Evolution from a respiratory ancestor to fill syntrophic and fermentative niches: comparative fenomics of six Geobacteraceae species

Abstract

<p>Abstract</p> <p>Background</p> <p>The anaerobic degradation of organic matter in natural environments, and the biotechnical use of anaerobes in energy production and remediation of subsurface environments, both require the cooperative activity of a diversity of microorganisms in different metabolic niches. The <it>Geobacteraceae </it>family contains members with three important anaerobic metabolisms: fermentation, syntrophic degradation of fermentation intermediates, and anaerobic respiration.</p> <p>Results</p> <p>In order to learn more about the evolution of anaerobic microbial communities, the genome sequences of six <it>Geobacteraceae </it>species were analyzed. The results indicate that the last common <it>Geobacteraceae </it>ancestor contained sufficient genes for anaerobic respiration, completely oxidizing organic compounds with the reduction of external electron acceptors, features that are still retained in modern <it>Geobacter </it>and <it>Desulfuromonas </it>species. Evolution of specialization for fermentative growth arose twice, via distinct lateral gene transfer events, in <it>Pelobacter carbinolicus </it>and <it>Pelobacter propionicus</it>. Furthermore, <it>P. carbinolicus </it>gained hydrogenase genes and genes for ferredoxin reduction that appear to permit syntrophic growth via hydrogen production. The gain of new physiological capabilities in the <it>Pelobacter </it>species were accompanied by the loss of several key genes necessary for the complete oxidation of organic compounds and the genes for the <it>c</it>-type cytochromes required for extracellular electron transfer.</p> <p>Conclusion</p> <p>The results suggest that <it>Pelobacter </it>species evolved parallel strategies to enhance their ability to compete in environments in which electron acceptors for anaerobic respiration were limiting. More generally, these results demonstrate how relatively few gene changes can dramatically transform metabolic capabilities and expand the range of environments in which microorganisms can compete.</p