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

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

doi:10.1038/s41396-022-01191-1

Cited by 36 publications

(17 citation statements)

References 78 publications

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“…In this study, we uniquely assess alteration of bacterial niche space for two phylogenetically distinct taxa after conditioning within five physiochemically distinct soil environments. Overall, our work agrees with other studies, which have highlighted the potential for rapid adaptive diversification by bacteria released from biotic pressures (Barber et al, 2022; Gómez & Buckling, 2013; Scheuerl et al, 2020). Multiple factors have been investigated as drivers of this change, including resource partitioning, seasonality, and spatial heterogeneity (Levin, 1972; Spencer et al, 2007; Travisano & Rainey, 2000).…”

Section: Discussionsupporting

confidence: 93%

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Rapid niche shifts in bacteria following conditioning in novel soil environments

et al. 2022

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1. Realized niche breadth is generally expected to be smaller than fundamental niche breadth. For soil microorganisms, this is due in part to competition from co-occurring microbes, so removing competitors should allow for expanded use of resource and habitats (i.e. ecological release).2. We hypothesized that conditioning bacterial isolates to biotically cleared soils would allow for niche breadth expansion relative to ancestral bacteria, and that this niche expansion would be driven by habitat-dependent niche shifts between derived populations. We grew two taxonomically divergent bacteria for 3 months in four biotically cleared soils and a biotically cleared 'home' soil. We then assessed changes in the niche breadth and fitness (i.e. growth; respiration; carbon resource use) of conditioned bacteria.3. Post-conditioning, Pseudomonas populations showed the potential for increased growth rate in-culture and in-soil when conditioned to soils, and constrained resource use relative to the ancestral population, while Paenibacillus showed minimal changes in soil habitat breadth, but expanded resource use in conditioned populations. 4. When introduced into complex novel environments containing reduced biotic pressure, soil bacteria can undergo rapid niche shifts, but this response varies across taxa and habitats. This suggests that species identity and habitat should interact to shape near-term niche shifts when microbes establish in new soil environments.

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Section: Discussionsupporting

confidence: 93%

“…In this study, we uniquely assess alteration of bacterial niche space for two phylogenetically distinct taxa after conditioning within five (Barber et al, 2022;Gómez & Buckling, 2013;Scheuerl et al, 2020).…”

Section: Discussionmentioning

confidence: 99%

Rapid niche shifts in bacteria following conditioning in novel soil environments

et al. 2022

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“…Our evolution experiment demonstrates how biotic interactions might facilitate the generation of strain diversity within microbiomes. These data also contribute to an emerging body of work demonstrating that microbes have very different evolutionary outcomes when biotic complexity is incorporated into experimental evolution (30,33,35,36,91,92). Because most medically and industrially important microbes often live with other microbial species that may impose strong biotic selection on target microbial species (23,25,93,94), management and engineering of microbiomes may need to incorporate how microbe-microbe interactions can shape evolution of microbial species.…”

Section: Debaryomyces Alone Treatmentmentioning

confidence: 90%

Species interactions promote parallel evolution of global transcriptional regulators in a widespreadStaphylococcusspecies

Cosetta

Niccum

Kamkari

et al. 2022

Preprint

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Experimental studies of microbial evolution have largely focused on monocultures of model organisms, but most microbes live in communities where interactions with other species may impact rates and modes of evolution. Using the cheese rind model microbial community, we determined how species interactions shape the evolution of the widespread food- and animal-associated bacterium Staphylococcus xylosus. We evolved S. xylosus for 450 generations alone or in co-culture with one of three microbes: the yeast Debaryomyces hansenii, the bacterium Brevibacterium aurantiacum, and the mold Penicillium solitum. We used the frequency of colony morphology mutants (pigment and colony texture phenotypes) and whole-genome sequencing of isolates to quantify phenotypic and genomic evolution after 15 weeks of the evolution. The yeast D. hansenii strongly promoted diversification of S. xylosus; by the end of the experiment, all populations co-cultured with the yeast were dominated by pigment and colony morphology mutant phenotypes. Populations of S. xylosus grown alone, with Brevibacterium, or with Penicillium did not evolve novel phenotypic diversity. Whole-genome sequencing of individual mutant isolates across all four treatments revealed numerous unique mutations in the operons for the SigB, Agr, and WalKR global regulators, but only in the D. hansenii treatment. Phenotyping and RNA-seq experiments demonstrated that these mutations altered pigment and biofilm production, spreading, stress tolerance, and metabolism of S. xylosus. Fitness experiments revealed trade-offs of these mutations across biotic environments caused by antagonistic pleiotropy, where beneficial mutations that evolved in the presence of the yeast Debaryomyces had strong negative fitness effects in other biotic environments.

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“…Previous studies have proposed a variety of explanations for the impact of diversity on ecosystem functions, including more efficient utilization of resources due to increased niche differentiation and resource exploitation (17), and the more likely emergence of species with crucial functional characteristics (18). The key to the difficulty in unifying these explanations is that the relationship between different species composition and community function and stability is inconsistent, which depends on the species' function, abundance, and interaction with other species (19,20). Recent studies have shown that there are also keystone taxa in microbial communities, which drive microbiome structure and function regardless of their abundance (21,22).…”

Section: Introductionmentioning

confidence: 99%

Keystone taxa responsible for the microbial community stability and performance of activated sludges

Liu

Fang

Liu

et al. 2023

Preprint

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Background: The functions and stability of a community depend on its species, which form complex interaction networks. The keystone taxa identified by network analysis are generally considered to play a vital role in the structure and function of microbial communities, but there is no uniformly accepted operational definition of such taxa. Further, what species and how they affect the community's stability and function are still poorly understood. Methods: To solve this problem, we performed a large-scale network analysis of the microbial communities residing in 1186 activated sludge (AS) samples. Results: We found that the AS co-occurrence network is a typical scale-free network. While most taxa in the AS co-occurrence network have little association, there are still a small number of taxa that are strongly interconnected. We defined a group of keystone taxa that have an important impact on network stability. Further analysis results indicate that the communities harboring the keystone taxa maintain higher stability, but these communities possess lower pollutant removal rates. In addition, we found that keystone taxa were more likely to appear in samples with lower sludge load. Conclusions: Our work identified the keystone taxa that maintain the stability of microbial communities in the AS systems but at the cost of reducing their function. This finding shed light on the relationship between composition, stability, and function within microbial communities. It also provides novel insights into manipulating the function of microbial communities by modifying their composition.

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

Cited by 36 publications

References 78 publications

Rapid niche shifts in bacteria following conditioning in novel soil environments

Rapid niche shifts in bacteria following conditioning in novel soil environments

Species interactions promote parallel evolution of global transcriptional regulators in a widespreadStaphylococcusspecies

Keystone taxa responsible for the microbial community stability and performance of activated sludges

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