysts,
capable of fixing atmospheric nitrogen and spore-like cells, the akinetes. This review focuses on akinetes of Nostocales,
emphasizing environmental triggers and cellular responses involved in differentiation, maturation, dormancy, and germination
of these resting cells. Morphological and structural changes, variation in akinete composition, and metabolism are summarized.
Special attention is given to the genetic regulation of the differentiation process in an attempt to close gaps in our understanding
of the dormancy phenomenon in cyanobacteria and to identify open questions for future research.
Plant productivity is predicted to increase in boreal forests owing to climate change, but this may depend on whether N inputs from biological N-fixation also increases. We evaluated how alteration of climatic factors affects N input from a widespread boreal N-fixer, i.e. cyanobacteria associated with the feather moss Pleurozium schreberi. In each of 10 forest stands in northern Sweden, we established climate-change plots, including a control (ambient climate) plot and three plots experiencing a +2°C temperature increase, an approximately threefold reduction in precipitation frequency, and either 0.07, 0.29 or 1.16 times normal summer precipitation. We monitored N-fixation in these plots five times between 2007 and 2009, and three times in 2010 after climate treatments ended to assess their recovery. Warmer temperatures combined with less frequent precipitation reduced feather moss moisture content and N-fixation rates regardless of total precipitation. After climate treatments ended, recovery of N-fixation rates occurred on the scale of weeks to months, suggesting resilience of N-fixation to changes in climatic conditions. These results suggest that modelling of biological N-inputs in boreal forests should emphasize precipitation frequency and evaporative water loss in conjunction with elevated temperature rather than absolute changes in mean precipitation.
Certain filamentous nitrogen-fixing cyanobacteria generate signals that direct their own multicellular development. They also respond to signals from plants that initiate or modulate differentiation, leading to the establishment of a symbiotic association. An objective of this review is to describe the mechanisms by which free-living cyanobacteria regulate their development and then to consider how plants may exploit cyanobacterial physiology to achieve stable symbioses. Cyanobacteria that are capable of forming plant symbioses can differentiate into motile filaments called hormogonia and into specialized nitrogen-fixing cells called heterocysts. Plant signals exert both positive and negative regulatory control on hormogonium differentiation. Heterocyst differentiation is a highly regulated process, resulting in a regularly spaced pattern of heterocysts in the filament. The evidence is most consistent with the pattern arising in two stages. First, nitrogen limitation triggers a nonrandomly spaced cluster of cells (perhaps at a critical stage of their cell cycle) to initiate differentiation. Interactions between an inhibitory peptide exported by the differentiating cells and an activator protein within them causes one cell within each cluster to fully differentiate, yielding a single mature heterocyst. In symbiosis with plants, heterocyst frequencies are increased 3- to 10-fold because, we propose, either differentiation is initiated at an increased number of sites or resolution of differentiating clusters is incomplete. The physiology of symbiotically associated cyanobacteria raises the prospect that heterocyst differentiation proceeds independently of the nitrogen status of a cell and depends instead on signals produced by the plant partner.
This paper examines the impact of food and energy production on the global N cycle by contrasting N flows in the late-19th century with those of the late-20th century. We have a good understanding of the amounts of reactive N created by humans, and the primary points of loss to the environment. However, we have a poor understanding of nitrogen's rate of accumulation in environmental reservoirs, which is problematic because of the cascading effects of accumulated N in the environment. The substantial regional variability in reactive nitrogen creation, its degree of distribution, and the likelihood of increased rates of reactive-N formation (especially in Asia) in the future creates a situation that calls for the development of a Total Reactive Nitrogen Approach that will optimize food and energy production and protect environmental systems.
Biological nitrogen (N) fixation is the primary source of N within natural ecosystems, yet the origin of boreal forest N has remained elusive. The boreal forests of Eurasia and North America lack any significant, widespread symbiotic N-fixing plants. With the exception of scattered stands of alder in early primary successional forests, N-fixation in boreal forests is considered to be extremely limited. Nitrogen-fixation in northern European boreal forests has been estimated at only 0.5 kg N ha(-1) yr(-1); however, organic N is accumulated in these ecosystems at a rate of 3 kg N ha(-1) yr(-1) (ref. 8). Our limited understanding of the origin of boreal N is unacceptable given the extent of the boreal forest region, but predictable given our imperfect knowledge of N-fixation. Herein we report on a N-fixing symbiosis between a cyanobacterium (Nostoc sp.) and the ubiquitous feather moss, Pleurozium schreberi (Bird) Mitt. that alone fixes between 1.5 and 2.0 kg N ha(-1) yr(-1) in mid- to late-successional forests of northern Scandinavia and Finland. Previous efforts have probably underestimated N-fixation potential in boreal forests.
Biological feedback mechanisms regulate fundamental ecosystem processes and potentially regulate ecosystem productivity. To
date, no studies have documented the down-regulation of terrestrial nitrogen (N) fixation via an ecosystem-level feedback
mechanism. Herein, we demonstrate such a feedback in boreal forests. Rapid cycling of N in early secondary succession forests
yielded greater throughfall N deposition, which in turn decreased N fixation by cyanobacterial associates in feather moss
carpets that reside on the forest floor. The forest canopy exerts a tight control on biotic N input at a period of high productivity.
The removal of cell-bound water through air drying and the addition of water to air-dried cells are forces that have played a pivotal role in the evolution of the prokaryotes. In bacterial cells that have been subjected to air drying, the evaporation of free cytoplasmic water (Vf) can be instantaneous, and an equilibrium between cell-bound water (Vb) and the environmental water (vapor) potential (psi wv) may be achieved rapidly. In the air-dried state some bacteria survive only for seconds whereas others can tolerate desiccation for thousands, perhaps millions, of years. The desiccated (anhydrobiotic) cell is characterized by its singular lack of water--with contents as low as 0.02 g of H2O g (dry weight)-1. At these levels the monolayer coverage by water of macromolecules, including DNA and proteins, is disturbed. As a consequence the mechanisms that confer desiccation tolerance upon air-dried bacteria are markedly different from those, such as the mechanism of preferential exclusion of compatible solutes, that preserve the integrity of salt-, osmotically, and freeze-thaw-stressed cells. Desiccation tolerance reflects a complex array of interactions at the structural, physiological, and molecular levels. Many of the mechanisms remain cryptic, but it is clear that they involve interactions, such as those between proteins and co-solvents, that derive from the unique properties of the water molecule. A water replacement hypothesis accounts for how the nonreducing disaccharides trehalose and sucrose preserve the integrity of membranes and proteins. Nevertheless, we have virtually no insight into the state of the cytoplasm of an air-dried cell. There is no evidence for any obvious adaptations of proteins that can counter the effects of air drying or for the occurrence of any proteins that provide a direct and a tangible contribution to cell stability. Among the prokaryotes that can exist as anhydrobiotic cells, the cyanobacteria have a marked capacity to do so. One form, Nostoc commune, encompasses a number of the features that appear to be critical to the withstanding of a long-term water deficit, including the elaboration of a conspicuous extracellular glycan, synthesis of abundant UV-absorbing pigments, and maintenance of protein stability and structural integrity. There are indications of a growing technology for air-dried cells and enzymes. Paradoxically, desiccation tolerance of bacteria has virtually been ignored for the past quarter century. The present review considers what is known, and what is not known, about desiccation, a phenomenon that impinges upon every facet of the distributions and activities of prokaryotic cells.
This paper examines the impact of food and energy production on the global N cycle by contrasting N flows in the late-19(th) century with those of the late-20(th) century. We have a good understanding of the amounts of reactive N created by humans, and the primary points of loss to the environment. However, we have a poor understanding of nitrogen's rate of accumulation in environmental reservoirs, which is problematic because of the cascading effects of accumulated N in the environment. The substantial regional variability in reactive nitrogen creation, its degree of distribution, and the likelihood of increased rates of reactive-N formation (especially in Asia) in the future creates a situation that calls for the development of a Total Reactive Nitrogen Approach that will optimize food and energy production and protect environmental systems.
There is little understanding of successional dynamics of N fixation in northern boreal forests. Recent evidence suggests that N fixation by cyanobacteria in association with the common feather moss Pleurozium schreberi contributes to a significant proportion of the total N economy. The purpose of the work herein was to determine how time since last fire influences N fixation rates in boreal forests. We evaluated seasonal N fixation rates on a total of 12 natural forest preserves varying in time since last fire (35-355 years). Each site was monitored for N fixation activity using a calibrated acetylene reduction assay. Nitrogen fixation rates were found to increase linearly with time since fire. This increase in N fixation with succession is likely a function of degree of colonization by cyanobacteria and site factors such as presence of available N. Surface applications of 4.5 kg N-ha -1·yr-1 as NH4NO3 were found to eliminate N fixation while applications of P resulted in only a slight and temporary increase of N fixation rates. In contrast to common observation our findings suggest that N fixation in boreal forests becomes more important in late succession. Limited N availability in late succession is clearly one of the primary drivers of N fixation rates in boreal forest ecosystems. These findings may help to explain the origin of high rates of net N accumulation in soil unaccounted for at northern boreal sites.
The mechanistic basis of feather moss–cyanobacteria associations, a main driver of nitrogen ( N ) input into boreal forests, remains unknown. Here, we studied colonization by N ostoc sp. on two feather mosses that form these associations ( P leurozium schreberi and H ylocomium splendens ) and two acrocarpous mosses that do not ( D icranum polysetum and P olytrichum commune ). We also determined how N availability and moss reproductive stage affects colonization, and measured N transfer from cyanobacteria to mosses.
The ability of mosses to induce differentiation of cyanobacterial hormogonia, and of hormogonia to then colonize mosses and re‐establish a functional symbiosis was determined through microcosm experiments, microscopy and acetylene reduction assays. Nitrogen transfer between cyanobacteria and Pleurozium schreberi was monitored by secondary ion mass spectrometry ( SIMS ).
All mosses induced hormogonia differentiation but only feather mosses were subsequently colonized. Colonization on P leurozium schreberi was enhanced during the moss reproductive phase but impaired by elevated N . Transfer of N from cyanobacteria to their host moss was observed.
Our results reveal that feather mosses likely secrete species‐specific chemo‐attractants when N ‐limited, which guide cyanobacteria towards them and from which they gain N . We conclude that this signalling is regulated by N demands of mosses, and serves as a control of N input into boreal forests.
Feather mosses in boreal forests form a dense ground-cover that is an important driver of both nutrient and carbon cycling. While moss growth is highly sensitive to moisture availability, little is known about how moss effects on nutrient and carbon cycling are affected by the dynamics of moisture input to the ecosystem. We experimentally investigated how rainfall regimes affected ecosystem processes driven by the dominant boreal feather moss Pleurozium schreberi by manipulating total moisture amount, frequency of moisture addition and moss presence/absence. Moisture treatments represented the range of rainfall conditions that occur in Swedish boreal forests as well as shifts in rainfall expected through climate change. We found that nitrogen (N) fixation by cyanobacteria in feather mosses (the main biological N input to boreal forests) was strongly influenced by both moisture amount and frequency, and their interaction; increased frequency had greater effects when amounts were higher. Within a given moisture amount, N fixation varied up to seven-fold depending on how that amount was distributed temporally. We also found that mosses promoted vascular litter decomposition rates, concentrations of litter nutrients, and active soil microbial biomass, and reduced N release into soil solution. These effects were usually strongest under low moisture amount and/or frequency, and revealed a buffering effect of mosses on the decomposer subsystem under moisture limitation. These results highlight that both the amount and temporal distribution of rainfall, determine the effect of feather mosses on ecosystem N input and the decomposer subsystem. They also emphasize the role of feather mosses in mediating moisture effects on decomposer processes. Finally, our results suggest that projected shifts in precipitation in the Swedish boreal forest through climate change will result in increased moss growth and N2 fixation but a reduced dependency of the decomposer subsystem on feather moss cover for moisture retention.
Productivity in boreal ecosystems is primarily limited by available soil nitrogen (N), and there is substantial interest in understanding whether deposition of anthropogenically derived reactive nitrogen (Nr) results in greater N availability to woody vegetation, which could result in greater carbon (C) sequestration. One factor that may limit the acquisition of Nr by woody plants is the presence of bryophytes, which are a significant C and N pool, and a location where associative cyanobacterial N-fixation occurs. Using a replicated stand-scale N-addition experiment (five levels: 0, 3, 6, 12, and 50 kg N ha−1 yr−1; n=6) in the boreal zone of northern Sweden, we tested the hypothesis that sequestration of Nr into bryophyte tissues, and downregulation of N-fixation would attenuate Nr inputs, and thereby limit anthropogenic Nr acquisition by woody plants. Our data showed that N-fixation per unit moss mass and per unit area sharply decreased with increasing N addition. Additionally, the tissue N concentrations of Pleuorzium schreberi increased and its biomass decreased with increasing N addition. This response to increasing N addition caused the P. schreberi N pool to be stable at all but the highest N addition rate, where it significantly decreased. The combined effects of changed N-fixation and P. schreberi biomass N accounted for 56.7% of cumulative Nr additions at the lowest Nr addition rate, but only a minor fraction for all other treatments. This ‘bryophyte effect’ can in part explain why soil inorganic N availability and acquisition by woody plants (indicated by their δ15N signatures) remained unchanged up to N addition rates of 12 kg ha−1 yr−1 or greater. Finally, we demonstrate that approximately 71.8% of the boreal forest experiences Nr deposition rates at or below 3 kg ha−1 yr−1, suggesting that bryophytes likely limit woody plant acquisition of ambient anthropogenic Nr inputs throughout a majority of the boreal forest.
Many chemical reactions at the Earth's surface are influenced by biota. Ecosystem ecologists study the flow of matter and energy in ecosystems com-posed of organisms and their abiotic environments. The study of ecosystem ecology can blur distinc-tions between 'basic' research and environmental management. How does our behavior (including ur-ban development and land-use, water consumption, pollution) influence the movement of energy, water, and elements at local, regional, national or global scales? Will perturbations to chemical and energy cycles alter existing controls on ecosystem pro-cesses, and can we learn enough about them for effective regulation? Plants are critical in regulating biogeochemical cycles. Their growth controls the exchange of gases that support life in our current biosphere, and af-fects soil development. As primary producers, they influence the distribution of energy for higher tro-phic levels. Understanding how plants influence ecosystem processes requires a multidisciplinary approach drawing on plant physiology and bio-chemistry, community ecology, and biogeochem-istry. Due to their unique physiology and ecology, bryophytes differ from vascular plants in influenc-ing cycles of elements, energy, and water. For ex-ample, bryophytes have evolved an effective water relation system. Poikilohydry and desiccation tol-erance allow bryophytes to tolerate longer periods of water stress than vascular plants, and to recover quickly with rehydration. With poorly developed conduction systems, water and solutes are taken up over the entire plant surface. Lack of both game-tophyte stomata and effective cuticles in many spe-cies allows free exchange of solutions and gases across cell surfaces. Thus bryophytes often serve as effective traps for water and nutrients. This also makes them more sensitive to atmospheric chemi-cal deposition than vascular plants. Bryophytes also can tolerate a wide range of temperatures and are found in almost all terrestrial and aquatic environments, including harsh Antarc-tic environments where vascular plant cover is low (cf. Fogg 1998; Seppelt 1995). Without roots, bryo-phytes can colonize hard substrates like rock and wood that are poor habitat for vascular species. Bryophytes stabilize soils and prevent the loss of soil and nutrients via erosion, particularly on sand dunes (Martinez & Maun 1999) and in cryptogamic soil crusts (Eldridge 1999; Evans & Johansen 1999). Cation exchange on Sphagnum cell walls re-leases protons, generating acidity that may inhibit plant and microbial growth (Clymo 1963; Craigie & Maass 1966; Spearing 1972). Finally, bryophytes influence ecosystem succession (Brock & Bregman 1989) through terrestrialization of water bodies, de-position of benthic organic matter or paludification of upland systems. Bryophyte colonization often precedes the establishment of tree surfaces by other canopy-dwelling plants (Nadkarni et al. 2000). Due to their physiology and life history traits, bryophytes influence ecosystem functions by pro-ducing organic matter, stabilizing soils or debris, trapping sediments and water, and providing food and habitat for algae, fungi, invertebrates, and am-phibians. In this review, my objectives are to high-light several mechanisms by which bryophytes in-fluence carbon (C) and nitrogen (N) cycles within and fluxes from ecosystems. As such, I will focus on how bryophytes fix, intercept, transform, and/or release C and N. My goals are to 1) introduce im-portant processes controlling inputs and outputs of C and N in both terrestrial and aquatic ecosystems, 2) review work on the growth, decomposition, and leaching of bryophyte material, as well as biotic and abiotic controls on these mechanisms, and 3) suggest areas for future research that would ad-vance our understanding of bryophytes in biogeo-chemical cycling.
Cyanobacteria are an ancient, morphologically diverse group of prokaryotes with an oxygenic photosynthesis. Many cyanobacteria also possess the ability to fix N 2 . Although well suited to an independent existence in nature, some cyanobacteria occur in symbiosis with a wide range of hosts (protists, animals and plants). Among plants, such symbioses have independently evolved in phylogenetically diverse genera belonging to the algae, fungi, bryophytes, pteridophytes, gymnosperms and angiosperms. These are N 2 ‐fixing symbioses involving heterocystous cyanobacteria, particularly Nostoc , as cyanobionts (cyanobacterial partners). A given host species associates with only a particular cyanobiont genus but such specificity does not extend to the strain level. The cyanobiont is located under a microaerobic environment in a variety of host organs and tissues (bladder, thalli and cephalodia in fungi; cavities in gametophytes of hornworts and liverworts or fronds of the Azolla sporophyte; coralloid roots in cycads; stem glands in Gunnera ). Except for fungi, the hosts form these structures ahead of the cyanobiont infection. The symbiosis lasts for one generation except in Azolla and diatoms, in which it is perpetuated from generation to generation. Within each generation, multiple fresh infections occur as new symbiotic tissues and organs develop. The symbioses are stable over a wide range of environmental conditions, and sensing–signalling between partners ensures their synchronized growth and development. The cyanobiont population is kept constant in relation to the host biomass through controlled initiation and infection, nutrient supply and cell division. In most cases, the partners have remained facultative, with the cyanobiont residing extracellularly in the host. However, in the water‐fern Azolla and the freshwater diatom Rhopalodia the association is obligate. The cyanobionts occur intracellularly in diatoms, the fungus Geosiphon and the angiosperm Gunner a . Close cell–cell contact and the development of special structures ensure efficient nutrient exchange between the partners. The mobile nutrients are normal products of the donor cells, although their production is increased in symbiosis. Establishment of cyanobacterial–plant symbioses differs from chloroplast evolution. In these symbioses, the cyanobiont undergoes structural–functional changes suited to its role as provider of fixed N rather than fixed C, and the level of intimacy is far less than that of an organelle. This review provides an updated account of cyanobacterial–plant symbioses, particularly concerning developments during the past 10 yr. Various aspects of these symbioses such as initiation and development, symbiont diversity, recognition and signalling, structural–functional modifications, integration, and nutrient exchange are reviewed and discussed, as are evolutionary aspects and the potential uses of cyanobacterial–plant symbioses. Finally we outline areas that require special attention for future research. Not only will these provide information of academic interest but they will also help to improve the use of Azolla as green manure, to enable us to establish artificial N 2 ‐fixing associations with cereals such as rice, and to allow the manipulation of free‐living cyanobacteria for photobiological ammonia or hydrogen production or for use as biofertilizers.
contents
Summary
449
I.
introduction
450
II.
the partners
451
III.
initiation and development of symbioses
458
IV.
the symbioses
462
V.
evolutionary aspects
472
VI.
artificial symbioses
474
VII.
future outlook and perspectives
475
Acknowledgements
477
References
477
The removal of cell-bound water through air drying and the addition of water to air-dried cells are forces that have played a pivotal role in the evolution of the prokaryotes. In bacterial cells that have been subjected to air drying, the evaporation of free cytoplasmic water (Vf) can be instantaneous, and an equilibrium between cell-bound water (Vb) and the environmental water (vapor) potential (psi wv) may be achieved rapidly. In the air-dried state some bacteria survive only for seconds whereas others can tolerate desiccation for thousands, perhaps millions, of years. The desiccated (anhydrobiotic) cell is characterized by its singular lack of water--with contents as low as 0.02 g of H2O g (dry weight)-1. At these levels the monolayer coverage by water of macromolecules, including DNA and proteins, is disturbed. As a consequence the mechanisms that confer desiccation tolerance upon air-dried bacteria are markedly different from those, such as the mechanism of preferential exclusion of compatible solutes, that preserve the integrity of salt-, osmotically, and freeze-thaw-stressed cells. Desiccation tolerance reflects a complex array of interactions at the structural, physiological, and molecular levels. Many of the mechanisms remain cryptic, but it is clear that they involve interactions, such as those between proteins and co-solvents, that derive from the unique properties of the water molecule. A water replacement hypothesis accounts for how the nonreducing disaccharides trehalose and sucrose preserve the integrity of membranes and proteins. Nevertheless, we have virtually no insight into the state of the cytoplasm of an air-dried cell. There is no evidence for any obvious adaptations of proteins that can counter the effects of air drying or for the occurrence of any proteins that provide a direct and a tangible contribution to cell stability. Among the prokaryotes that can exist as anhydrobiotic cells, the cyanobacteria have a marked capacity to do so. One form, Nostoc commune, encompasses a number of the features that appear to be critical to the withstanding of a long-term water deficit, including the elaboration of a conspicuous extracellular glycan, synthesis of abundant UV-absorbing pigments, and maintenance of protein stability and structural integrity. There are indications of a growing technology for air-dried cells and enzymes. Paradoxically, desiccation tolerance of bacteria has virtually been ignored for the past quarter century. The present review considers what is known, and what is not known, about desiccation, a phenomenon that impinges upon every facet of the distributions and activities of prokaryotic cells.
A transect of 68 acid grasslands across Great Britain, covering the lower range of ambient annual nitrogen deposition in the industrialized world (5 to 35 kg Nha-1 year-1), indicates that long-term, chronic nitrogen deposition has significantly reduced plant species richness. Species richness declines as a linear function of the rate of inorganic nitrogen deposition, with a reduction of one species per 4-m2 quadrat for every 2.5 kg Nha-1 year-1 of chronic nitrogen deposition. Species adapted to infertile conditions are systematically reduced at high nitrogen deposition. At the mean chronic nitrogen deposition rate of central Europe (17 kg Nha-1 year-1), there is a 23% species reduction compared with grasslands receiving the lowest levels of nitrogen deposition.
A field survey was conducted to detect signals of atmospheric nitrogen (N) in 11 dune systems along a nitrogen deposition gradient in the United Kingdom. In the mobile and semi-fixed dunes, above-ground biomass was positively related to N inputs. This increase was largely due to increased height and cover of Ammophila arenaria. In the long term, this increased biomass may lead to increased organic matter accumulation and consequently accelerated soil development. In the fixed dunes, above ground biomass also showed a positive relationship with N inputs as did soil C : N ratio while soil available N was negatively related to N inputs. Plant species richness was negatively related to N inputs. In the dune slacks, while soil and bulk vegetation parameters showed no relationship with N inputs, cover of Carex arenaria and Hypochaeris radicata increased. Site mean Ellenberg N numbers showed no relationship with N deposition either within habitats or across the whole dataset. Neither abundance-weighting nor inclusion of the Siebel numbers for bryophytes improved the relationship. The survey reveals that the relationships of soil and vegetation with atmospheric N deposition vary between sand dune habitats but, despite this variability, clear correlations with N inputs exist. While this survey cannot establish causality, on the basis of the relationships observed we suggest a critical load range of 10 - 20 kg N ha(-1) yr(-1) for coastal sand dunes in the UK.
The suitability of the two pleurocarpous mosses Pleurozium schreberi and Scleropodium purum for assessing spatial variation in nitrogen deposition was investigated. Sampling was carried out at eight sites in the western part of Germany with bulk deposition rates ranging between 6.5 and 18.5 kg N ha(-1) yr(-1). In addition to the effect of deposition on the nitrogen content of the two species, its influence on 15N natural abundance (delta15N values) and on productivity was examined. Annual increases of the mosses were used for all analyses. Significant relationships between bulk N deposition and nitrogen content were obtained for both species; delta15N-values reflected the ratio of NH4-N to NO3-N in deposition. A negative effect of nitrogen input on productivity, i.e. decreasing biomass per area with increasing N deposition due to a reduction of stem density, was particularly evident with P. schreberi. Monitoring of N deposition by means of mosses is considered an important supplement to existing monitoring programs. It makes possible an improved spatial resolution, and thus those areas that receive high loads of nitrogen are more easily discernible.
Separate effects of ammonium (NH4+) and nitrate (NO3-) on boreal forest understorey vegetation were investigated in an experiment where 12.5 and 50.0 kg nitrogen (N) ha(-1) year(-1) was added to 2 m2 sized plots during 4 years. The dwarf-shrubs dominating the plant community, Vaccinium myrtillus and V. vitis-idaea, took up little of the added N independent of the chemical form, and their growth did not respond to the N treatments. The grass Deschampsia flexuosa increased from the N additions and most so in response to NO3-. Bryophytes took up predominately NH4+ and there was a negative correlation between moss N concentration and abundance. Plant pathogenic fungi increased from the N additions, but showed no differences in response to the two N forms. Because the relative contribution of NH4+ and NO3- to the total N deposition on a regional scale can vary substantially, the N load a habitat can sustain without substantial changes in the biota should be set considering specific vegetation responses to the predominant N form in deposition.
Acetylene reduction (AR) rates by cyanobacteria epiphytic on a moss at Marion Island (46 degrees 54' S, 37 degrees 45' E) increased from -5 degrees C to a maximum at 25 to 27 degrees C. Q(10) values between 0 and 25 degrees C were between 2.3 and 2.9, depending on photosynthetic photon flux density. AR rates declined sharply at temperatures above the optimum and were lower at 35 degrees C than at 0 degrees C. Photosynthetic photon flux density at low levels markedly influenced AR, and half of the maximum rate occurred at 84 mumol m s, saturation occurring at ca. 1,000 mumol m s. Higher photosynthetic photon flux density levels decreased AR rates. AR increased up to the highest sample moisture content investigated (3,405%), and the pH optimum was between 5.9 and 6.2. The addition of P, Co, and Mo, individually or together, depressed AR.
N fixation in feather moss carpets is maximized in late secondary successional boreal forests; however, there is limited understanding of the ecosystem factors that drive cyanobacterial N fixation in feather mosses with successional stage. We conducted a reciprocal transplant experiment to assess factors in both early and late succession that control N fixation in feather moss carpets dominated by Pleurozium schreberi. In 2003, intact microplots of moss carpets (30 cm x 30 cm x 10-20 cm deep) were excavated from three early secondary successional (41-101 years since last fire) forest sites and either replanted within the same stand or transplanted into one of three late successional (241-356 years since last fire) forest sites and the transverse was done for late successional layers of moss. Moss plots were monitored for changes in N-fixation rates by acetylene reduction (June 2003-September 2005) and changes in the presence of cyanobacteria on moss shoots by microscopy (2004). Forest nutrient status was measured using ionic resin capsules buried in the humus layer. Late successional forests exhibit high rates of N fixation and consistently high numbers of cyanobacteria on moss shoots, but low levels of available N. Conversely, early successional forests have higher N availability and have low rates of N fixation and limited presence of cyanobacteria on moss shoots. Transplantation of moss carpets resulted in a significant shift in presence and activity of cyanobacteria 1 year after initiation of the experiment responding to N fertility differences in early versus late successional forests.
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