Hydrogen production by Sulfurospirillum species enables syntrophic interactions of Epsilonproteobacteria

Stefan Kruse,Lorenz Adrian,Gabriele Diekert,Tobias Goris,Martin Westermann

doi:10.1038/s41467-018-07342-3

Abstract

Hydrogen-producing bacteria are of environmental importance, since hydrogen is a major electron donor for prokaryotes in anoxic ecosystems. Epsilonproteobacteria are currently considered to be hydrogen-oxidizing bacteria exclusively. Here, we report hydrogen production upon pyruvate fermentation for free-living Epsilonproteobacteria, Sulfurospirillum spp. The amount of hydrogen produced is different in two subgroups of Sulfurospirillum spp., represented by S. cavolei and S. multivorans. The former produces more hydrogen and excretes acetate as sole organic acid, while the latter additionally produces lactate and succinate. Hydrogen production can be assigned by differential proteomics to a hydrogenase (similar to hydrogenase 4 from E. coli) that is more abundant during fermentation. A syntrophic interaction is established between Sulfurospirillum multivorans and Methanococcus voltae when cocultured with lactate as sole substrate, as the former cannot grow fermentatively on lactate alone and the latter relies on hydrogen for growth. This might hint to a yet unrecognized role of Epsilonproteobacteria as hydrogen producers in anoxic microbial communities.

Highlights

Hydrogen-producing bacteria are of environmental importance, since hydrogen is a major electron donor for prokaryotes in anoxic ecosystems
Few data on growth behavior are available in the literature, but S. multivorans was reported to exhibit poor growth on pyruvate as sole energy source compared to respiratory growth with pyruvate and fumarate or tetrachloroethene (PCE) as electron acceptor[33]
Among the proteins encoded in the S. cavolei genome, which do not have an ortholog in S. multivorans, we found a cluster encoding an [FeFe] hydrogenase (Supplementary Figure 12) known to contribute to fermentative H2 production in many bacteria, e.g. Clostridia

Summary

Introduction

Hydrogen-producing bacteria are of environmental importance, since hydrogen is a major electron donor for prokaryotes in anoxic ecosystems. A syntrophic interaction is established between Sulfurospirillum multivorans and Methanococcus voltae when cocultured with lactate as sole substrate, as the former cannot grow fermentatively on lactate alone and the latter relies on hydrogen for growth This might hint to a yet unrecognized role of Epsilonproteobacteria as hydrogen producers in anoxic microbial communities. Four gene clusters, each encoding a [NiFe] hydrogenase, were found in the genome of S. multivorans[23] and most other Sulfurospirillum spp.[26] Two of these appear to be H2producing, the other two are potential H2-uptake enzymes as deduced from sequence similarity to known hydrogenases. A coculture experiment of S. multivorans with the methanogenic archaeon Methanococcus voltae revealed an interspecies H2 transfer between both organisms suggesting a hitherto undiscovered contribution of Sulfurospirillum spp. and other Epsilonproteobacteria to the microbial anaerobic food web as H2 producers

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Results

Conclusion