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Bacterial–fungal interactions promote parallel evolution of global transcriptional regulators in a widespread Staphylococcus species

The ISME Journal volume 17, pages 1504–1516 (2023)Cite this article

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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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Fig. 1: The yeast Debaryomyces hansenii causes phenotypic diversification of S. xylosus BC10 during experimental evolution.
Fig. 2: Whole-genome sequencing identifies mutations in putative global regulators of S. xylosus BC10 in the +Debaryomyces treatment.
Fig. 3: Phenotypic assays reveal biological impacts of global regulator mutations in evolved S. xylosus BC10.
Fig. 4: RNA sequencing highlights transcriptomic impacts of global regulator mutations in S. xylosus BC10.
Fig. 5: Growth and competition experiments reveal fitness of evolved S. xylosus mutants in different biotic environments.

Data availability

All raw fastq read files of re-sequenced evolved isolates of S. xylosus BC10 have been deposited in NCBI in BioProject PRJNA856679. Raw RNA-seq read files from this study have been deposited in NCBI in BioProject PRJNA856810.

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Acknowledgements

This work was funded by a grant from the United States National Science Foundation (CAREER IOS/BIO 1942063) to BEW. The authors are grateful to members of the Wolfe lab, including Robert May, Nicolas Louw, Kasturi Lele, Dillon Arrigan, Chris Tomo, and Mak Boylan, for providing extensive feedback on previous versions of this manuscript.

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  1. These authors contributed equally: Casey Cosetta, Brittany Niccum.

Authors and Affiliations

  1. Department of Biology, Tufts University, Medford, MA, 02155, USA

    Casey M. Cosetta, Brittany Niccum, Nick Kamkari, Michael Dente, Matthew Podniesinski & Benjamin E. Wolfe

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  1. Casey M. Cosetta
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Contributions

BN, CC, and BEW designed the study. BN conducted the evolution experiment. CC and BEW conducted the whole-genome resequencing. CC conducted the fitness experiments. BEW conducted and analyzed the RNA-seq experiment. CC, NK, MD, and MP conducted the phenotypic assays. CC, BN, and BEW conducted statistical analyses, created figures, and wrote the first drafts of the manuscript. All authors read, revised, and approved the final manuscript.

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Correspondence to Benjamin E. Wolfe.

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Cosetta, C.M., Niccum, B., Kamkari, N. et al. Bacterial–fungal interactions promote parallel evolution of global transcriptional regulators in a widespread Staphylococcus species. ISME J 17, 1504–1516 (2023). https://doi.org/10.1038/s41396-023-01462-5

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