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

Matheus Carnevali, Paula B.; Schulz, Frederik; Castelle, Cindy J.; Kantor, Rose S.; Shih, Patrick M.; Sharon, Itai; Santini, Joanne M.; Olm, Matthew R.; Amano, Yuki; Thomas, Brian C.; Anantharaman, Karthik; Burstein, David; Becraft, Eric D.; Stepanauskas, Ramunas; Woyke, Tanja; Banfield, Jillian F.

doi:10.1038/s41467-018-08246-y

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

Journal Article · 28 January 2019 · Nature Communications

DOI: https://doi.org/10.1038/s41467-018-08246-y · OSTI ID:1546638

^[1];

^[2]; Castelle, Cindy J. ^[1]; Kantor, Rose S. ^[1];

^[3]; Sharon, Itai ^[4];

^[5]; Olm, Matthew R. ^[1];

^[6]; Thomas, Brian C. ^[1];

^[1];

^[1]; Becraft, Eric D. ^[7];

^[7];

^[2];

^[8]

Univ. of California, Berkeley, CA (United States)
USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Univ. of California, Berkeley, CA (United States); Migal Galilee Research Institute, Kiryat Shmona (Israel); Tel Hai College, Upper Galilee (Israel)
Univ. College London (United Kingdom)
Japan Atomic Energy Agency (JAEA), Tokai (Japan); Japan Atomic Energy Agency (JAEA), Horonobe (Japan)
Bigelow Lab. for Ocean Sciences, East Boothbay, ME (United States)
Univ. of California, Berkeley, CA (United States); Chan Zuckerberg Biohub, San Francisco, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Innovative Genomics Institute, Berkley, CA (United States)

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.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 1546638

Journal Information:: Nature Communications, Journal Name: Nature Communications Journal Issue: 1 Vol. 10; ISSN 2041-1723

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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