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Unraveling negative biotic interactions determining soil microbial community assembly and functioning.

ABSTRACT: Microbial communities play important roles in all ecosystems and yet a comprehensive understanding of the ecological processes governing the assembly of these communities is missing. To address the role of biotic interactions between microorganisms in assembly and for functioning of the soil microbiota, we used a top-down manipulation approach based on the removal of various populations in a natural soil microbial community. We hypothesized that removal of certain microbial groups will strongly affect the relative fitness of many others, therefore unraveling the contribution of biotic interactions in shaping the soil microbiome. Here we show that 39% of the dominant bacterial taxa across treatments were subjected to competitive interactions during soil recolonization, highlighting the importance of biotic interactions in the assembly of microbial communities in soil. Moreover, our approach allowed the identification of microbial community assembly rule as exemplified by the competitive exclusion between members of Bacillales and Proteobacteriales. Modified biotic interactions resulted in greater changes in activities related to N- than to C-cycling. Our approach can provide a new and promising avenue to study microbial interactions in complex ecosystems as well as the links between microbial community composition and ecosystem function.

SUBMITTER: Romdhane S

PROVIDER: S-EPMC8692615 | biostudies-literature | 2022 Jan

REPOSITORIES: biostudies-literature

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Unraveling negative biotic interactions determining soil microbial community assembly and functioning.

Romdhane Sana S Spor Aymé A Aubert Julie J Bru David D Breuil Marie-Christine MC Hallin Sara S Mounier Arnaud A Ouadah Sarah S Tsiknia Myrto M Philippot Laurent L

The ISME journal 20210728 1

Microbial communities play important roles in all ecosystems and yet a comprehensive understanding of the ecological processes governing the assembly of these communities is missing. To address the role of biotic interactions between microorganisms in assembly and for functioning of the soil microbiota, we used a top-down manipulation approach based on the removal of various populations in a natural soil microbial community. We hypothesized that removal of certain microbial groups will strongly ...[more]

PMID: 34321619

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Project description:Microbial probiotics are intended to improve functions in diverse ecosystems, yet probiotics often fail to establish in a preexisting microbiome. This is a species invasion problem. The relative importance of the two major factors controlling establishment in this context-propagule pressure (inoculation dose and frequency) and biotic interactions (composition of introduced and resident communities)-is unknown. We tested the effect of these factors in driving microbial composition and functioning following 12 microbial community invasions (e.g., introductions of many microbial invaders) in microcosms. Ecosystem functioning over a 30-day postinvasion period was assessed by measuring activity (respiration) and environment modification (dissolved organic carbon abundance). To test the dependence on environmental context, experiments were performed in two resource environments. In both environments, biotic interactions were more important than propagule pressure in driving microbial composition and community function, but the magnitude of effect varied by environment. Successful invaders comprised approximately 8% of the total number of operational taxonomic units (OTUs). Bacteria were better invaders than fungi, with average relative abundances of 7.4% ± 6.8% and 1.5% ± 1.4% of OTUs, respectively. Common bacterial invaders were associated with stress response traits. The most resilient bacterial and fungal families, in other words, those least impacted by invasions, were linked to antimicrobial resistance or production traits. Illuminating the principles that determine community composition and functioning following microbial invasions is key to efficient community engineering.IMPORTANCE With increasing frequency, humans are introducing new microbes into preexisting microbiomes to alter functioning. Example applications include modification of microflora in human guts for better health and those of soil for food security and/or climate management. Probiotic applications are often approached as trial-and-error endeavors and have mixed outcomes. We propose that increased success in microbiome engineering may be achieved with a better understanding of microbial invasions. We conducted a microbial community invasion experiment to test the relative importance of propagule pressure and biotic interactions in driving microbial community composition and ecosystem functioning in microcosms. We found that biotic interactions were more important than propagule pressure in determining the impact of microbial invasions. Furthermore, the principles for community engineering vary among organismal groups (bacteria versus fungi).

Project description:Soil microbial community assembly is crucial for understanding the mechanisms of microbial communities that regulate ecosystem-level functioning. The relative contributions of stochastic and deterministic processes to microbial community assembly remain poorly defined, and major questions exist concerning the soil organic carbon (SOC) dynamics of microbial community assembly in deep soil. Here, the bacterial community assembly processes were explored across five soil profile depths (up to 80 cm) during a 15-year field experiment involving four fertilization regimes. We found that the bacterial community assembly was initially governed by deterministic selection in topsoil but was progressively structured by increasing stochastic dispersal with depth. The migration rate (m) and β-null deviation pattern supported the hypothesis of a relatively greater influence of dispersal in deep soil, which was correlated with bacterial community assembly by stochastic processes. These changes in the entire community assembly reflected consistent assembly processes of the two most dominant phyla, Acidobacteria and Chloroflexi Structural equation modeling showed that soil features (pH and total phosphorus) and bacterial interactions (competition and network complexity) were significantly related to bacterial community assembly in the 0-to-10-cm and 10-to-20-cm layers. Partial Mantel tests, structural equation modeling, and random forest modeling consistently indicated a strong and significant correlation between bacterial community assemblages and SOC dynamics, implying that bacterial assembly processes would potentially suppress SOC metabolism and mineralization when the contributions of stochastic dispersal to communities increased in deeper layers. Our results have important implications for integrating bacterial community assembly processes into the predictions of SOC dynamics.IMPORTANCE We have provided a framework to better understand the mechanisms governing the balance between stochastic and deterministic processes and to integrate the shifts in community assembly processes with microbial carbon metabolism. Our study reinforced that environmental filtering and bacterial cooccurrence patterns influence the stochastic/deterministic continuum of soil bacterial community assembly and that stochasticity may act through deeper soil layers to influence carbon metabolism. Delineating theoretically the potential linkages between community assembly and SOC dynamics across a broad range of microbial systems represents an interesting topic for future research.

Dataset Information

Unraveling negative biotic interactions determining soil microbial community assembly and functioning.

Publications

Unraveling negative biotic interactions determining soil microbial community assembly and functioning.

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