Community history affects the predictability of microbial ecosystem development

Abstract

Microbial communities mediate crucial biogeochemical, biomedical and biotechnological processes, yet our understanding of their assembly, and our ability to control its outcome, remain poor. Existing evidence presents conflicting views on whether microbial ecosystem assembly is predictable, or inherently unpredictable. We address this issue using a well-controlled laboratory model system, in which source microbial communities colonize a pristine environment to form complex, nutrient-cycling ecosystems. When the source communities colonize a novel environment, final community composition and function (as measured by redox potential) are unpredictable, although a signature of the community's previous history is maintained. However, when the source communities are pre-conditioned to their new habitat, community development is more reproducible. This situation contrasts with some studies of communities of macro-organisms, where strong selection under novel environmental conditions leads to reproducible community structure, whereas communities under weaker selection show more variability. Our results suggest that the microbial rare biosphere may have an important role in the predictability of microbial community development, and that pre-conditioning may help to reduce unpredictability in the design of microbial communities for biotechnological applications.

Functional Redundancy and Ecosystem Function — The Soil Microbiota as a Case Study

“…This is particularly important in soils, which exhibit a very high species turnover rate: in one case, the bacterial and archaeal ammonia oxidizing communities in a range of Dutch agricultural soils showed above 50% change in community structure between seasons [61,62]. In another, it was shown that when colonizing a novel environment, the microbial community undergoes drastic rearrangement, and draws heavily from members of the 'rare biosphere' [9,63], a strategy which may be crucial for stressresponse [51].…”

“…Specifically, in microbial systems, where diversity and abundance are extreme and growth rates are rapid, it was formerly assumed that redundancy is so high that diversity and community composition are decoupled from functioning due to the following observations: 1) most microbial species are ubiquitous and present in very low densities, awaiting an opportunity to "bloom"; 2) the rapid adaptability of microbes means that such a system will never be so impoverished as to cease functioning; and 3) the microbial system is so tightly linked to its physical environment that it cannot be studied within the context of cause-effect that is generally necessary for BEF studies. However, recent studies have shown that community composition matters to function [5,6]: in soil, microbial communities exhibit a home-field advantage in decomposing endemic vs. foreign litter [7,8] and different communities do not become more similar when exposed to the same environment [9]. This ongoing discussion has been particularly important in the realm of ecosystem models, where stable physical parameters or very coarse microbial parameters (such as total biomass) are assumed to accurately represent microbial contributions to ecosystem function [10].…”

Functional Redundancy of Soil Microbiota – Does More Always Mean Better?

“…This causes that some ecosystems are functioning properly only in the original environment which is caused by coevolution of microorganisms and their adaptation to environmental conditions (Keiser et al 2011). Moreover, one of the studies has shown that different microbial communities have not become similar under the same conditions, suggesting that the original composition of microorganisms could be a predictor of the responses of a particular ecosystem and its development (Pagaling et al 2014). For that reason, it is increasingly common to classify microorganisms communities not on the basis of their taxonomic affiliation but on their functions.…”

Oscillating microbial dynamics driven by small populations, limited nutrient supply and high death rates

“…In particular, nutrient supply may be unpredictable, nutrient and biomass removal rates may not balance, and population sizes may be small so that random fluctuations due to birth and death events play an important role. Recent studies have shown that microbial communities can undergo unpredictable divergence from similar initial conditions [1], dramatic fluctuations in species composition [2] and even chaotic dynamics [3][4][5][6]. Stochastic models for microbial ecosystem dynamics will be needed to obtain detailed understanding of such results.…”