Abstract

Antagonistic interactions are widespread in the microbial world and affect microbial evolutionary dynamics. Natural microbial communities often display spatial structure, which affects biological interactions, but much of what we know about microbial antagonism comes from laboratory studies of well-mixed communities. To overcome this limitation, we manipulated two killer strains of the budding yeast Saccharomyces cerevisiae, expressing different toxins, to independently control the rate at which they released their toxins. We developed mathematical models that predict the experimental dynamics of competition between toxin-producing strains in both well-mixed and spatially structured populations. In both situations, we experimentally verified theory's prediction that a stronger antagonist can invade a weaker one only if the initial invading population exceeds a critical frequency or size. Finally, we found that toxin-resistant cells and weaker killers arose in spatially structured competitions between toxin-producing strains, suggesting that adaptive evolution can affect the outcome of microbial antagonism in spatial settings.

Highlights

  • Microbes affect nearly every aspect of life on Earth, from carbon fixation (Falkowski, Barber, & Smetacek, 1998) to human health (Srivastava & Bhargava, 2016)

  • We developed an experimental system in which two strains of the budding yeast, 85 Saccharomyces cerevisiae, expressed two different toxins from two different, inducible promoters (Figure 1A)

  • We investigated the dynamics of competitive exclusion in three environments: spatially well-mixed populations in liquid cultures or on surfaces, and spatially structured populations on surfaces

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Summary

Introduction

Microbes affect nearly every aspect of life on Earth, from carbon fixation (Falkowski, Barber, & Smetacek, 1998) to human health (Srivastava & Bhargava, 2016). Antagonistic interactions are found in both prokaryotes (Atanasova, Pietila, & Oksanen, 2013; Cheung, Danna, O'Connor, Price, & Shand, 1997, Riley & Wertz, 2002, Veening & Blokesch, 2017) and eukaryotes (Boynton, 2019) They occur in many ecological niches such as the rhizosphere (Kent & Triplett, 2002), aquatic systems (Feichtmayer, Deng, & Griebler, 2017, Drebes Dörr, & Blokesh, 2020) and human infections (Schoustra, Dench, Dali, Aaron, & Kassen, 2012, Libberton, Horsburgh, & Brockhurst, 2015, Heilbronner, Krismer, Brötz-Oesterhelt, & Peschel, 2021), and are frequently exploited for biocontrol applications (Kim et al, 2006; Weller, 2007). We discuss mathematical models that give us intuition for the formation of depletion zones at the interface between two antagonist strains in spatially structured communities and we discuss mutants that appeared during the experiments and affected the dynamics of antagonism

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