Write a PREreview

Disturbance is known to affect 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, diversity, and ecosystem function of complex microbial communities within an engineered system. We carried out a microcosm experiment where activated sludge bioreactors were subjected to a range of disturbances in the form of a toxic pollutant, tracking changes in ecosystem function. Microbial communities were assessed by combining distance-based methods, general linear multivariate models, α-diversity indices, and null model analyses on metagenomics and 16S rRNA gene amplicon data. A stronger temporal decrease in α-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. Tradeoffs were observed in community 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-niche assembly processes, is essential to understanding the impact of disturbance in complex microbial communities.

Importance

Microbes drive the Earth’s biogeochemical cycles, yet how they respond to perturbations like anthropogenic pollutants is poorly understood. As human impact continues to increase worldwide, foreseeing how disturbances will affect microbial communities and the ecosystem services they provide is key for ecosystem management and conservation efforts. Employing laboratory-scale wastewater treatment bioreactors, this study shows that changes in community diversity accompany variations in the underlying deterministic-stochastic assembly mechanisms. Disturbances could promote stochastic community structuring, which despite harboring higher diversity could lead to variable overall function, possibly explaining why after similar perturbations the process outcome differs. A conceptual framework, termed the ‘intermediate stochasticity hypothesis’ is proposed to theoretically predict bacterial community shifts in diversity and ecosystem function, given a range of possible disturbance types, in a well-replicated time-series experiment. Our findings are relevant for managing complex microbial systems, which could display similar responses to disturbance, like oceans, soils or the human gut.