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The impact of failure: unsuccessful bacterial invasions steer the soil microbial community away from the invader's niche.

ABSTRACT: Although many environments like soils are constantly subjected to invasion by alien microbes, invaders usually fail to succeed, succumbing to the robust diversity often found in nature. So far, only successful invasions have been explored, and it remains unknown to what extent an unsuccessful invasion can impact resident communities. Here we hypothesized that unsuccessful invasions can cause impacts to soil functioning by decreasing the diversity and niche breadth of resident bacterial communities, which could cause shifts to community composition and niche structure-an effect that is likely exacerbated when diversity is compromised. To examine this question, diversity gradients of soil microbial communities were subjected to invasion by the frequent, yet oft-unsuccessful soil invader, Escherichia coli, and evaluated for changes to diversity, bacterial community composition, niche breadth, and niche structure. Contrary to expectations, diversity and niche breadth increased across treatments upon invasion. Community composition and niche structure were also altered, with shifts of niche structure revealing an escape by the resident community away from the invader's resources. Importantly, the extent of the escape varied in response to the community's diversity, where less diverse communities experienced larger shifts. Thus, although transient and unsuccessful, the invader competed for resources with resident species and caused tangible impacts that modified both the diversity and functioning of resident communities, which can likely generate a legacy effect that influences future invasion attempts.

SUBMITTER: Mallon CA

PROVIDER: S-EPMC5864238 | biostudies-literature | 2018 Mar

REPOSITORIES: biostudies-literature

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The impact of failure: unsuccessful bacterial invasions steer the soil microbial community away from the invader's niche.

Mallon C A CA Le Roux X X van Doorn G S GS Dini-Andreote F F Poly F F Salles J F JF

The ISME journal 20180126 3

Although many environments like soils are constantly subjected to invasion by alien microbes, invaders usually fail to succeed, succumbing to the robust diversity often found in nature. So far, only successful invasions have been explored, and it remains unknown to what extent an unsuccessful invasion can impact resident communities. Here we hypothesized that unsuccessful invasions can cause impacts to soil functioning by decreasing the diversity and niche breadth of resident bacterial communiti ...[more]

PMID: 29374268

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Project description:BackgroundCommunity-driven invasion, also known as community coalescence, occurs widely in natural ecosystems. Despite that, our knowledge about the process and mechanisms controlling community-driven invasion in soil ecosystems is lacking. Here, we performed a set of coalescence experiments in soil microcosms and assessed impacts up to 60 days after coalescence by quantifying multiple traits (compositional, functional, and metabolic) of the invasive and coalescent communities.ResultsOur results showed that coalescences significantly triggered changes in the resident community's succession trajectory and functionality (carbohydrate metabolism), even when the size of the invasive community is small (~ 5% of the resident density) and 99% of the invaders failed to survive. The invasion impact was mainly due to the high suppression of constant residents (65% on average), leading to a lose-lose situation where both invaders and residents suffered with coalescence. Our results showed that surviving residents could benefit from the coalescence, which supports the theory of "competition-driven niche segregation" at the microbial community level. Furthermore, the result showed that both short- and long-term coalescence effects were predicted by similarity and unevenness indexes of compositional, functional, and metabolic traits of invasive communities. This indicates the power of multi-level traits in monitoring microbial community succession. In contrast, the varied importance of different levels of traits suggests that competitive processes depend on the composition of the invasive community.ConclusionsOur results shed light on the process and consequence of community coalescences and highlight that resource competition between invaders and residents plays a critical role in soil microbial community coalescences. These findings provide valuable insights for understanding and predicting soil microbial community succession in frequently disturbed natural and agroecosystems. Video Abstract.

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.

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).

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The impact of failure: unsuccessful bacterial invasions steer the soil microbial community away from the invader's niche.

Publications

The impact of failure: unsuccessful bacterial invasions steer the soil microbial community away from the invader's niche.

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