The thermophilic biomass-degrading bacterium Caldicellulosiruptor bescii utilizes two enzymes to oxidize glyceraldehyde 3-phosphate during glycolysis

Scott, Israel M.; Rubinstein, Gabriel M.; Poole, II, Farris L.; Lipscomb, Gina L.; Schut, Gerrit J.; Williams-Rhaesa, Amanda M.; Stevenson, David M.; Amador-Noguez, Daniel; Kelly, Robert M.; Adams, Michael W. W.

doi:10.1074/jbc.RA118.007120

Title: The thermophilic biomass-degrading bacterium Caldicellulosiruptor bescii utilizes two enzymes to oxidize glyceraldehyde 3-phosphate during glycolysis

Journal Article · Sat Jun 01 00:00:00 EDT 2019 · Journal of Biological Chemistry

DOI:https://doi.org/10.1074/jbc.RA118.007120· OSTI ID:1769205

Scott, Israel M.; Rubinstein, Gabriel M.; Poole, II, Farris L.; Lipscomb, Gina L.; Schut, Gerrit J.; Williams-Rhaesa, Amanda M.; Stevenson, David M.; Amador-Noguez, Daniel; Kelly, Robert M.;

Caldicellulosiruptor bescii is an extremely thermophilic, cellulolytic bacterium with a growth optimum at 78 °C and is the most thermophilic cellulose degrader known. It is an attractive target for biotechnological applications, but metabolic engineering will require an in-depth understanding of its primary pathways. A previous analysis of its genome uncovered evidence that C. bescii may have a completely uncharacterized aspect to its redox metabolism, involving a tungsten-containing oxidoreductase of unknown function. Herein, we purified and characterized this new member of the aldehyde ferredoxin oxidoreductase (AOR) family of tungstoenzymes. We show that it is a heterodimeric glyceraldehyde-3-phosphate (GAP) ferredoxin oxidoreductase (GOR) present not only in all known Caldicellulosiruptor species, but also in 44 mostly anaerobic bacterial genera. GOR is phylogenetically distinct from the monomeric GAP-oxidizing enzyme found previously in several Archaea. We found that its large subunit (GOR-L) contains a single tungstopterin site and one iron–sulfur [4Fe-4S] cluster, that the small subunit (GOR-S) contains four [4Fe-4S] clusters, and that GOR uses ferredoxin as an electron acceptor. Deletion of either subunit resulted in a distinct growth phenotype on both C₅- and C₆-sugars, with an increased lag phase, but higher cell densities. Using metabolomics and kinetic analyses, we show that GOR functions in parallel with the conventional GAP dehydrogenase, providing an alternative ferredoxin-dependent glycolytic pathway. These two pathways likely facilitate the recycling of reduced redox carriers (NADH and ferredoxin) in response to environmental H₂ concentrations. This metabolic flexibility has important implications for the future engineering of this and related species.

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Research Organization:: Univ. of Georgia, Athens, GA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: SC0019391

OSTI ID:: 1769205

Alternate ID(s):: OSTI ID: 1613209

Journal Information:: Journal of Biological Chemistry, Journal Name: Journal of Biological Chemistry Vol. 294 Journal Issue: 25; ISSN 0021-9258

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 14 works

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Title: The thermophilic biomass-degrading bacterium Caldicellulosiruptor bescii utilizes two enzymes to oxidize glyceraldehyde 3-phosphate during glycolysis

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