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

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.

Electrochemical Microwell Plate to Study Electroactive Microorganisms in Parallel and Real-Time

“…The reasons for this different shift in the community and hence the microbial electrochemical performance cannot be deciphered. They may range from increased oxygen availability by leakage into the wells to stochastic microbial processes ( Zhou et al, 2013 ; Ofiţeru et al, 2010 ) including the first settling at the electrode ( Kees et al, 2021 ). This was already discussed for microbial electrochemical selection and cultivation previously ( Koch et al, 2019 ).…”

Determinants of multiheme cytochrome extracellular electron transfer uncovered by systematic peptide insertion

“…Materials like electrodes can be challenging to directly use in library selection as changes in electron flux can be confounded by changes in biofilm formation or surface interactions. 45…”

First settlers persist

“…In this line, Kees et al have recently shed light on the underlying phenomena from a different angle. 6 Figure 1 summarizes their study on two strains of the model EAM Shewanella oneidensis with one strain being impaired in growth in relation to the other. The growth of these strains was investigated in solution (planktonically) with fumarate as electron acceptor and at an electrode.…”

“…The specific characteristics of Shewanella oneidensis (rarely forming multi-layered biofilms, no planktonic growth when using an anode as sole terminal electron acceptor) enabled quantification of the biofilm population by measuring the emigrated progeny of the electrode colonizers. 6 Therefore, the complementary methods of flow cytometry and dilution plate counting could be applied, also proving cell viability.…”

“…In summary, the excellent study by Kees et al provides substantial evidence that the fastest and not the fittest colonizers survive and dominate Shewanella biofilm electrodes. 6 It brings a certain twist toward the ecology of biofilm electrodes and discusses the particular but fascinating ecological principles of systems with an obligate connection between the microbial energy harvest and the substratum. Although the authors strictly restrict their conclusions to the tested model system and further investigations are indeed needed, we anticipate a universal impact and ask what are possible implications for technical implementation of biofilm electrodes?…”