Species interactions constrain adaptation and preserve ecological stability in an experimental microbial community

Jake N Barber,Michael J Mcdonald,Aysha L Sezmis,Jane Hawkey,Luke C Nicholson,Kathryn E Holt,Laura C Woods,Louise M Judd

doi:10.1038/s41396-022-01191-1

Jake N Barber, Michael J Mcdonald + Show 6 more

Open Access

https://doi.org/10.1038/s41396-022-01191-1

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Abstract

Species loss within a microbial community can increase resource availability and spur adaptive evolution. Environmental shifts that cause species loss or fluctuations in community composition are expected to become more common, so it is important to understand the evolutionary forces that shape the stability and function of the emergent community. Here we study experimental cultures of a simple, ecologically stable community of Saccharomyces cerevisiae and Lactobacillus plantarum, in order to understand how the presence or absence of a species impacts coexistence over evolutionary timescales. We found that evolution in coculture led to drastically altered evolutionary outcomes for L. plantarum, but not S. cerevisiae. Both monoculture- and co-culture-evolved L. plantarum evolved dozens of mutations over 925 generations of evolution, but only L. plantarum that had evolved in isolation from S. cerevisiae lost the capacity to coexist with S. cerevisiae. We find that the evolutionary loss of ecological stability corresponds with fitness differences between monoculture-evolved L. plantarum and S. cerevisiae and genetic changes that repeatedly evolve across the replicate populations of L. plantarum. This work shows how coevolution within a community can prevent destabilising evolution in individual species, thereby preserving ecological diversity and stability, despite rapid adaptation.

Highlights

Microbial communities are bound by a range of competitive and cooperative interactions [1], and a growing number of experimental studies show that changes in species composition can drastically alter the course of evolution for those species that remain [2,3,4,5,6,7,8,9,10,11,12,13]
L. plantarum and S. cerevisiae are ecologically stable in coculture and occupy distinct niches We obtained an isolate of L. plantarum from a sourdough bread culture (Methods), established laboratory cultures and carried out reciprocal invasion assays to determine whether L. plantarum and S. cerevisiae could establish an ecologically stable co-culture
After passaging for 10 days (5 transfers), we found that all replicate co-cultures (n = 15) converged upon a stable equilibrium frequency, with an average L. plantarum frequency of 47.7% (95% Confidence Interval (CI) [44.8%, 50.7%], range [22.2–64.7%]) (Fig. 1A)

Summary

Introduction

Microbial communities are bound by a range of competitive and cooperative interactions [1], and a growing number of experimental studies show that changes in species composition can drastically alter the course of evolution for those species that remain [2,3,4,5,6,7,8,9,10,11,12,13]. Incorporating multiple species into experimental, multigenerational cultures has revealed a range of outcomes, including accelerated molecular and fitness evolution [14, 15], decelerated fitness evolution [14], more efficient use of resources [5, 16,17,18], and community stabilisation [7, 8, 17]. These results highlight that, in addition to the environment, the identity and role of a species in the community are crucial for determining the outcome of evolution. Another result from studies of laboratory bacterial communities is that the opportunities for adaptation diminish when there are more species in the co-culture [21] and that reducing the number of species in a community increases the opportunity for adaptation [16, 22, 23]

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Conclusion