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Nat Commun. 2019 Jan 28;10(1):463. doi: 10.1038/s41467-018-08246-y.

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

Author information

1
Department of Earth and Planetary Science, University of California, Berkeley, Berkeley, 94720, CA, USA.
2
DOE Joint Genome Institute, Walnut Creek, 94598, CA, USA.
3
Department of Civil and Environmental Engineering, University of California, Berkeley, Berkeley, 94720, CA, USA.
4
Feedstocks Division, Joint BioEnergy Institute, Emeryville, 94608, CA, USA.
5
Environmental Genomics and Systems Biology Division, Lawrence Berkeley National Laboratory, Berkeley, 94720, CA, USA.
6
Department of Plant Biology, University of California, Davis, Davis, 95616, CA, USA.
7
Migal Galilee Research Institute, Kiryat Shmona, 11016, Israel.
8
Tel Hai College, Upper Galilee, 12210, Israel.
9
Institute of Structural & Molecular Biology, Division of Biosciences, University College London, London, WC1E 6BT, UK.
10
Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, 94720, CA, USA.
11
Nuclear Fuel Cycle Engineering Laboratories, Japan Atomic Energy Agency, Tokai, 319-1111, Ibaraki, Japan.
12
Horonobe Underground Research Center, Japan Atomic Energy Agency, Horonobe, 098-3224, Hokkaido, Japan.
13
Department of Bacteriology, University of Wisconsin-Madison, Madison, 53706, WI, USA.
14
School of Molecular and Cell Biology and Biotechnology, George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, 69978, Israel.
15
Bigelow Laboratory for Ocean Sciences, East Boothbay, 04544, ME, USA.
16
Department of Biological Sciences, North Alabama University, Florence, 35632, AL, USA.
17
Department of Earth and Planetary Science, University of California, Berkeley, Berkeley, 94720, CA, USA. jbanfield@berkeley.edu.
18
Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, 94720, CA, USA. jbanfield@berkeley.edu.
19
Chan Zuckerberg Biohub, San Francisco, 94158, CA, USA. jbanfield@berkeley.edu.
20
Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, 94705, CA, USA. jbanfield@berkeley.edu.
21
Innovative Genomics Institute, Berkley, 94704, CA, USA. jbanfield@berkeley.edu.

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.

PMID:
30692531
PMCID:
PMC6349859
DOI:
10.1038/s41467-018-08246-y
[Indexed for MEDLINE]
Free PMC Article

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