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Physiological, genomic, and sulfur isotopic characterization of methanol metabolism by Desulfovibrio carbinolicus

Sim, Min Sub and Skennerton, Connor T. and Orphan, Victoria J. (2021) Physiological, genomic, and sulfur isotopic characterization of methanol metabolism by Desulfovibrio carbinolicus. PLoS ONE, 16 (1). Art. No. e0245069. ISSN 1932-6203. https://resolver.caltech.edu/CaltechAUTHORS:20210115-120616827

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Abstract

Methanol is often considered as a non-competitive substrate for methanogenic archaea, but an increasing number of sulfate-reducing microorganisms (SRMs) have been reported to be capable of respiring with methanol as an electron donor. A better understanding of the fate of methanol in natural or artificial anaerobic systems thus requires knowledge of the methanol dissimilation by SRMs. In this study, we describe the growth kinetics and sulfur isotope effects of Desulfovibrio carbinolicus, a methanol-oxidizing sulfate-reducing deltaproteobacterium, together with its genome sequence and annotation. D. carbinolicus can grow with a series of alcohols from methanol to butanol. Compared to longer-chain alcohols, however, specific growth and respiration rates decrease by several fold with methanol as an electron donor. Larger sulfur isotope fractionation accompanies slowed growth kinetics, indicating low chemical potential at terminal reductive steps of respiration. In a medium containing both ethanol and methanol, D. carbinolicus does not consume methanol even after the cessation of growth on ethanol. Among the two known methanol dissimilatory systems, the genome of D. carbinolicus contains the genes coding for alcohol dehydrogenase but lacks enzymes analogous to methanol methyltransferase. We analyzed the genomes of 52 additional species of sulfate-reducing bacteria that have been tested for methanol oxidation. There is no apparent relationship between phylogeny and methanol metabolizing capacity, but most gram-negative methanol oxidizers grow poorly, and none carry homologs for methyltransferase (mtaB). Although the amount of available data is limited, it is notable that more than half of the known gram-positive methanol oxidizers have both enzymatic systems, showing enhanced growth relative to the SRMs containing only alcohol dehydrogenase genes. Thus, physiological, genomic, and sulfur isotopic results suggest that D. carbinolicus and close relatives have the ability to metabolize methanol but likely play a limited role in methanol degradation in most natural environments.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1371/journal.pone.0245069DOIArticle
ORCID:
AuthorORCID
Sim, Min Sub0000-0002-3491-9002
Skennerton, Connor T.0000-0003-1320-4873
Orphan, Victoria J.0000-0002-5374-6178
Additional Information:© 2021 Sim et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Received: September 6, 2020; Accepted: December 21, 2020; Published: January 14, 2021. Funding: This work was supported by the Mid-Career Researcher Program (2019R1A2C1087039) through the National Research Foundation of Korea (NRF) funded by the Korea government (MSIT) to MSS, and Gordon and Betty Moore Foundation Grant GBMF 3306 and the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research program DE-SC0020373 to VJO. The funders have no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The authors have declared that no competing interests exist. Data Availability Statement: All relevant data are included within the paper. Author Contributions: Conceptualization: Min Sub Sim, Victoria J. Orphan. Data curation: Min Sub Sim, Connor T. Skennerton. Formal analysis: Min Sub Sim, Connor T. Skennerton. Investigation: Min Sub Sim, Connor T. Skennerton, Victoria J. Orphan. Resources: Victoria J. Orphan. Writing – original draft: Min Sub Sim, Connor T. Skennerton. Writing – review & editing: Min Sub Sim, Connor T. Skennerton, Victoria J. Orphan.
Funders:
Funding AgencyGrant Number
National Research Foundation of Korea2019R1A2C1087039
Gordon and Betty Moore FoundationGBMF 3306
Department of Energy (DOE)DE-SC0020373
Issue or Number:1
Record Number:CaltechAUTHORS:20210115-120616827
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20210115-120616827
Official Citation:Sim MS, Skennerton CT, Orphan VJ. (2021) Physiological, genomic, and sulfur isotopic characterization of methanol metabolism by Desulfovibrio carbinolicus. PLoS ONE 16(1):e0245069. https://doi.org/10.1371/journal.pone.0245069
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:107508
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:15 Jan 2021 20:54
Last Modified:15 Jan 2021 20:54

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