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Abstract Studies of microbial interactions often emphasize interactions with large, easily measurable growth differences and short-term ecological outcomes spanning just a few generations. However, more subtle interactions, such as those without obvious phenotypes, may play a significant role in shaping both the short-term ecological dynamics and the long-term evolutionary trajectories of microbial species. We used the cheese rind model microbiome to examine how two fungal species, Penicillium camemberti and Geotrichum candidum, impact global gene expression and genome evolution of the bacterium Pseudomonas carnis LP. Even though fungi had limited impacts on the growth of P. carnis LP, approximately 4–40% of its genome was differentially expressed, depending on the specific fungal partner. When we evolved this Pseudomonas strain alone or in co-culture with each of the fungi, we observed frequent mutations in global regulators of nitrogen regulation, secondary metabolite production, and motility, depending on the fungus. Strikingly, many strains with mutations in the nitrogen regulatory gene ntrB emerged when evolved alone or with G. candidum, but not with P. camemberti. Metabolomic and fitness experiments demonstrate that release of free amino acids by P. camemberti removes the fitness advantages conferred by ntrB mutations. Collectively, these results demonstrate that even in the absence of major short-term growth effects, fungi can have substantial impacts on the transcriptome and genomic evolution of bacterial species.
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Bacterial–fungal interactions promote parallel evolution of global transcriptional regulators in a widespread Staphylococcus species
Abstract 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. 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 B. aurantiacum, or with P.solitum did not evolve novel phenotypic diversity. Whole-genome sequencing of individual mutant isolates across all four treatments identified numerous unique mutations in the operons for the SigB, Agr, and WalRK global regulators, but only in the D. hansenii treatment. Phenotyping and RNA-seq experiments highlighted altered pigment and biofilm production, spreading, stress tolerance, and metabolism of S. xylosus mutants. Fitness experiments revealed antagonistic pleiotropy, where beneficial mutations that evolved in the presence of the yeast had strong negative fitness effects in other biotic environments. This work demonstrates that bacterial-fungal interactions can have long-term evolutionary consequences within multispecies microbiomes by facilitating the evolution of strain diversity.
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- Award ID(s):
- 1942063
- PAR ID:
- 10485264
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- The ISME Journal
- Volume:
- 17
- Issue:
- 9
- ISSN:
- 1751-7362
- Format(s):
- Medium: X Size: p. 1504-1516
- Size(s):
- p. 1504-1516
- Sponsoring Org:
- National Science Foundation
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