Cyclic pairwise interaction representing a rock–paper–scissors game maintains the population of the vulnerable yeast Saccharomyces cerevisiae within a multispecies sourdough microbiome

DOI IR (HANDLE) Web Site Research Data 23 References Open Access
  • Oshiro, Mugihito
    Central Laboratory of Yamazaki Baking Company Limited Laboratory of Soil and Environmental Microbiology, Division of Systems Bioengineering, Department of Bioscience and Biotechnology, Faculty of Agriculture, Graduate School, Kyushu University
  • Zendo, Takeshi
    Laboratory of Microbial Technology, Division of Systems Bioengineering, Department of Bioscience and Biotechnology, Faculty of Agriculture, Graduate School, Kyushu University
  • Tashiro, Yukihiro
    Laboratory of Soil and Environmental Microbiology, Division of Systems Bioengineering, Department of Bioscience and Biotechnology, Faculty of Agriculture, Graduate School, Kyushu University
  • Nakayama, Jiro
    Laboratory of Microbial Technology, Division of Systems Bioengineering, Department of Bioscience and Biotechnology, Faculty of Agriculture, Graduate School, Kyushu University
  • Kate S. Howell
    editor

Bibliographic Information

Other Title
  • Cyclic pairwise interaction representing a rock–paper–scissors game maintains the population of the vulnerable yeast <i>Saccharomyces cerevisiae</i> within a multispecies sourdough microbiome

Description

Sourdough starters are spontaneously generated multispecies communities consisting of lactic acid bacteria (LAB) and yeasts. Traditionally used to make baked goods, these communities of microorganisms can be propagated through successive transfers to other containers. Successive transfers result in microbial community dynamics; however, the mechanisms guiding the dynamics are not fully elucidated. This study tracked five species of sourdough LAB-yeast communities (three LAB species and two yeast species) during successive transfers in vitro to explore the interspecies interactions driving the multispecies community dynamics. The microbial dynamics were modeled with a generalized Lotka–Volterra (gLV) equation, which can mathematically identify ecological types of interspecies interactions. The gLV model simulated the population dynamics of each species with Pearson’s correlation coefficient values of ≥0.817. Pairwise experiments revealed that competition (negative/negative) predominated among all pairwise interactions (70%), followed by amensalism (negative/neutral) (30%). In the pairwise community, the LAB species Limosilactobacillus fermentum suppressed Saccharomyces cerevisiae growth through amensalism; however, S. cerevisiae population was maintained when the community comprised 3–5 species, including the LAB species L. fermentum and Pediococcus pentosaceus. The key interspecies interactions for maintaining the S. cerevisiae population were theoretically determined using the gLV model; the three identified species interacted non-transitively with S. cerevisiae in a cyclic pairwise interaction, metaphorically representing a rock–paper–scissors relationship, which systemically supported the S. cerevisiae population in the multispecies community. These theoretical insights indicate that cyclic pairwise interaction is the main driver of LAB-yeast population dynamics, which helps sustain a vulnerable yeast species in a sourdough multispecies community.

Journal

  • Microbiology Spectrum

    Microbiology Spectrum 11 (6), e01370-23-, 2023-12-12

    American Society for Microbiology

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