Natural Selection in Synthetic Communities Highlights the Roles of Methylococcaceae and Methylophilaceae and Suggests Differential Roles for Alternative Methanol Dehydrogenases in Methane Consumption

Zheng Yu,Ludmila Chistoserdova,David A C Beck

doi:10.3389/fmicb.2017.02392

Abstract

We describe experiments that follow species dynamics and gene expression patterns in synthetic bacterial communities including species that compete for the single carbon substrate supplied, methane, and species unable to consume methane, which could only succeed through cooperative interactions. We demonstrate that these communities mostly select for two functional guilds, methanotrophs of the family Methylococcaceae and non-methanotrophic methylotrophs of the family Methylophilaceae, these taxonomic guilds outcompeting all other species included in the synthetic mix. The metatranscriptomics analysis uncovered that in both Methylococcaceae and Methylophilaceae, some of the most highly transcribed genes were the ones encoding methanol dehydrogenases (MDH). Remarkably, expression of alternative MDH genes (mxaFI versus xoxF), previously shown to be subjects to the rare Earth element switch, was found to depend on environmental conditions such as nitrogen source and methane and O2 partial pressures, and also to be species-specific. Along with the xoxF genes, genes encoding divergent cytochromes were highly expressed in both Methylophilaceae and Methylococcaceae, suggesting their function in methanol metabolism, likely encoding proteins serving as electron acceptors from XoxF enzymes. The research presented tested a synthetic community model that is much simplified compared to natural communities consuming methane, but more complex than the previously utilized two-species model. The performance of this model identifies prominent species for future synthetic ecology experiments and highlights both advantages of this approach and the challenges that it presents.

Highlights

Metabolism of methane is an important part of biogeochemical cycling of carbon (Singh et al, 2010)
Methylophilaceae other than Methylophilus tended to overexpress xoxF over mxaF. (2) Second, we demonstrate that both O2 and methane partial pressures have control over the rare Earth element (REE) switch, high methane selecting for the MxaFI–methanol dehydrogenases (MDH), “low” methane and “low” O2 selecting for XoxF, and “high” methane “low” O2, nitrate allowing for transcription of both systems at similar levels
We here demonstrated the utility of multispecies SCs in studying complex biogeochemical processes, such as communal metabolism of methane, in a simplified, controllable model

Summary

Introduction

Metabolism of methane is an important part of biogeochemical cycling of carbon (Singh et al, 2010). Experimental evidence is somewhat contradictory to the notion of “public goods,” as specific species cooccurrences, such as cooperative behavior of Methylococcaceae and Methylophilaceae, have been noted in manipulated microcosms (Kalyuzhnaya et al, 2008; Beck et al, 2013; Hernandez et al, 2015; Oshkin et al, 2015), and in natural populations inhabiting methane-rich environments such as permafrosts (Martineau et al, 2010; Crevecoeur et al, 2015) or methane-fueled cave biofilms (Karwautz et al, 2017). Vitamin B12 exchange has been previously implicated in maintaining stable cocultures of methanotrophs and nonmethanotrophs (Iguchi et al, 2011)

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