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Tolerance of Phyllospadix scouleri seedlings to hydrogen sulfide

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Abstract

Phyllospadix scouleri is a common seagrass along the rocky intertidal coast of the Pacific Northwest. Previously we established a correlation between increased sulfide and hydrogen sulfide (H2S) and Zostera marina seedling senescence. While Z. marina grows in soft sediment environments, here we evaluate the possibility that P. scouleri may experience similar decreases in health when exposed to increasing H2S loading. To do this, seedlings were immersed in various concentrations of H2S, in axenic media, and photosynthetic and respiratory output was measured. We found that at high doses (mM) of H2S Photosystem II was inhibited whereas Photosystem I remained active. At lower levels, total photosynthetic output decreased with increasing H2S concentrations. Using these data we produced an LD50 of 430 μM at 48 h and 86 μM at 7 days. Our study confirms that Phyllospadix seedlings are also vulnerable to increasing sulfide loads.

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... Under stress from, for example shading (Holmer and Laursen, 2002), the oxygen release from seagrass roots decreases and sulphide production consequently increases. Sulphide can then diffuse via root and rhizome tissues into the photosynthesizing tissues (Hasler-Sheetal and Holmer, 2015;Mascaró et al., 2009), where it can inhibit photosynthesis by, for example, affecting photosystem II (Dooley et al., 2015) or the activity of enzymes such as cytochrome c oxidase in mitochondria (Koch et al., 1990;Lamers et al., 2013), leading to a decline in energy production and negative effects on a range of other metalcontaining enzymes (Hasler-Sheetal et al., 2016). ...
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Target discrimination is a key technique in missile defense system, and after analyzing the defense system configuration, an integrated target discrimination mathematical model based on recursive temporal-spatial data fusion is performed, which brings the expert knowledge, environmental information and measure information into the integrated discrimination flow. During spatial fusion process, the reliability of discrimination approach is measured by Analytical Hierarchy Process (AHP), and the concept of fusion weight is introduced to measure the value of discrimination approach for participating in fusion, which is determined by reliability of discrimination approach and consensus among sensors' results. During temporal fusion process, the fusion discrimination result is inherited and updated by Dempster-Shafer theory. Simulation results show that the integrated discrimination model can fuse the local decision from discrimination approaches effectively, restrain the influence of singularity and tolerate the error of discrimination.
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Root respiration decreased across the transect from the intertidal site to the 2 subtidal stations of increased sediment anaerobiosis. Data collected in field and laboratory experiments in which the hydrogen sulphide concentration surrounding the roots and rhizomes was enhanced showed physiological adaptations characteristic of tolerance to anaerobiosis. Zostera marina is thus capable of responding to markedly different microenvironments. - from Authors
Article
Plants of saline habitats can encounter anoxic conditions to extents which vary with habitat and life form. Rhizophytes (with roots or rhizoids in a sediment) routinely have anoxia or hypoxia in their roots, rhizoids and rhizomes. Haptophytes (attached to large particles of substrate) and planophytes (unattached) are generally less prone to anoxia or hypoxia, exceptions being ice-encased polar haptophytes and estuarine and muddy shore macroscopic planophytes (pleustophytes) which can become hypoxic or anoxic as a result of burial in sediment or under new growth. A major difference between anoxia in low-salinity habitats and anoxia in saline habitats is the presence of high sulphate concentrations in most saline habitats including seawater. Use of sulphate as electron acceptor in microbial oxidation or organic carbon produces sulphide, with relatively less production of methane than in anoxic habitats with lower sulphate concentrations. In addition to its role as a toxin. ³⁴S/³²S natural abundance data show that ³⁴S-depleted sulphide is directly or indirectly used as a sulphur source for roots and rhizomes of seagrasses and for the whole organism of emergent salt marsh herbs and mangroves. Granted the presence of hydrogen sulphide in the rhizosphere, its entry by lipid-solution permeation of the plasmalemma is inevitable. The balance of evidence favours the entry of hydrogen sulphide rather than the oxidation of ³⁴S-depleted sulphide to ³⁴S-depleted sulphate in an aerobic rhizosphere with subsequent entry of sulphate.
Article
The study presented here examined the effects of administering hydrogen sulfide (H2S) to several ancient extant plant species to determine the organisms’ response to stress. Even though sulfur is an essential macronutrient required for growth and productivity, there are toxic compounds of this element that exert detrimental effects and produce physiological stress. It is speculated that the accumulation of H2S, a lethal gas, may have been a major contributing factor in past mass extinction events, where the environment was fairly anoxic with fluctuating temperatures. The potential of this toxic compound to exist as an environmental stressor suggests that certain organisms may have adapted to survive these periods of mass extinctions. It is hypothesized that due to the abundant presence of H2S in the past, ancient land plants may have an adaptive advantage that allowed them to survive and thrive. In this study, species of bryophytes and algae were exposed to specific concentrations of aqueous H2S over a seven-day period and measured their photosynthetic capacity at timed intervals using a FluorCam. Studying the effects of this toxic gas on ancient plants is imperative to our understanding of sulfur's varying biological roles, and provides insight on the evolutionary phenotypic variations amongst plants and stress responses in order to survive mass extinctions. Results indicate that Hypnum, Chlamydomonas, and Charophyta are all able to tolerate significant quantities of H2S and show resilience through increased photosynthetic capacity over a period of exposure, indicating a genetic and phenotypic legacy response.
Article
Successful establishment of seedlings in populations of Zostera marina (eelgrass), especially for restoration efforts using stored seeds, depends in part on viability and germination of seeds. Seeds of Z. marina were collected from plants and stored in seawater at 5 °C for up to several years. Seed viability, assessed with the viability stain, tetrazolium chloride, decreased steadily over a four-year period. There was a strong correlation between age and viability; viability of fresh seeds was approximately 77% whereas for four-year old seeds was 32%. However, only 51 of 975 of fresh seeds that germinated (∼5%) developed leaves. The physical structure of the seed was evaluated to understand the effects of aging. It was determined that as seeds age there is an increase in the number of fractures on the seed coat. These data combined with the recent awareness that global seagrass populations are declining present valuable information to help maintain viable seed repositories which may contribute to the conservation and restoration of these wild plants.
Article
Temporal and spatial variation of d34S, total sulfur (TS) concentration, and elemental sulfur concentration (S0) in leaves, roots, and rhizomes of Zostera marina was followed between June 2002 and May 2003 at four locations in Roskilde Fjord and Øresund, Denmark. These were related to temporal changes in sediment sulfide concentrations, sulfur pool size, and sulfur pool d34S. The d34 So fZ. marina was most negative in the roots, followed by rhizomes and leaves, indicating that roots were mostly affected by sulfide. A significant relationship between decreasing d34S and increasing TS in the plant tissues indicated that sulfide accumulated in the plant and, furthermore, a positive relation between TS and S0 in the plant suggests that part of the sulfide is reoxidized to S0. There were marked temporal changes in all variables at all sites, but the pattern of change varied between sites. The temporal and spatial heterogeneity in plant d34S, TS, and S0 depended on a variety of factors, such as sediment sulfide concentrations and the below : aboveground biomass ratio of the plants. This suggests that mechanisms of sulfide invasion are complex, and several factors (plant morphology, environmental variables) acting in concert or against each other need to be considered to successfully predict sulfide invasion in seagrasses.
Article
The effects of pH changes on photosynthesis in three Mediterranean seagrass species were assessed by combining laboratory experiments with field records of pH. The response of photosynthesis to increasing pH was examined under laboratory conditions. Posidonia oceanica and Cymodocea nodosa showed a linear decrease in photosynthetic rates with pH; values at pH 8.8 were 25–80% of those obtained at pH 8.2. Zostera noltii was much less sensitive to pH increase than the other two species, maintaining high photosynthetic rates up to pH 8.8 and showing a significant reduction only at pH 9. Daily changes in pH over the seagrass meadows showed a maximum amplitude of ca. 0.5 pH units. However, the maximum daily values of pH were reached towards the end of the daily period of photosynthesis, and hence the estimated reduction in photosynthesis caused by the rising pH was relatively small (13–17%), in very shallow (i.e. 1 m deep or less) P. oceanica and C. nodosa meadows, and even less (about 4%) in deeper areas.
Article
Survival, metabolism and growth of Zostera marina exposed to hypoxia and sulfides in the water column were examined during a 3-week experiment. Z. marina was collected in the Archipelago of South Fyn, Denmark and kept under controlled laboratory conditions where they were exposed to low oxygen concentrations and two concentrations of sulfides in the water column. Survival of Z. marina was negatively influenced by the presence of sulfides, and photosynthetic activity stopped after 6 days of exposure to high sulfide concentrations (100–1000μM). Rates of photosynthesis also decreased in plants exposed to hypoxia, but the plants remained alive during the 3-week incubation. Rates of leaf elongation (exposed: 0–13.5mmmm−1d−2; control: 24mmmm−1d−2) and number of leaves per shoot (exposed: 3.2–4.2; control: 5.1) decreased in all treatments compared to control plants indicating that hypoxia and sulfides have negative impacts on Z. marina metabolism. The non-structural carbohydrate reserves in roots were reduced by up to 81% compared to the controls, whereas the reserves of starch in the rhizomes remained similar to the controls. The exposure to hypoxia and sulfides resulted in loss of above-ground biomass, most severe in the sulfide treatment (55% decrease in shoot:root ratio), suggesting that both parameters may play important roles during die-back events of seagrasses.
Article
Article
The effect of synergy between sediment organic enrichment and lack of night oxygen renewal in the water column on growth and survival of Zostera marina, and how it is reflected in the sulfur parameters in the plants (δ34S, TS and S0) was studied experimentally. An experiment consisting of Z. marina mesocosms with different levels of organic enrichment and water column aeration was established, and the effects on sediment conditions, sulfide invasion and growth and survival of Z. marina were examined over a 4 week period. Shoots growing in Ambient Organic matter–sediments showed signs of sulfide invasion, as TS increased in all plant compartments and δ34S of the plant tissues decreased during the experiment, but neither growth rate nor survival were significantly affected. The lack of night oxygen renewal had no evident effects in non-enriched sediments as porewater sulfide concentrations, AVS- and CRS-pools were not different from the corresponding 24 h aeration treatment. Plant growth rate and survival were neither different from the corresponding 24 h aeration treatment. On the contrary, shoots growing on High Organic matter-sediments suffered a massive sulfide invasion and it was directly correlated to the observed decrease in growth rates. Even though the lack of night oxygen renewal had no evident effects on sediment variables there were, however, strong indications that the different aeration levels affected plant performance, suggesting a lower sulfide oxidation capacity and confirming that low water column oxygen concentrations reduces the defense capacity of the shoots against sulfide invasion.Although δ34S, TS and S0 concentrations together provided a powerful set of indicators to detect the invasion of sulfide in Z. marina shoots, this study enlightens the need for a deeper investigation of sulfide intrusion in seagrasses and the relation between plant sulfur parameters and sediment conditions.
Article
Seeds of Zostera marina L. are capable of germinating in anaerobic (nitrogen-gassed) seawater (10%) and developing into seedlings with unusual morphology. The axial hypocotyl of seedlings grown in light and dark was characteristically elongated (mean in dark = 32 mm), but the pumule and adventitious roots remained rudimentary and embryonic in appearance. Aerobic seedlings by contrast exhibited little hypocotyl elongation (mean in dark = 5 mm), and plumule nad roots were well developed. The stalk-like blade of the cotyledon elongated in both aerobic and anaerobic cultures, but growth of the cotyledonary sheath surrounding the plumule was most marked in the presence of oxygen. When seedlings were grown anaerobically in the dark for 16 days and then transferred to aerobic-light conditions, elongation of the axial hypocotyl ceased instantly, but plumule and cotyledonary sheath growth was evident within 32 h, and by 96 h after transfer there was pronounced greening of the plumule leaves and swelling of the root primordia. Hypocotyl elongation of seedlings from seeds planted in sediment varied directly with planting depth. Elongation of the hypocotyl pushed the cotyledonary node with rudimentary plumule and root primordia up through the sediment to a position below the sediment surface where hypocotyl elongation stopped and plumule and root growth commenced. The cotyledonary blade which grew concomitantly with the axial hypocotyl continued to elongate after protruding from the sediment into the overlying water. Results from experiments in which the distal part of a seedling cotyledon was exposed to aerated water while the rest of the seedling was maintained in N2-gassed water suggested that the cotyledon may function as a conduit for oxygen diffusion to the plumular region of the seedling.
Article
Combinations of stresses showed an additive effect in comparison to the individual stress responses. It is apparent from these results that thermal, elevated-light or osmotic stress increases the sensitivity of Halophila ovalis to any of the other stress factors. Photosynthetic stress was detected using chlorophyll a fluorescence. Quantum yield was consistently the most effective measure of photosynthetic stress from combination stress exposures. Chlorophyll pigment analysis supported the general decline in photosynthetic capacity as indicated by the chlorophyll fluorescence; however, several anomalies did occur.
Article
The objectives of this study were to determine the distribution and abundance of Zostera marina (eelgrass) in relation to the distribution of the mat forming bacteria Beggiatoa spp., and the levels of sulfide and organic material (wood waste) in the sediment. Underwater videography and intertidal surveys were used to map the distribution and abundance of Z. marina beds and Beggiatoa in the nearshore area of Commencement Bay, WA (USA), a location that has a long history of sawmill activity. Zostera marina occurred from the intertidal to −6 m mean lower low water (MLLW) on sandy substrates in areas with low levels of sulfide (<50 μm) and organic material (<5 % total volatile solids). Areas with high sulfide levels (>200 μm) occurred where there were significant amounts of organic material in the sediments, which was found to be wood waste that had been discarded from sawmills. Zostera marina was absent from the intertidal and occurred at lower densities in areas with high sulfide levels. In contrast, mats of Beggiatoa were only found in areas where the sulfide levels were >1000 μm and there were significant deposits of wood. Thus, the negative correlation between the distribution and abundance of Z. marina and Beggiatoa suggests that the presence of Beggiatoa mats could be used as a biological indicator of inhibiting levels of hydrogen sulfide in the marine environment.
Article
In this study, we examined anatomical adaptations in the seagrass genus Phyllospadix to rocky substrates and surf exposed habitats not generally exploited by seagrasses. It was hypothesized that the genus exhibits anatomical features related to its specific habitat that distinguish it from a closely related sediment-rooted seagrass. Zostera marina L. A corollary to this hypothesis predicted that individual Phyllospadix species show additional specialization, based on observations that three species are distinctly zoned where they occur together.Comparison with Z. marina was used to define anatomical features in Phyllospadix that are considered adaptations to rocky littoral environments. These features include greater hypodermal fiber and root hair development, thickened rhizomes and smaller lacunae. Comparison among Phyllospadix spp. for microhabitat adaptations was less fruitful, although distribution patterns and comparative leaf thickness of the three species indicated that where P. torreyi S. Watson co-occurs with P. serrulatus Rupr. ex Aschers. P. torreyi may out-compete the latter for space, possibly because it is less vulnerable to disturbance.
Article
The effect of temperature on the photosynthesis and growth of seagrasses may be summarized by considering the ways in which temperature alters the characteristics of the photosynthesis-irradiance (P-I) curve of seagrasses. Within the limits of physiological tolerance (∼6–30°C) temperature has little effect on the initial slope of the P-I curve. At 35–40°C the photosynthetic capacity of seagrasses is reduced. Within the limits of physiological tolerance, the rate of photosynthesis at light saturation, the dark respiration rate and the light compensation point more than double as temperature increases. The optimum temperature for photosynthesis decreases from 25–35°C at light saturation to as low as 5°C as irradiance decreases. As a result of these effects of temperature on the P-I curve, growth of seagrasses in high(saturating) light environments increases with temperature, whereas growth of seagrasses in low (near the light compensation point) light environments decreases as temperature increases.
Article
A large-scale mesocosm (sixteen 500 L tanks) experiment was conducted to investigate the effects of hypersalinity (45–65 psu), porewater sulfide (2–6 mM) and nighttime water column hypoxia (5–3 mg L−1) on the tropical seagrass Thalassia testudinum Banks ex König. We examined stressor effects on growth, shoot survival, tissue sulfur (S0, TS, δ34S) and leaf quantum efficiencies, as well as, porewater sulfides (∑TSpw) and mesocosm water column O2 dynamics. Sulfide was injected into intact seagrass cores of T. testudinum exposing below-ground tissues to 2, 4, and 6 mM S2−, but rapid oxidation resulted in ∑TSpw < 1.5 mM. Hypersalinity at 65 psu lowered sulfide oxidation and significantly affected plant growth rates and quantum efficiencies (Fv/Fm < 0.70). The most depleted rhizome δ34S signatures were also observed at 65 psu, suggesting increased sulfide exposure. Hypoxia did not influence ∑TSpw and plant growth, but strengthened the hypersalinity response and decreased rhizome S0, indicating less efficient oxidation of ∑TSpw. Following nighttime hypoxia treatments, ecosystem level metabolism responded to salinity treatments. When O2 levels were reduced to 5 and 4 mg L−1, daytime O2 levels recovered to approximately 6 mg L−1; however, this recovery was more limited when O2 levels were lowered to 3 mg L−1. Subsequent to O2 reductions to 3 mg O2 L−1, nighttime O2 levels rose in the 35 and 45 psu tanks, stayed the same in the 55 psu tanks, and declined in the 65 psu tanks. Thus, hypersalinity at 65 psu affects T. testudinum's oxidizing capacity and places subtle demands on the positive O2 balance at an ecosystem level. This O2 demand may influence T. testudinum die-off events, particularly after periods of high temperature and salinity. We hypothesize that the interaction between hypersalinity and sulfide toxicity in T. testudinum is their synergistic effect on the critical O2 balance of the plant.
Article
Low iron content in tropical carbonate sediments limits the formation of iron–sulfide compounds such as pyrite. Thus, seagrasses in the tropics may be more susceptible to sulfide toxicity. Sediment sulfide levels greater than 2 mM and up to 13 mM have been hypothesized to cause widespread ‘die-back’ of the tropical seagrass Thalassia testudinum in a subtropical lagoon, Florida Bay. Hydroponic chambers were used to determine the effects of sulfide (0.0, 2.0, 4.0, 6.0 and 10.0 mM) on root and leaf adenylate ratios, energy charge (EC), leaf O2 flux, and growth of T. testudinum under light-saturated conditions. T. testudinum did not suffer mortality under short-term (48 h) exposure to sulfide concentrations up to 10 mM, but several metabolic stress responses were observed. Root ATP and energy charge significantly declined (P<0.05) as a function of increasing sulfide concentrations. Root EC was reduced from 0.78 in the control to 0.63–0.59 in the 2.0–6.0 mM treatments, and fell to 0.43 in the 10.0 mM treatment. Leaf elongation rates declined (P<0.05) by an average of 43% in 2.0–6.0 mM sulfide and 67% in 10 mM sulfide. Although root EC, root ATP production and leaf elongation rates significantly declined under root sulfide exposure, sulfide concentrations of 2.0–10.0 mM failed to produce visual signs of acute sulfide toxicity, such as leaf chlorosis, leaf or root necrotic tissue development, or loss of leaf or root turgor. Photosynthesis and leaf EC remained high after sulfide treatments, suggesting a resilience of T. testudinum leaf metabolism to short-term sulfide exposure. Our data do not support the hypothesis that sulfide initiates rapid ‘die-off’ episodes of T. testudinum in Florida Bay, although this phytotoxin may play a critical role as a root carbon drain over long-term exposures.
Article
The present study shows that in the presence of 600 nm light, sulfide acts as a specific inhibitor of photosynthetic electron transport between water and Photosystem II in the cyanobacteria Aphanothece halophytica and Synechococcus 6311 as well as in tobacco chloroplasts. In the presence of 600 nm light sulfied affects the fast fluorescence transients as does a low concentration (10 mM) of hydroxylamine; the fluorescence yield decreases in the presence of either chemical and can be restored by the addition of 3-(3,4-dichlorophenyl)-1,1-dimethylurea. In chloroplasts, however, NH2OH, an electron donor at high concentrations (40 mM), relieves the sulfide effect. In the dark, sulfide affects the cyanobacterial fluorescence transients through decrease of oxygen tension. The fluorescence yield increases in a similar pattern to that observed under nitrogen flushing. Upon omission of sulfide in A. halophytica, the characteristic aerobic fluorescence transients return, consistent with the ease of alternation between oxygenic and sulfide-dependent anoxygenic photosynthesis in many cyanobacteria.
Article
Chlorophyll fluorescence measurements have a wide range of applications from basic understanding of photosynthesis functioning to plant environmental stress responses and direct assessments of plant health. The measured signal is the fluorescence intensity (expressed in relative units) and the most meaningful data are derived from the time dependent increase in fluorescence intensity achieved upon application of continuous bright light to a previously dark adapted sample. The fluorescence response changes over time and is termed the Kautsky curve or chlorophyll fluorescence transient. Recently, Strasser and Strasser (1995) formulated a group of fluorescence parameters, called the JIP-test, that quantify the stepwise flow of energy through Photosystem II, using input data from the fluorescence transient. The purpose of this study was to establish relationships between the biochemical reactions occurring in PS II and specific JIP-test parameters. This was approached using isolated systems that facilitated the addition of modifying agents, a PS II electron transport inhibitor, an electron acceptor and an uncoupler, whose effects on PS II activity are well documented in the literature. The alteration to PS II activity caused by each of these compounds could then be monitored through the JIP-test parameters and compared and contrasted with the literature. The known alteration in PS II activity of Chenopodium album atrazine resistant and sensitive biotypes was also used to gauge the effectiveness and sensitivity of the JIP-test. The information gained from the in vitro study was successfully applied to an in situ study. This is the first in a series of four papers. It shows that the trapping parameters of the JIP-test were most affected by illumination and that the reduction in trapping had a run-on effect to inhibit electron transport. When irradiance exposure proceeded to photoinhibition, the electron transport probability parameter was greatly reduced and dissipation significantly increased. These results illustrate the advantage of monitoring a number of fluorescence parameters over the use of just one, which is often the case when the F(V)/F(M) ratio is used.