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Frequency of disturbance alters diversity, function, and underlying assembly mechanisms of complex bacterial communities.

ABSTRACT: Disturbance is known to affect the ecosystem structure, but predicting its outcomes remains elusive. Similarly, community diversity is believed to relate to ecosystem functions, yet the underlying mechanisms are poorly understood. Here, we tested the effect of disturbance on the structure, assembly, and ecosystem function of complex microbial communities within an engineered system. We carried out a microcosm experiment where activated sludge bioreactors operated in daily cycles were subjected to eight different frequency levels of augmentation with a toxic pollutant, from never (undisturbed) to every day (press-disturbed), for 35 days. Microbial communities were assessed by combining distance-based methods, general linear multivariate models, ?-diversity indices, and null model analyses on metagenomics and 16S rRNA gene amplicon data. A stronger temporal decrease in ?-diversity at the extreme, undisturbed and press-disturbed, ends of the disturbance range led to a hump-backed pattern, with the highest diversity found at intermediate levels of disturbance. Undisturbed and press-disturbed levels displayed the highest community and functional similarity across replicates, suggesting deterministic processes were dominating. The opposite was observed amongst intermediately disturbed levels, indicating stronger stochastic assembly mechanisms. Trade-offs were observed in the ecosystem function between organic carbon removal and both nitrification and biomass productivity, as well as between diversity and these functions. Hence, not every ecosystem function was favoured by higher community diversity. Our results show that the assessment of changes in diversity, along with the underlying stochastic-deterministic assembly processes, is essential to understanding the impact of disturbance in complex microbial communities.

SUBMITTER: Santillan E

PROVIDER: S-EPMC6370796 | biostudies-literature | 2019

REPOSITORIES: biostudies-literature

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Project description:Press disturbances are of interest in microbial ecology, as they can drive microbial communities to alternative stable states. However, the effect of press disturbances in community assembly mechanisms, particularly with regard to taxa and functional genes at different levels of abundance (i.e., common and rare), remains largely unknown. Here, we tested the effect of a continuous alteration in substrate feeding scheme on the structure, function, and assembly of bacterial communities. Two sets of replicate 5-liter sequencing batch reactors were operated at two different organic carbon loads for a period of 74 days, following 53 days of acclimation after inoculation with sludge from a full-scale treatment plant. Temporal dynamics of community taxonomic and functional gene structure were derived from metagenomics and 16S rRNA gene metabarcoding data. Disturbed reactors exhibited different community function, structure, and assembly compared to undisturbed reactors. Bacterial taxa and functional genes showed dissimilar α-diversity and community assembly patterns. Deterministic assembly mechanisms were generally stronger in disturbed reactors and in common fractions compared to rare ones. Function quickly recovered after the disturbance was removed, but community structure did not. Our results highlight that functional gene data from metagenomics can indicate patterns of community assembly that differ from those obtained from taxon data. This study reveals how a joint evaluation of assembly mechanisms and community structure of bacterial taxa and functional genes as well as ecosystem function can unravel the response of complex microbial systems to a press disturbance.IMPORTANCE Ecosystem management must be viewed in the context of increasing frequencies and magnitudes of various disturbances that occur at different scales. This work provides a glimpse of the changes in assembly mechanisms found in microbial communities exposed to sustained changes in their environment. These mechanisms, deterministic or stochastic, can cause communities to reach a similar or variable composition and function. For a comprehensive view, we use a joint evaluation of temporal dynamics in assembly mechanisms and community structure for both bacterial taxa and their functional genes at different abundance levels, in both disturbed and undisturbed states. We further reverted the disturbance state to contrast recovery of function with community structure. Our findings are relevant, as very few studies have employed such an approach, while there is a need to assess the relative importance of assembly mechanisms for microbial communities across different spatial and temporal scales, environmental gradients, and types of disturbance.

Project description:Diversity is often associated with the functional stability of ecological communities from microbes to macroorganisms. Understanding how diversity responds to environmental perturbations and the consequences of this relationship for ecosystem function are thus central challenges in microbial ecology. Unimodal diversity-disturbance relationships, in which maximum diversity occurs at intermediate levels of disturbance, have been predicted for ecosystems where life history tradeoffs separate organisms along a disturbance gradient. However, empirical support for such peaked relationships in macrosystems is mixed, and few studies have explored these relationships in microbial systems. Here we use complex microbial microcosm communities to systematically determine diversity-disturbance relationships over a range of disturbance regimes. We observed a reproducible switch between community states, which gave rise to transient diversity maxima when community states were forced to mix. Communities showed reduced compositional stability when diversity was highest. To further explore these dynamics, we formulated a simple model that reveals specific regimes under which diversity maxima are stable. Together, our results show how both unimodal and non-unimodal diversity-disturbance relationships can be observed as a system switches between two distinct microbial community states; this process likely occurs across a wide range of spatially and temporally heterogeneous microbial ecosystems. The diversity of microbial communities is linked to the functioning and stability of ecosystems. As humanity continues to impact ecosystems worldwide, and as diet and disease perturb our own commensal microbial communities, the ability to predict how microbial diversity will respond to disturbance is of critical importance. Using microbial microcosm experiments, we find that community diversity responds to different disturbance regimes in a reproducible and predictable way. Maximum diversity occurs when two communities, each suited to different environmental conditions, are mixed due to disturbance. This maximum diversity is transient except under specific regimes. Using a simple mathematical model, we show that transient unimodality is likely a common feature of microbial diversity-disturbance relationships in fluctuating environments.

Project description:Dispersal can influence the response of bacterial communities to environmental changes and disturbances. However, the extent to which dispersal contributes to the community response in dependence of the character and strength of the disturbance remains unclear. Here, we conducted a transplant experiment using dialysis bags in which bacterioplankton originating from brackish and marine regions of the Saint Lawrence Estuary were reciprocally incubated in the two environments for 5 days. Dispersal treatments were set-up by subjecting half of the microcosms in each environment to an exchange of cells between the marine and brackish assemblages at a daily exchange rate of 6% (v/v), and the other half of microcosms were kept as the non-dispersal treatments. Bacterial 16S rRNA sequencing was then used to examine the diversity and composition of the active communities. Alpha diversity of the marine communities that were exposed to the brackish environment was elevated greatly by dispersal, but declined in the absence of dispersal. This indicates that dispersal compensated the loss of diversity in the marine communities after a disturbance by introducing bacterial taxa that were able to thrive and coexist with the remaining community members under brackish conditions. On the contrary, alpha diversity of the brackish communities was not affected by dispersal in either environment. Furthermore, dispersal led to an increase in similarity between marine and brackish communities in both of the environments, with a greater similarity when the communities were incubated in the brackish environment. These results suggest that the higher initial diversity in the brackish than in the marine starting community made the resident community less susceptible to dispersing bacteria. Altogether, this study shows that dispersal modifies the diversity and composition of the active communities in response to a salinity disturbance, and enables the local adjustment of specific bacteria under brackish environmental conditions.

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Frequency of disturbance alters diversity, function, and underlying assembly mechanisms of complex bacterial communities.

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