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Interactions of Bacteria, Fungi, and Their Nematode Grazers: Effects on Nutrient Cycling and Plant Growth

DOI:10.2307/1942528
Authors:
R. E. Ingham at Oregon State University
R. E. Ingham
John A Trofymow at Natural Resources Canada
John A Trofymow
Elaine R. Ingham
Elaine R. Ingham
Elaine R. Ingham
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David C. Coleman at University of Georgia
David C. Coleman
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Abstract

The most common system responses attributed to microfloral grazers (protozoa, nematodes, microarthropods) in the literature are increased plant growth, increased N uptake by plants, decreased or increased bacterial populations, increased CO"2 evolution, increased N and P mineralization, and increased substrate utilization. Based on this evidence in the literature, a conceptual model was proposed in which microfloral grazers were considered as separate state variables. To help evaluate the model, the effects of microbivorous nematodes on microbial growth, nutrient cycling, plant growth, and nutrient uptake were examined with reference to activities within and outside of the rhizosphere. Blue grama grass (Bouteloua gracilis) was grown in gnotobiotic microcosms containing sandy loam soil low in inorganic N, with or without chitin amendments as a source of organic N. The soil was inoculated with bacteria (Pseudomonas paucimobilis or P. stutzeri) or fungus (Fusarium oxysporum), with half the bacterial microcosms inoculated with bacterial-feeding nematodes (Pelodera sp. or Acrobeloides sp.) and half the fungal microcosms inoculated with fungal-feeding nematodes (Aphelenchus avenae). Similar results were obtained from both the unamended and the chitin-amended experiments. Bacteria, fungi, and both trophic groups of nematodes were more abundant in the rhizosphere than in nonrhizosphere soil. All treatments containing nematodes and bacteria had higher bacterial densities than similar treatments without nematodes. Plants growing in soil with bacteria and bacterial-feeding nematodes grew faster and initially took up more N than plants in soil with only bacteria, because of increased N mineralization by bacteria, NH"4^+-N excretion by nematodes, and greater initial exploitation of soil by plant roots. Addition of fungal-feeding nematodes did not increase plant growth or N uptake because these nematodes excreted less NH"4^+-N than did bacterial-feeding nematode populations and because the N mineralized by the fungus alone was sufficient for plant growth. Total shoot P was significantly greater in treatments with fungus or Pelodera sp. than in the sterile plant control or treatments with plants plus Pseudomonas stutzeri until the end of the experiment. The additional mineralization that occurs due to the activities of microbial grazers may be significant for increasing plant growth only when mineralization by microflora alone is insufficient to meet the plants' requirements. However, while the advantage of increased N mineralization by microbial grazers may be short-term, it may occur in many ecosystems in those short periods of ideal conditions when plant growth can occur. Thus, these results support other claims in the literature that microbial grazers may perform important regulatory functions at critical times in the growth of plants.
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Interactions of Bacteria, Fungi, and their Nematode Grazers: Effects on Nutrient Cycling and
Plant Growth
Author(s): Russell E. Ingham, J. A. Trofymow, Elaine R. Ingham, David C. Coleman
Source:
Ecological Monographs,
Vol. 55, No. 1 (Mar., 1985), pp. 119-140
Published by: Ecological Society of America
Stable URL: http://www.jstor.org/stable/1942528
Accessed: 08/01/2009 15:10
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... However, relationships between different bacterial-feeding nematodes, bacterial diversity, and community composition when organic and inorganic fertilizers are used together remain unclear. Additionally, bacterial-feeding nematodes can excrete inorganic N (mainly NH 4 + -N) to stimulate bacterial growth (Ingham et al. 1985), which is particularly important for maintaining soil bacterial abundance and N availability in agroecosystems. However, whether bacterial-feeding nematodes affect soil N availability through their effect on bacterial diversity and which genera of bacterial-feeding nematodes mainly contribute to the improvement of soil N availability when organic and inorganic fertilizers are used together is still unclear. ...
... First, moderate predation by nematodes can promote bacterial growth (Fu et al. 2005). Second, nematodes supply nutrients to bacteria to stimulate their growth by excreting inorganic N (mainly NH 4 + -N) and organic matter (Ingham et al. 1985). Third, numerous bacterial species can attach to the body surface or digestive system of nematodes (Jiang et al. 2017). ...
... Additionally, in this study, bacterial community composition had stronger influence on the NO 3 − -N content than bacterial diversity and abundance, considering that NO 3 − -N showed no correlation with the bacterial diversity index, and bacterial community composition showed a stronger effect on the NO 3 − -N content than bacterial abundance. In other study, bacterial-feeding nematodes are found to secrete NH 4 + -N after feeding on bacteria (Ingham et al. 1985). The SNPK soil had a significantly higher bacterial-feeding nematode abundance than unfertilized soil, with bacterial-feeding nematodes being a critical factor driving the changes in the NH 4 + -N content in this study. ...
Correlations Between the Soil Bacterial-Feeding Nematodes, Bacteria, and Nitrogen in the Cropland of the Upper Yangtze River, China
Article
Full-text available
  • Aug 2023
Bacterial-feeding nematodes affect bacteria-mediated nitrogen (N) cycling processes by their predation on bacteria. However, the correlations between bacterial abundance, diversity, community composition, and the abundance of bacterial-feeding nematodes in the presence of organic combined with inorganic fertilizers, and their effects on soil N availability are unclear. Here, four field fertilization treatments, including unfertilized control (CK), chemical N, phosphorus (P) and potassium (K) fertilizers (NPK), NPK plus crop straw (SNPK), and NPK plus pig manure (MNPK), were performed for studying relationships among bacterial abundance, diversity, community composition, and the abundance of bacterial-feeding nematodes along with corresponding effects on soil N availability. Results showed that nitrate nitrogen (NO3−-N) content was significantly upregulated in the SNPK and MNPK treatments compared to that in the NPK treatment and showed a significant positive relationship with bacterial abundance and community composition. As revealed by partial least squares structural equation model (PLS-SEM), bacterial community composition had a stronger effect on the NO3−-N content, and bacterial-feeding nematodes indirectly affected the NO3−-N content by directly positively affecting the bacterial community composition, among which the bacterial-feeding nematode Eucephalobus played a stronger role in the production of NO3−-N. Overall, the findings of this study suggested that bacterial-feeding nematodes can improve soil N availability through impacting bacterial community composition rather than bacterial diversity and abundance. These results suggest that bacterial-feeding nematodes may play an important role in improving soil N availability in farmlands.
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... However, soil nematodes, including plant-feeding (PF), bacterialfeeding (BF), fungal-feeding (FF), and omnivorous-carnivorous (OC) feeding-groups, have been shown to be sensitive to the increased availability of soil N in grasslands (Peng et al., 2022;Wardle et al., 2013;Xing et al., 2022). As widespread and diverse fauna groups in grasslands (Bardgett and Chan, 1999;, soil nematodes have potential effects on soil carbon (C) and nutrient cycling (Ferris, 2010;Ferris et al., 1997;Ingham et al., 1985). Many earlier studies examined the effects of N addition on nematode communities in grasslands at the local scale, with great variations in the direction and magnitude of responses to N enrichment across different studies (Chen et al., 2015a;Song et al., 2016;Treseder, 2008). ...
... For instance, PF nematodes can infect the roots of many plant species, which induce the leakage of carbohydrates and nutrients from injured roots; thus, increasing food supplies for microbial communities and accelerating C cycling in the rhizosphere soil (Gan and Wickings, 2020;Yeates et al., 1999;Yeates et al., 1998). In addition, BF and FF nematodes primarily feed on bacteria and fungi, respectively, which accelerates the growth and metabolism of microbes and promotes the C mineralization rate (Alkemade et al., 1992;Ingham et al., 1985;Trofymow and Coleman, 2021;Wu et al., 2007). However, the predation of OC nematodes on BF and FF nematodes can suppress the growth and reproduction of freeliving nematodes. ...
... After controlling the effects of lnRR of MBC, partial regression analysis showed that variations in the lnRR of the soil C min rate was primarily explained by the lnRR of nematode taxon richness, the lnRR of total abundance, and lnRRs of PF and FF abundances. The high diversity of nematode communities has been shown to stimulate a wider variety of microbes and thus increase microbial biomass Ingham et al., 1985). Therefore, the decline of nematode taxon richness and abundance under N enrichment may weaken its positive impacts on microbial biomass and contribute to the reduction of C min . ...
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... Thus, growers need to be judicious in their use of biofumigant crops-restricting their use over time as to not impinge upon soil microbial functioning [22]. For example, biofumigant crops can have deleterious effects on essential beneficial microbes such as arbuscular mycorrhizal fungi (AMF) and free-living nematodes (FLNs) [23,24]). There is evidence that these crops may negatively affect AMF by inhibiting spore germination [25,26], suppressing the AM symbioses [27,28]. ...
Using Brassica Cover Crops as Living Mulch in a Vineyard, Changes over One Growing Season
Article
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  • Dec 2023
Farmers hoping to manage cropping systems sustainably are turning to cover crops to help mitigate plant pathogens. Plants with biofumigant properties are used to control soil-borne pathogens in agricultural settings, especially in till systems, where the brassicas are incorporated into the soil as green manure or seed meal. The effect of these crops is not well studied in no-till systems; thus, it is hard to know if they are as effective as green manure. Whether or not these cover crops can effect changes during a single growth season has not yet been studied. This study compared the response of the soil microbial community to four different brassica cover crops, two of which are commonly used in vineyards (Sinapis alba L. (white mustard) and Raphanus sativus (L.) Domin (tillage radish)) as well as two brassicas that are native or naturalized to the Okanagan (Capsella bursa-pastoris (L.) Medik. (Shepherd’s purse) and Boechera holboelli (Hornem.) Á. Löve and D. Löve (Holbøll’s rockcress)). Cover crops did not affect fungal species richness, but B. holboelli recover crops were associated with increased evenness among fungal taxa. Both C. bursa-pastoris and S. alba had lower levels of plant parasitic nematodes compared to non-brassica controls. These results were apparent only after a single growing season, which indicates growers could use this approach as needed, minimizing long-term exposure to biofumigants for beneficial soil microbes.
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... They play crucial roles in ecosystem processes, such as improving soil physical properties, participating in carbon and nitrogen cycling by feeding on bacteria and fungi (Ingham et al. 1985), and maintaining ecosystem health by occupying key positions in the soil food cycle (Ferris 2010;Zhang et al. 2017). In contrast, soil nematode communities are affected by subtle changes in both abiotic and biotic factors (Neher et al. 2005). ...
Effects of tree species identity and soil origin on soil nematode communities and trophic composition in coniferous and broad-leaved forests
Preprint
Full-text available
  • Oct 2023
Purpose The effects of trees on soil nematode communities are related to nutrient cycles in forest ecosystems. We conducted greenhouse pot experiments to determine the effects of coniferous and broad-leaved tree species on soil nematodes. Methods Soils were collected from a coniferous plantation and broad-leaved forests. Seedlings of a coniferous tree (Cryptomeria japonica) and a broadleaved tree (Quercus serrata) were planted in soils derived from each species. After 11 months, seedling biomass, soil properties, and ectomycorrhizal fungal colonization of Q. serrata were measured. Soil nematodes were morphologically identified to the genus/family level and differentiated by community and trophic composition. Results C. japonica root biomass was significantly higher than that of Q. serrata regardless of the soil and nematode community structures were significantly different between the species. The fungal: bacterial ratio and density of fungivorous nematodes were significantly higher in broad-leaved soils. Herbivorous nematodes increased significantly in C. japonica seedlings grown in broad-leaved soils. Structural equation modeling indicated that soil origin and tree species directly regulated nematode trophic compositions. Conclusion Our findings suggest that tree species modify soil micro-food webs by affecting microbial abundance and nematode trophic composition. Specifically, C. japonica, with a larger root biomass, increased the number of herbivorous nematodes, whereas Q. serrata, with ectomycorrhizal fungal symbiosis, increased the number of fungivorous nematodes. Thus, tree species are tightly involved in shaping nematode communities in forest ecosystems through root traits and mycorrhizal types.
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... 3. Dave Coleman, Pat Reid, Don Klein, and Vern Cole measured belowground processes including microbes, fauna, roots, and nutrient cycling studied in gnotobiotic microcosms. The major findings of this research concluded that trophic interactions by microbivorous fauna (protists, nematodes, and microarthropods) led to significantly enhanced nutrient return to soils, followed by enhanced plant growth (Coleman et al., 1983;Ingham et al., 1985). 4. The need for simulation modeling expertise encouraged Bill Hunt to rejoin NREL. ...
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... For instance, soil nematodes had a C: N ratio similar to that of their microbial prey that would be lower in the predator through respiration of C (Ferris et al., 1997). The extra N and Nrich compounds such as inorganic N were released to soil (Ingham et al., 1985). In conclusion, strong abiotic-biotic interactions indirectly promoted ecosystem functions through stimulating growth and metabolism of plants and soil biota. ...
Ecosystem‐level decoupling in response to reduced precipitation frequency and degradation in steppe grassland
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Grasslands across arid and semi‐arid regions are predicted to experience reductions in precipitation frequency. Besides, grassland degradation has become a serious problem in many of these areas. Despite increasing evidence suggesting compound effects of these synchronous alterations on biotic and abiotic ecosystem constituents, we still do not know how they will impact the coupling among ecosystem constituents and its consequences on ecosystem functioning. Here, we assessed the effects of decreased precipitation frequency and grassland degradation on ecosystem coupling, quantified based on the mean strength of pairwise correlations among multispecies communities and their physicochemical environment, individual functions and ecosystem multifunctionality, and reported their relationships within a mechanistic plant–nematode–micro‐organism–soil interactions framework. Decreased precipitation frequency led to poorly coupled ecosystems, and reduced aboveground plant biomass, soil water content, soil nutrient levels, soil biota abundance and multifunctionality. By contrast, belowground plant biomass and soil potential enzyme activities increased under decreased precipitation frequency treatment. Severe degradation resulted in decoupled ecosystems and suppressed most of individual functions and multifunctionality. Using structural equation modelling, we showed that coupling had a strong direct positive effect on multifunctionality (standardized total effect: 0.74), while multifunctionality was weakened by greater soil water variation (−0.54) and higher soil pH (−0.53). The great sensitivity of ecosystem coupling to altered precipitation regimes and degradation highlights the importance of considering interactions among biotic and abiotic components when predicting early ecological impacts under changing environments. Moreover, the positive relationship between ecosystem coupling and functioning suggests that restoration of degraded grasslands may be achieved by intensifying ecological interactions. Read the free Plain Language Summary for this article on the Journal blog.
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... Nematodes are a dominant component of soil biodiversity [1,2] that play fundamental roles in nutrient cycling [3][4][5] and controlling the structure and activities of the microbial community [6,7]. Free-living nematodes enhance plant growth and crop production [5,[8][9][10] whereas plant-parasitic nematodes are a major pest group in agriculture causing considerable economic losses [11,12]. ...
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... The increased food web structure thus obtained is thought to enhance the natural regulation of soilborne pests and diseases, including that of plant-parasitic nematodes, thus supplying an important regulation ecosystem service to agroecosystems, and reducing the dependence on chemical pesticides [112]. Moreover, through their regulatory role in the decomposer community, bacterial-and fungal-feeding nematodes have the capacity to increase resource partitioning, substrate-use efficiency, and nutrient mineralization by bacteria and fungi, thus contributing to plant nutrition whilst promoting C sequestration [113]. Finally, increasing crop diversity, either in space (intercropping, polycropping) or in time (rotation) may be able to dilute herbivory and antagonism by specialist organisms-a well-described soil-feedback mechanism that leads to overyielding or increased plant productivity [114]. ...
Linking Nematode Communities and Soil Health under Climate Change
Article
Full-text available
  • Jul 2023
Soil health is intimately intertwined with ecosystem services. Climate change negatively impacts ecosystem functioning, by altering carbon and nitrogen biogeochemical cycles and shifting nutrient bioavailability, thus hampering food production and exacerbating biodiversity loss. Soil ecosystem services are provided by belowground biota, and as the most abundant metazoans on Earth, nematodes are key elements of soil food webs and reliable bioindicators of soil health. Here, we carry out a literature review from 2019, the year that the Intergovernmental Panel on Climate Change published a report relating and expressing serious concerns on the effects of climate change on the land degradation and sustainability of terrestrial ecosystems. We focus on documenting and discussing the composition of nematode communities contributing to improving soil health, and soil management practices to promote their presence and limit the effects of climate change on soils. By recognizing beneficial nematodes as plant-promoting agents, we could harness their potential to our benefit, catalyze decomposition services, improve plant performance, and increase carbon sequestration. This way, we will contribute to soil health and a well-balanced and well-managed system, making it possible to increase productivity, guarantee food security, and reduce the yield gap, with a limited human footprint on the environment.
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Root Fragment Amendments Increase Nematode Density and Mycobiome Stochasticity in Douglas-Fir Seedlings
Article
Full-text available
  • Oct 2023
Relatively little is known about whole-plant fungal communities (mycobiome) and associated soil nematodes, especially with respect to woody plant seedlings and disturbance caused by forest harvesting. In a growth chamber experiment, we tested simulated clear-cut soil conditions on shoot biomass, total soil nematode density, and the shoot and root mycobiome of Douglas-fir, Pseudotsuga menziesii (Mirb.) Franco, seedlings. Soil treatments included unamended bare soil and soil amended with root segments of kinnikinnick, Arctostaphylos uva-ursi (L.) Spreng., pinegrass, Calamagrostis rubescens Buckley, or P. menziesii seedlings. We used next-generation Illumina sequencing and the PIPITS pipeline to obtain fungal taxa used for mycobiome community richness and Jaccard-based taxonomic normalized stochasticity ratio to assess mycobiome community assembly stochasticity. Total nematode density, measured from Baermann funnel extractions, increased in soils supplemented with A. uva-ursi or C. rubescens root segments. Root mycobiomes were more stochastic in the A. uva-ursi than P. menziesii or the bare conditions, whereas the shoot mycobiome was more stochastic in the C. rubescens treatment than in the P. menziesii treatment. Our results suggest that refugia plants impact the phyto-biome, in this case plant-associated nematodes and the stochasticity of root and shoot mycobiome community assembly, while not showing noticeable impacts on above-ground plant growth.
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Nematode Diversity Associated With Grapevines in İzmir, Manisa, Çanakkale, Balıkesir, and Bilecik Provinces in Türkiye
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A study was conducted in İzmir, Manisa, Çanakkale, Balıkesir, and Bilecik provinces to determine nematode diversity and vineyard community structure. Thiry-six genera (İzmir 34 genera; Manisa 32 genera; Bilecik 21 genera; Çanakkale 28 genera) with different trophic groups were recorded: fungivores (3 genera; e.g., Aphelenchoides spp.), bacterivores (9 genera, e.g., Achromadora Cobb, 1913 and Plectus Bastian 1865 spp.), omnivore (4 genera; e.g., Aporcelaimus Thorne, 1936 and Dorylaimus Thorne & Swanger, 1936 and Eudorylaimus Andrassy, 1959 spp.), predators (3 genera; e.g., Clarkus spp.), herbivores (17 genera; e.g., Boleodorus tylactus Thorne, 1941). Twenty-six species of herbivores were identified, and the most common species were from the genera Filenchus Andrassy, 1954, Geocenamus Thorne & Malek, 1968; Pratylenchus Filipjev, 1934 and Helicotylenchus Steiner, 1945. Dorylaimus Dujardin, 1845; Mesorhabditis Osche, 1952; Cephalobus Bastian, 1865; Acrobeloides Cobb, 1924; Mesodorylaimus Andreassy, 1959; Aphelenchus Bastian, 1865, Ditylenchus Filipjev, were other commonly found nematode genera. Meloidogyne incognita, M. javanica, Mesocriconema xenoplax, Longidorus elongatus, Xiphinema index, X. italiae, Praylenchus thornei, and P. neglectus, we identified constitute a severe threat to grape production by causing crop damage or transmitting virus diseases.
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Responses of Fungi to Nutrient-Limiting Conditions and to Inhibitory Substances in Natural Habitats
Article
Fungi, as heterotrophic microorganisms, coexist with numerous other microorganisms, with whom they must compete for a share of nutrients. Since such nutrients, particularly energy substrate, are often in short supply, adaptive traits have evolved that enhance survival (Lockwood, 1977). Moreover, numerous organic metabolic products are produced as a result of microbial degradation of various substrates. These, together with various mineral components of a habitat, also may affect microorganisms, including fungi. In this review we attempt to discuss the responses of fungi to nutrient competition with other microorganisms and to the presence of inhibitory substances that occur in natural environments.
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Influence of Grazing by Collembola on the Activity of Senescent Fungal Colonies Grown on Media of Different Nutrient Concentration
Article
  • Mar 1981
Vermiculite granules were impregnated with four concentrations (3.33, 16.67, 33.36 and 133.36 g l-1) of Czapek Dox solution and were inoculated with the fungus Botrytis cinerea. The cultures were then incubated in respirometers for 30 d before different numbers of Folsomia candida were added. Grazing by Collembola in cultures grown on the lowest nutrient levels produced a significant decline in fungal activity in comparison with controls. However grazing by animals in cultures grown on higher nutrient concentrations did stimulate fungal respiration, producing a maximum increase in cultures containing the highest nutrient levels of over 100% of respiration levels measured in controls. Changes in the numbers of animals in the cultures suggested that fungal respiration followed a bellshaped response to increases in grazing intensity. The results are discussed in relation to the influence of nutrient depletion and the accumulation of toxic metabolites on the response by senescent fungal colonies, in decomposing litter, to soil animal grazing. /// Гранулы вермикулита наполняли раствором Чапека-Докса 4-х концентраций (3,33, 16,67, 33,36, 133,36 г/л) и инокулировали грибом Botrytis cinerea. Культуры инкубировали затем в респирометрах 30 дней, а затем добавляли различное количество коллембол Folsomia candida. Выедание коллемболами культур, растущих при самом низком запасе элементов питания приводит к сильному снижению активности роста грибов в сравнении с контролем. Однако, выедание в культурах с более высокими концентрациями элементов питания стимулирует дыхание грибов, дающее максимум повышения в культурах с наибольшим запасом питательных веществ - свыше 100% по сравнению с контролем. Изменения численности животных в культурах показывают, что кпивая дыхания грибов имеет колоколообразную форму зависимости от интенсивности выедания. Результаты обсуждаются в сврзи с вопросами влияния истощения элементов питания и аккумуляции токсичных метаболитов на реакции старых грибных колоний в разлагающейся подстилке в отношении выедания почвенными животными.
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The Relationship between Protozoan Populations and Biological Activity in Soils
Article
  • Feb 1973
The protozoan populations of soil, both free-living and parasitic, are discussed in relation to their size, distribution, biomass, and metabolic activity. Flagellates, small amoebae, and ciliates are the most widespread and active of free-living forms, while the distribution of parasites is related to the distribution of their hosts. The theory of partial sterilization, which first related protozoan populations to soil fertility, is discussed within the broader context of the soil organic cycle. The role of freeliving protozoa as micropredators and the importance of the soil biomass, as well as fresh plant debris, as a substrate for microbial activity are emphasized. The nature and activity of the microbial population are related to plant productivity and the size of the soil animal biomass. It is suggested that comparatively small changes in population and biomass may be associated with greatly accelerated metabolic turnover wheremicropredation takes place. This suggestion is supported by data from microrespirometry experiments.
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The Influence of Soil Fauna on Decomposition by Micro-organisms in Blanket Bog Litter
Article
  • Feb 1978
(1) Two different methods were used to assess the influence of the enchytraeid Cognettia sphagnetorum Vedj. and the tipulid Molophilus ater (Meigen) on the decomposition of blanket bog litter. The litter and the animals were confined within bags of nylon mesh sufficiently fine to prevent significant loss of particulate matter. Loss of weight over a period of 3 months in the field was measured and also the rate of uptake of oxygen at 10 degrees C by the contents of the bags at the end of the field experiment. (2) The experimental results were analysed using analysis of variance and stepwise multiple regression to assess the effects of litter-type, densities and combinations of animal species, and season, on the processes of weight loss and respiration rate and also on the change of standing crop of the animals used. (3) Season, litter-type, number of enchytraeids and number of tipulids used in the experiment were all shown to have a significant influence on weight loss. One M. ater appeared to have approximately five times the influence of one Cognettia sphagnetorum of one third of its body weight. (4) The rate of uptake of oxygen by the litter bags was shown to be influenced by season and by the type of litter. The rate of respiration of bags with animals was higher than the controls but these differences were not significant. (5) The type of litter had a significant effect on the change in standing crop of C. sphagnetorum. Survival of Molophilus ater was poor except for winter 1971/2 and litter-type and the presence of Cognettia sphagnetorum had a marked effect on change in standing crop. (6) It was concluded that the experiments demonstrated that C. sphagnetorum and Molophilus ater increased the rate of weight-loss of litter and that this was due to increased microbial activity as a result of the feeding activity of the animals.
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