Survival of the first rather than the fittest in a Shewanella electrode biofilm

Eric D Kees,Jeffrey A Gralnick,Stephen P Miller,Antony M Dean,Caleb E Levar,Daniel R Bond

doi:10.1038/s42003-021-02040-1

Eric D Kees, Jeffrey A Gralnick + Show 4 more

Open Access

https://doi.org/10.1038/s42003-021-02040-1

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Abstract

For natural selection to operate there must exist heritable variation among individuals that affects their survival and reproduction. Among free-living microbes, where differences in growth rates largely define selection intensities, competitive exclusion is common. However, among surface attached communities, these dynamics become less predictable. If extreme circumstances were to dictate that a surface population is immortal and all offspring must emigrate, the offspring would be unable to contribute to the composition of the population. Meanwhile, the immortals, regardless of reproductive capacity, would remain unchanged in relative abundance. The normal cycle of birth, death, and competitive exclusion would be broken. We tested whether conditions required to set up this idealized scenario can be approximated in a microbial biofilm. Using two differentially-reproducing strains of Shewanella oneidensis grown on an anode as the sole terminal electron acceptor – a system in which metabolism is obligately tied to surface attachment – we found that selection against a slow-growing competitor is drastically reduced. This work furthers understanding of natural selection dynamics in sessile microbial communities, and provides a framework for designing stable microbial communities for industrial and experimental applications.

Highlights

For natural selection to operate there must exist heritable variation among individuals that affects their survival and reproduction
We first tested whether the two strains of S. oneidensis selected for competition conform as expected to the competitive exclusion principle when grown together in planktonic cultures
The observed selection coefficient is = −0.291 ± 0.009 h−1, which is very similar to the predicted value of 0.329 −0.627 = −0.298 h−1, obtained as the difference between the growth rate of each strain in pure culture

Summary

Introduction

For natural selection to operate there must exist heritable variation among individuals that affects their survival and reproduction. Using two differentially-reproducing strains of Shewanella oneidensis grown on an anode as the sole terminal electron acceptor – a system in which metabolism is obligately tied to surface attachment – we found that selection against a slowgrowing competitor is drastically reduced. Under an idealized scenario (described and modeled in detail in Supplementary Note), a colonizing surface-attached population would experience no death or detachment and would not be replaced or overtaken by its progeny or competing cells. Under these conditions, the first organisms to colonize a surface would persist regardless of their capacity for growth, allowing for the initial diversity of a founding population to be preserved. Since planktonic emigrants from the electrode surface will be non-growing, our experimental system, a continuously fed anaerobic three-electrode bioreactor (Fig. 1a) enables competition on the anodes to be monitored by counting the planktonic population (Fig. 1b)

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