Summary
The importance of assembly processes in shaping biological communities is poorly understood, especially for microbes. Here, we report on the forces that structure soil bacterial communities ...along a 2000 m elevational gradient. We characterized the relative importance of habitat filtering and competition on phylogenetic structure and turnover in bacterial communities. Bacterial communities exhibited a phylogenetically clustered pattern and were more clustered with increasing elevation. Biotic factors (i.e., relative abundance of dominant bacterial lineages) appeared to be most important to the degree of clustering, evidencing the role of the competitive ability of entire clades in shaping the communities. Phylogenetic turnover showed the greatest correlation to elevation. After controlling the elevation, biotic factors showed greater correlation to phylogenetic turnover than all the habitat variables (i.e., climate, soil and vegetation). Structural equation modelling also identified that elevation and soil organic matter exerted indirect effects on phylogenetic diversity and turnover by determining the dominance of microbial competitors. Our results suggest that competition among bacterial taxa induced by soil carbon contributes to the phylogenetic pattern across elevational gradient in the Tibetan Plateau. This highlights the importance of considering not only abiotic filtering but also biotic interactions in soil bacterial communities across stressful elevational gradients.
In the last two decades, a change in land use has taken place in Europe. Manures that used to be applied to agricultural soils are now used in biogas reactors, and instead, digestate is applied. ...Here, we simulated soil amendment with either fresh or anaerobically digested cattle manure. The aim was to investigate the resilience of the resident microbiota and detect differences in the microbial biomass and activity after fertilizer amendment. Furthermore, the physiological community profile and the role of the indigenous microbial community was elucidated. In a microcosm experiment, two kinds of agricultural soil (γ-irradiated versus non-irradiated) were amended with either treatment. The effect of amendments on the community composition and physiological activity was tested immediately, after 1 and 3 months of incubation through 16S rRNA gene amplicon sequencing (initial soil community), genetic and physiological profiling (PCR-DGGE and MicroResp™), and measurement of basal respiration and microbial biomass. Either fertilizer did not affect the community composition of dominant fungi and bacteria in non-irradiated soils. This indicates the ability of the indigenous microbiota to outcompete allochthonous microorganisms. Soil microbial biomass was not changed, whereas basal respiration was significantly higher after amendment, especially when using fresh manure. MicroResp™ revealed slightly higher respiration for some substrates after 1 month; this finding was, however, not persistent and similar for manure and digestate. Generally, after 1 month, treatments returned to control levels for all parameters. In conclusion, amendment with anaerobically digested manure did not have a greater impact on soil microbial properties.
Plant genetic variation, through its phenotypic display, can determine the composition of below ground microbial communities. Variation within a species is increasingly acknowledged to have ...substantial ecological consequences, particularly through trophic cascades. We hypothesized that the intraspecific genotypic variation of the tree host might impact the phylogenetic composition of its rhizospheric microbial communities, by favouring particular clades, that might be further reflected in ecosystem process rates.
We tested whether the intraspecific genotypic variation of Pinus pinaster modulates nutrient cycling by determining the phylogenetic structure of its symbiotic ectomycorrhizal fungi and rhizospheric bacteria. We sequenced fungal and bacterial molecular markers and reconstructed phylogenies in the rhizosphere of P. pinaster trees belonging to three genotypic variants (Mediterranean, Atlantic, African) in three 45‐year‐old common garden experiments, and measured seven soil enzymatic activities.
Local effects, based on differences in elevation and soil conditions across sites, were strong predictors of the ectomycorrhizal and bacterial communities thriving in tree’s rhizosphere. Across‐site variation also explained differences in phosphorus cycling. We detected, however, a significant effect of the plant genotype on the phylogenetic structure of the root‐associated microbiota that was consistent across sites.
The most productive Mediterranean plant genotype sheltered the most distinct root microbiome, with the dominant Basidiomycetes and Proteobacteria having a strong influence on the phylogenetic microbial community structure and associating with an enhanced hydrolysis of celluloses, hemicelluloses and chitin. Beneath the less productive Atlantic genotype, the less abundant Ascomycetes and up to thirteen bacterial phyla shaped the phylogenetic microbial structure, and predicted the rates of peptidase. Ectomycorrhizal fungi explained the activity of cellulases and protease, and bacteria that of hemicellulases and chitinase, suggesting functional complementarity.
Synthesis. This is the first report using three‐replicated long‐term common gardens in mature forests to disentangle plant genotype‐ and site‐specific drivers of the rhizospheric microbiome and its enzymatic potential. We concluded that intraspecific variation in primary producers leaves a phylogenetic signature in mutualists and decomposers that further modulate key steps in carbon and nitrogen cycles. These results emphasize the ecological relevance of plant intraspecific diversity in determining essential plant–soil feedbacks that control ecosystem productivity and performance.
This is the first report using three‐replicated long‐term common gardens in mature forests to disentangle plant genotype‐ and site‐specific drivers of the rhizospheric microbiome and its enzymatic potential. We concluded that intraspecific variation in primary producers leaves a phylogenetic signature in mutualists and decomposers that further modulate key steps in carbon and nitrogen cycles. These results emphasize the ecological relevance of plant intraspecific diversity in determining essential plant–soil feedbacks that control ecosystem productivity and performance.
Competition can lead to the exclusion of bacterial taxa when there is a transitive relationship among competitors with a hierarchy of competitive success. However, competition may not prevent ...bacterial coexistence if competitors form intransitive loops, in which none is able to outcompete all the rest. Both transitive and intransitive competition have been demonstrated in bacterial model systems. However, in natural soil microbial assemblages competition is typically understood as a dominance relationship leading to the exclusion of weak competitors. Here, we argue that transitive and intransitive interactions concurrently determine the structure of soil microbial communities. We explain why pairwise interactions cannot depict competition correctly in complex communities, and propose an alternative through the detection of strongly connected components (SCCs) in microbial networks. We finally analyse the existence of SCCs in soil bacterial communities in two Mediterranean ecosystems, for illustrative purposes only (rather than with the aim of providing a methodological tool) due to current limitations, and discuss future avenues to experimentally test the existence of SCCs in nature.
Fire alters the structure and composition of above‐ and belowground communities with concurrent shifts in phylogenetic diversity. The inspection of postfire trends in the diversity of ecological ...communities incorporating phylogenetic information allows to better understand the mechanisms driving fire resilience. While fire reduces plant phylogenetic diversity based on the recruitment of evolutionarily related species with postfire seed persistence, it increases that of soil microbes by limiting soil resources and changing the dominance of competing microbes. Thus, during postfire community reassembly, plant and soil microbes might experience opposing temporal trends in their phylogenetic diversity that are linked through changes in the soil conditions. We tested this hypothesis by investigating the postfire evolution of plant and soil microbial (fungi, bacteria and archaea) communities across three 20‐year chronosequences. Plant phylogenetic diversity increased with time since fire as pioneer seeders facilitate the establishment of distantly related late‐successional shrubs. The postfire increase in plant phylogenetic diversity fostered plant productivity, eventually recovering soil organic matter. These shifts over time in the soil conditions explained the postfire restoration of fungal and bacterial phylogenetic diversity, which decreased to prefire levels, suggesting that evolutionarily related taxa with high relative fitness recover their competitive superiority during community reassembly. The resilience to fire of phylogenetic diversity across biological domains helps preserve the evolutionary history stored in our ecosystems.
Nurse plants drive the assembly of facilitated communities and commonly promote plant–soil feedbacks, and are thus recognized as key engineers in abiotically stressful ecosystems. The literature ...neglects; however, the role of the communities which benefit from the presence of the nurse as contributors to soil ecosystem functions. We hypothesized that the nurse and its beneficiaries synergistically enhance essential ecosystem functions mediated by soil microbiota.
To track how plant–plant facilitation impacts plant–soil feedbacks, we selected three nurse species in semi‐arid mine tailings and defined three microsites (open space, nurse canopy and nurse + facilitated canopy). In each microsite, we quantified 18 abiotic and biotic variables associated with four functions: reduction in climatic stress, reduction in edaphic stress, soil fertility and soil microbial productivity (decomposition and nutrient cycling).
Litter biomass increased from open spaces to the microsite beneath the nurses, and further beneath the nurses and their beneficiaries. Litter biomass was a good predictor of both the reduction in climatic stress and increase in edaphic stress (likely owing to metal bioaccumulation). We attributed increments in soil organics and heterotrophic respiration beneath the nurses and their beneficiaries, compared to nurses alone, to biomass effects through increased litter deposition. Variation in fertility and microbial productivity among microsites shaped by the nurses and their facilitated communities was attributed to both diversity and biomass effects. In particular, fertility was promoted beneath phenotypically diverse facilitated communities, as inferred from ten above‐ and below‐ground traits. However, microbial productivity increased at low levels of root biomass likely due to reduced plant–microbe competition for nutrients.
Synthesis. Our results show that facilitated plant communities sheltered by nurse species relieve local abiotic stress and promote plant–microbe interactions, both through biomass and biodiversity effects. These observations shift the conception of facilitated species from simple beneficiaries of the nurse's effects to co‐drivers of essential ecosystem functions.
Resumen
Las plantas nodriza actúan como especies clave ensamblando la comunidad vegetal y promoviendo las interacciones planta‐suelo en ecosistemas de alto estrés gobernados por facilitación. Sin embargo, habitualmente se ignora el papel adicional que la comunidad de especies facilitadas puede ejercer sobre las funciones ecosistémicas del suelo. En este trabajo hipotetizamos que la comunidad de plantas facilitadas contribuye sinérgicamente con la nodriza a la mejora de funciones ecosistémicas mediadas por la microbiota edáfica.
Para evaluar cómo la facilitación entre plantas promueve las interacciones planta‐suelo seleccionamos tres nodrizas en depósitos mineros con vegetación parcheada en ambientes semiáridos y definimos tres micrositios (claro, copa bajo nodriza y copa bajo nodriza con comunidad de facilitadas). Posteriormente, cuantificamos en dichos micrositios 18 variables abióticas y bióticas relacionadas con cuatro funciones principales: reducción del estrés climático, reducción del estrés edáfico, fertilidad edáfica y productividad microbiana (descomposición y ciclado de nutrientes).
La biomasa de hojarasca aumentó en el sentido claro < nodriza <nodriza con facilitadas, y fue un buen predictor de la reducción del estrés climático, aunque incrementó la concentración edáfica de algunos metales pesados. Observamos un incremento de la fertilidad y de la respiración heterotrófica en el micrositio nodriza con facilitadas con respecto a la nodriza, que atribuimos a un efecto del aumento en biomasa (biomass effect) promovido por una mayor deposición de hojarasca. La variabilidad en la fertilidad y productividad microbiana bajo la nodriza con facilitadas la atribuimos tanto a un efecto de la variación en biomasa como en diversidad (diversity effect). En particular, la fertilidad se incrementó en comunidades de facilitadas más diversas fenotípicamente (fenotipo medido a partir de 10 rasgos aéreos y subterráneos). Por el contrario, la productividad microbiana aumentó en micrositios nodriza + facilitada con una menor biomasa de raíces, probablemente debido a una menor competencia planta‐microorganismo por los nutrientes.
Síntesis. Nuestros resultados cambian la concepción de las especies facilitadas como meras beneficiarias de la presencia de una nodriza, para atribuirles un papel como promotoras de funciones ecosistémicas esenciales, mediadas por los efectos de la diversidad y biomasa sobre el estrés abiótico y las interacciones con la microbiota edáfica.
Our results show that facilitated plant communities sheltered by nurse species relieve local abiotic stress and promote plant–microbe interactions, both through biomass and biodiversity effects. These observations shift the conception of facilitated species from simple beneficiaries of the nurse’s effects to co‐drivers of essential ecosystem functions.
Microorganisms are vital in mediating the earth's biogeochemical cycles; yet, despite our rapidly increasing ability to explore complex environmental microbial communities, the relationship between ...microbial community structure and ecosystem processes remains poorly understood. Here, we address a fundamental and unanswered question in microbial ecology: 'When do we need to understand microbial community structure to accurately predict function?' We present a statistical analysis investigating the value of environmental data and microbial community structure independently and in combination for explaining rates of carbon and nitrogen cycling processes within 82 global datasets. Environmental variables were the strongest predictors of process rates but left 44% of variation unexplained on average, suggesting the potential for microbial data to increase model accuracy. Although only 29% of our datasets were significantly improved by adding information on microbial community structure, we observed improvement in models of processes mediated by narrow phylogenetic guilds via functional gene data, and conversely, improvement in models of facultative microbial processes via community diversity metrics. Our results also suggest that microbial diversity can strengthen predictions of respiration rates beyond microbial biomass parameters, as 53% of models were improved by incorporating both sets of predictors compared to 35% by microbial biomass alone. Our analysis represents the first comprehensive analysis of research examining links between microbial community structure and ecosystem function. Taken together, our results indicate that a greater understanding of microbial communities informed by ecological principles may enhance our ability to predict ecosystem process rates relative to assessments based on environmental variables and microbial physiology.
Summary
Fire alters ecosystems by changing the composition and community structure of soil microbes. The phylogenetic structure of a community provides clues about its main assembling mechanisms. ...While environmental filtering tends to reduce the community phylogenetic diversity by selecting for functionally (and hence phylogenetically) similar species, processes like competitive exclusion by limiting similarity tend to increase it by preventing the coexistence of functionally (and phylogenetically) similar species. We used co‐occurrence networks to detect co‐presence (bacteria that co‐occur) or exclusion (bacteria that do not co‐occur) links indicative of the ecological interactions structuring the community. We propose that inspecting the phylogenetic structure of co‐presence or exclusion links allows to detect the main processes simultaneously assembling the community. We monitored a soil bacterial community after an experimental fire and found that fire altered its composition, richness and phylogenetic diversity. Both co‐presence and exclusion links were more phylogenetically related than expected by chance. We interpret such a phylogenetic clustering in co‐presence links as a result of environmental filtering, while that in exclusion links reflects competitive exclusion by limiting similarity. This suggests that environmental filtering and limiting similarity operate simultaneously to assemble soil bacterial communities, widening the traditional view that only environmental filtering structures bacterial communities.
Quantifying diversity with phylogeny-informed metrics helps understand the effects of diversity on ecosystem functioning (EF). The sign of these effects remains controversial because phylogenetic ...diversity and taxonomic identity may interactively influence EF. Positive relationships, traditionally attributed to complementarity effects, seem unimportant in natural soil bacterial communities. Negative relationships could be attributed to fitness differences leading to the overrepresentation of few productive clades, a mechanism recently invoked to assemble soil bacteria communities. We tested in two ecosystems contrasting in terms of environmental heterogeneity whether two metrics of phylogenetic community structure, a simpler measure of phylogenetic diversity (NRI) and a more complex metric incorporating taxonomic identity (PCPS), correctly predict microbially mediated EF. We show that the relationship between phylogenetic diversity and EF depends on the taxonomic identity of the main coexisting lineages. Phylogenetic diversity was negatively related to EF in soils where a marked fertility gradient exists and a single and productive clade (Proteobacteria) outcompete other clades in the most fertile plots. However, phylogenetic diversity was unrelated to EF in soils where the fertility gradient is less marked and Proteobacteria coexist with other abundant lineages. Including the taxonomic identity of bacterial lineages in metrics of phylogenetic community structure allows the prediction of EF in both ecosystems.
The relationship between phylogenetic diversity and ecosystem functioning is dependent on the taxonomic identity of the main coexisting bacterial lineages.
Summary
Denitrification causes nitrogen losses from terrestrial ecosystems. The magnitude of nitrogen loss depends on the prevalence of denitrifiers, which show ecological differences if they harbour ...nirS or nirK genes encoding nitrite reductases with the same biological function. Thus, it is relevant to understand the mechanisms of co‐existence of denitrifiers, including their response to environmental filters and competition due to niche similarities. We propose a framework to analyse the co‐existence of denitrifiers across multiple assemblages by using nir gene‐based co‐occurrence networks. We applied it in Mediterranean soils before and during 1 year after an experimental fire. Burning did not modify nir community structure, but significantly impacted co‐occurrence patterns. Bacteria with the same nir co‐occurred in space, and those with different nir excluded each other, reflecting niche requirements: nirS abundance responded to nitrate and salinity, whereas nirK to iron content. Prior to fire, mutual exclusion between bacteria with the same nir suggested competition due to niche similarities. Burning provoked an immediate rise in mineral nitrogen and erased the signals of competition, which emerged again within days as nir abundances peaked. nir co‐occurrence patterns can help infer the assembly mechanisms of denitrifying communities, which control nitrogen losses in the face of ecological disturbance.
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