A stable genetic polymorphism underpinning microbial syntrophy.

Tobias Großkopf,Mark Alston,David Swarbreck,Leighton Folkes,Simone Zenobi,Orkun S Soyer

doi:10.1038/ismej.2016.80

Tobias Großkopf, Mark Alston + Show 4 more

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https://doi.org/10.1038/ismej.2016.80

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Abstract

Syntrophies are metabolic cooperations, whereby two organisms co-metabolize a substrate in an interdependent manner. Many of the observed natural syntrophic interactions are mandatory in the absence of strong electron acceptors, such that one species in the syntrophy has to assume the role of electron sink for the other. While this presents an ecological setting for syntrophy to be beneficial, the potential genetic drivers of syntrophy remain unknown to date. Here, we show that the syntrophic sulfate-reducing species Desulfovibrio vulgaris displays a stable genetic polymorphism, where only a specific genotype is able to engage in syntrophy with the hydrogenotrophic methanogen Methanococcus maripaludis. This 'syntrophic' genotype is characterized by two genetic alterations, one of which is an in-frame deletion in the gene encoding for the ion-translocating subunit cooK of the membrane-bound COO hydrogenase. We show that this genotype presents a specific physiology, in which reshaping of energy conservation in the lactate oxidation pathway enables it to produce sufficient intermediate hydrogen for sustained M. maripaludis growth and thus, syntrophy. To our knowledge, these findings provide for the first time a genetic basis for syntrophy in nature and bring us closer to the rational engineering of syntrophy in synthetic microbial communities.

Highlights

Syntrophic interactions represent cases of metabolic cooperation between two phenotypically distinct organisms (Schink, 1997; McInerney et al, 2008; Sieber et al, 2012; Morris et al, 2013)
We show that this ability to engage in syntrophy Microscopy with Mm is underpinned by a stable genetic For microscopic analysis, 5 μl of culture was placed polymorphism in Desulfovibrio vulgaris strain Hildenborough (DvH); under a sulfate-free, minimal on a microscope glass slide and covered with a glass lactate media, only a specific genotype of DvH can coverslip
It is well known that sulfate-reducing bacteria (SRB) can act as both hydrogen consumers and producers, taking the latter role in the absence of terminal electron acceptors such as sulfate (Muyzer and Stams, 2008)

Summary

Introduction

Syntrophic interactions represent cases of metabolic cooperation between two phenotypically distinct organisms (Schink, 1997; McInerney et al, 2008; Sieber et al, 2012; Morris et al, 2013) These interactions are common among microbes living in environments that can be readily depleted of strong electron acceptors. The low thermodynamic energy associated with fermentative metabolic pathways results in 'thermodynamic inhibition' of microbial growth due to product accumulation (Schink, 1997; Kleerebezem and Stams, 2000; Großkopf and Soyer, 2014, 2016). Formation of spatial structures like metabolism as a key driver for syntrophy formation biofilms is frequently observed in monocultures in general

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