TY - JOUR
T1 - Hydrogen-based metabolism as an ancestral trait in lineages sibling to the Cyanobacteria
AU - Matheus Carnevali, Paula B.
AU - Schulz, Frederik
AU - Castelle, Cindy J.
AU - Kantor, Rose S.
AU - Shih, Patrick M.
AU - Sharon, Itai
AU - Santini, Joanne M.
AU - Olm, Matthew R.
AU - Amano, Yuki
AU - Thomas, Brian C.
AU - Anantharaman, Karthik
AU - Burstein, David
AU - Becraft, Eric D.
AU - Stepanauskas, Ramunas
AU - Woyke, Tanja
AU - Banfield, Jillian F.
N1 - Funding Information:
Laura Hug and Christopher Brown provided assistance with analyses, Shufei Lei and Kate Lane assisted with bioinformatics and data management, Kelly Wrighton, Kim Handley, and Kenneth Hurst Williams provided samples. Sallie Chisholm, Paul Berube, and Steven Biller are acknowledged for their help securing the marine samples. We thank the staff of Bigelow Laboratory Single-Cell Genomics Center for the generation of single-cell data. Teruki Iwatsuki, Kazuki Hayashida, Toshihiro Kato, and Mitsuru Kubota assisted with groundwater sampling at Mizunami Underground Research Laboratory, Japan Atomic Energy Agency (JAEA). Thanks to Chris Greening for feedback regarding FDH-Ehr complexes on the bioRxiv version of this manuscript, and to Denis Baurain and an anonymous reviewer for all the useful comments on the manuscript. The research was supported by the Department of Energy (DOE), Office of Science and Office of Biological and Environmental Research (Lawrence Berkeley National Lab; Operated by the University of California, Berkeley). DNA sequencing for the Rifle samples was conducted by the U.S. Department of Energy Joint Genome Institute, a DOE Office of Science User Facility, supported under Contract No. DE-AC02-05CH11231. Marine single amplified genomes were generated and sequenced with the support of NSF grants DEB-1441717 and OCE-1335810, and Simons Foundation grant 510023 (to R.S.). Fecal samples were collected from patients in the clinical PhaseI/II SEASP trial in Bangladesh that was jointly led by Graham George and Ingrid Pickering (University of Saskatchewan), with the assistance of the SEASP team https://clinicaltrials.gov/ct2/show/ NCT02377635, and funded by the Canadian Federal Government, through Grand Challenges Canada, Stars in Global Health and by the Global Institute for Water Security. The study was funded by the Canadian Federal Government, through a program entitled Grand Challenges Canada, Stars in Global Health, with additional funds from the Global Institute for Water Security at the University of Saskatchewan.
Publisher Copyright:
© 2019, The Author(s).
PY - 2019/12/1
Y1 - 2019/12/1
N2 - 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.
AB - 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.
UR - https://www.scopus.com/pages/publications/85060636096
U2 - 10.1038/s41467-018-08246-y
DO - 10.1038/s41467-018-08246-y
M3 - Article
C2 - 30692531
AN - SCOPUS:85060636096
SN - 2041-1723
VL - 10
JO - Nature Communications
JF - Nature Communications
IS - 1
M1 - 463
ER -