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Convergent evolution of unusual complex I homologs with increased proton pumping capacity: energetic and ecological implications

Chadwick, Grayson L. and Hemp, James and Fischer, Woodward W. and Orphan, Victoria J. (2018) Convergent evolution of unusual complex I homologs with increased proton pumping capacity: energetic and ecological implications. ISME Journal, 12 (11). pp. 2668-2680. ISSN 1751-7362. PMCID PMC6194058. https://resolver.caltech.edu/CaltechAUTHORS:20180711-165717508

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Abstract

Respiratory complex I is part of a large family of homologous enzymes that carry out the transfer of electrons between soluble cytoplasmic electron carriers and membrane-bound electron carriers. These complexes are vital bioenergetic enzymes that serve as the entry points into electron transport chains for a wide variety of microbial metabolisms, and electron transfer is coupled to proton translocation. The core complex of this enzyme is made up of 11 protein subunits, with three major proton pumping subunits. Here, we document a large number of modified complex I gene cassettes found in genome sequences from diverse cultured bacteria, shotgun metagenomics, and environmentally derived archaeal fosmids all of which encode a fourth proton pumping subunit. The incorporation of this extra subunit into a functional protein complex is supported by large amino acid insertions in the amphipathic helix that runs the length of the protein complex. Phylogenetic analyses reveal that these modified complexes appear to have arisen independently multiple times in a remarkable case of convergent molecular evolution. From an energetic perspective, we hypothesize that this modification on the canonical complex I architecture allows for the translocation of a fifth proton per reaction cycle—the physiological utility of this modified complex is discussed.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/s41396-018-0210-1DOIArticle
https://rdcu.be/2RIYPublisherFree ReadCube access
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6194058/PubMed CentralArticle
ORCID:
AuthorORCID
Chadwick, Grayson L.0000-0003-0700-9350
Hemp, James0000-0001-7193-0553
Fischer, Woodward W.0000-0002-8836-3054
Orphan, Victoria J.0000-0002-5374-6178
Additional Information:© International Society for Microbial Ecology 2018. Received: 2 November 2017 / Revised: 17 January 2018 / Accepted: 20 March 2018. This publication was funded by the Gordon and Betty Moore Foundation through Grant #GBMF3780 and through work supported by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research [DE-SC0016469] and the NASA Astrobiology Institute, award # NNA13AA92A (to V.J.O.). G.L.C. was supported by the NIH/NRSA training grant, T32 GM007616. We would like to thank Michael Wagner and Holger Daims for their thoughtful reading and comments on the manuscript, as well as the careful attention of an anonymous reviewer. The authors declare that they have no conflict of interest.
Funders:
Funding AgencyGrant Number
Gordon and Betty Moore FoundationGBMF3780
Department of Energy (DOE)DE-SC0016469
NASANNA13AA92A
NIH Predoctoral FellowshipT32 GM007616
Issue or Number:11
PubMed Central ID:PMC6194058
Record Number:CaltechAUTHORS:20180711-165717508
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20180711-165717508
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:87789
Collection:CaltechAUTHORS
Deposited By: George Porter
Deposited On:12 Jul 2018 14:47
Last Modified:03 Oct 2019 19:59

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