AUTHOR=Keller Andreas H. , Schleinitz Kathleen M. , Starke Robert , Bertilsson Stefan , Vogt Carsten , Kleinsteuber Sabine 

TITLE=Metagenome-Based Metabolic Reconstruction Reveals the Ecophysiological Function of Epsilonproteobacteria in a Hydrocarbon-Contaminated Sulfidic Aquifer

JOURNAL=Frontiers in Microbiology

VOLUME=6

YEAR=2015

URL=https://www.frontiersin.org/journals/microbiology/articles/10.3389/fmicb.2015.01396

DOI=10.3389/fmicb.2015.01396

ISSN=1664-302X

ABSTRACT=<p>The population genome of an uncultured bacterium assigned to the <italic>Campylobacterales</italic> (<italic>Epsilonproteobacteria</italic>) was reconstructed from a metagenome dataset obtained by whole-genome shotgun pyrosequencing. Genomic DNA was extracted from a sulfate-reducing, <italic>m</italic>-xylene-mineralizing enrichment culture isolated from groundwater of a benzene-contaminated sulfidic aquifer. The identical epsilonproteobacterial phylotype has previously been detected in toluene- or benzene-mineralizing, sulfate-reducing consortia enriched from the same site. Previous stable isotope probing (SIP) experiments with <sup>13</sup>C<sub>6</sub>-labeled benzene suggested that this phylotype assimilates benzene-derived carbon in a syntrophic benzene-mineralizing consortium that uses sulfate as terminal electron acceptor. However, the type of energy metabolism and the ecophysiological function of this epsilonproteobacterium within aromatic hydrocarbon-degrading consortia and in the sulfidic aquifer are poorly understood. Annotation of the epsilonproteobacterial population genome suggests that the bacterium plays a key role in sulfur cycling as indicated by the presence of an <italic>sqr</italic> gene encoding a sulfide quinone oxidoreductase and <italic>psr</italic> genes encoding a polysulfide reductase. It may gain energy by using sulfide or hydrogen/formate as electron donors. Polysulfide, fumarate, as well as oxygen are potential electron acceptors. Auto- or mixotrophic carbon metabolism seems plausible since a complete reductive citric acid cycle was detected. Thus the bacterium can thrive in pristine groundwater as well as in hydrocarbon-contaminated aquifers. In hydrocarbon-contaminated sulfidic habitats, the epsilonproteobacterium may generate energy by coupling the oxidation of hydrogen or formate and highly abundant sulfide with the reduction of fumarate and/or polysulfide, accompanied by efficient assimilation of acetate produced during fermentation or incomplete oxidation of hydrocarbons. The highly efficient assimilation of acetate was recently demonstrated by a pulsed <sup>13</sup>C<sub>2</sub>-acetate protein SIP experiment. The capability of nitrogen fixation as indicated by the presence of <italic>nif</italic> genes may provide a selective advantage in nitrogen-depleted habitats. Based on this metabolic reconstruction, we propose acetate capture and sulfur cycling as key functions of <italic>Epsilonproteobacteria</italic> within the intermediary ecosystem metabolism of hydrocarbon-rich sulfidic sediments.</p>