Hydrogen-based metabolism as an ancestral trait in lineages sibling to the Cyanobacteria

Paula B. Matheus Carnevali, Frederik Schulz, Cindy J. Castelle, Rose S. Kantor, Patrick M. Shih, Itai Sharon, Joanne M. Santini, Matthew R. Olm, Yuki Amano, Brian C. Thomas, Karthik Anantharaman, David Burstein, Eric D. Becraft, Ramunas Stepanauskas, Tanja Woyke and Jillian F. Banfield ()
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Paula B. Matheus Carnevali: University of California, Berkeley
Frederik Schulz: DOE Joint Genome Institute
Cindy J. Castelle: University of California, Berkeley
Rose S. Kantor: University of California, Berkeley
Patrick M. Shih: Feedstocks Division, Joint BioEnergy Institute
Itai Sharon: University of California, Berkeley
Joanne M. Santini: University College London
Matthew R. Olm: University of California, Berkeley
Yuki Amano: Nuclear Fuel Cycle Engineering Laboratories, Japan Atomic Energy Agency
Brian C. Thomas: University of California, Berkeley
Karthik Anantharaman: University of California, Berkeley
David Burstein: University of California, Berkeley
Eric D. Becraft: Bigelow Laboratory for Ocean Sciences
Ramunas Stepanauskas: Bigelow Laboratory for Ocean Sciences
Tanja Woyke: DOE Joint Genome Institute
Jillian F. Banfield: University of California, Berkeley

Nature Communications, 2019, vol. 10, issue 1, 1-15

Abstract: Abstract The evolution of aerobic respiration was likely linked to the origins of oxygenic Cyanobacteria. Close phylogenetic neighbors to Cyanobacteria, such as Margulisbacteria (RBX-1 and ZB3), Saganbacteria (WOR-1), Melainabacteria and Sericytochromatia, may constrain the metabolic platform in which aerobic respiration arose. Here, we analyze genomic sequences and predict that sediment-associated Margulisbacteria have a fermentation-based metabolism featuring a variety of hydrogenases, a streamlined nitrogenase, and electron bifurcating complexes involved in cycling of reducing equivalents. The genomes of ocean-associated Margulisbacteria encode an electron transport chain that may support aerobic growth. Some Saganbacteria genomes encode various hydrogenases, and others may be able to use O2 under certain conditions via a putative novel type of heme copper O2 reductase. Similarly, Melainabacteria have diverse energy metabolisms and are capable of fermentation and aerobic or anaerobic respiration. The ancestor of all these groups may have been an anaerobe in which fermentation and H2 metabolism were central metabolic features. The ability to use O2 as a terminal electron acceptor must have been subsequently acquired by these lineages.

Date: 2019
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DOI: 10.1038/s41467-018-08246-y

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