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Title: The importance of hydrogen and formate transfer for syntrophic fatty, aromatic and alicyclic metabolism [plus supplemental information]

Journal Article · · Environmental Microbiology

In this study, we used a combination of genomic, transcriptional, and enzymatic analyses to determine the mechanism of interspecies electron transfer by two model syntrophic microorganisms, Syntrophomonas wolfei and Syntrophus aciditrophicus. Both organisms contain multiple hydrogenase and formate dehydrogenase genes, but lack genes for outer membrane cytochromes and nanowire formation. Syntrophically grown cells and cell-free extracts of S. aciditrophicus and S. wolfei had both hydrogenase and formate dehydrogenase activities. Butyrate metabolism and CH4 production by washed cell suspensions of S. wolfei and Methanospirillum hungatei were inhibited by hydrogenase inhibitors (cyanide and carbon monoxide), but not by a formate dehydrogenase inhibitor (hypophosphite). Syntrophic benzoate oxidation and CH4 production by washed cell suspensions of S. aciditrophicus and M. hungatei were inhibited by hypophosphite, but not cyanide and carbon monoxide. All three inhibitors halted syntrophic cyclohexane-1-carboxylate metabolism. Two hydrogenase genes, hydA1 and hydA2, were more highly expressed when S. wolfei was grown syntrophically. S. aciditrophicus expressed multiple hydrogenase and formate dehydrogenase genes during syntrophic benzoate and cyclohexane-1-carboxylate growth, one of which (fdhA2) was highly differentially expressed during syntrophic benzoate growth. Therefore, these syntrophic microorganisms have flexible metabolisms that allow them to use either H2 or formate transfer depending on the substrate involved.

Research Organization:
Univ. of Oklahoma, Norman, OK (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division
Grant/Contract Number:
FG02-96ER20214
OSTI ID:
1604793
Journal Information:
Environmental Microbiology, Vol. 16, Issue 1; ISSN 1462-2912
Publisher:
WileyCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 67 works
Citation information provided by
Web of Science

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Membrane Complexes of Syntrophomonas wolfei Involved in Syntrophic Butyrate Degradation and Hydrogen Formation journal November 2016
Expanding the Diet for DIET: Electron Donors Supporting Direct Interspecies Electron Transfer (DIET) in Defined Co-Cultures journal March 2016
Stimulation of carbon nanomaterials on syntrophic oxidation of butyrate in sediment enrichments and a defined coculture journal August 2018
Plugging in or going wireless: strategies for interspecies electron transfer journal May 2014
Hydrogen or formate: Alternative key players in methanogenic degradation: Hydrogen/formate as interspecies electron carriers journal March 2017
Syntrophus conductive pili demonstrate that common hydrogen-donating syntrophs can have a direct electron transfer option journal January 2020
Elucidating Syntrophic Butyrate-Degrading Populations in Anaerobic Digesters Using Stable-Isotope-Informed Genome-Resolved Metagenomics journal August 2019
Proteomic analysis reveals metabolic and regulatory systems involved in the syntrophic and axenic lifestyle of Syntrophomonas wolfei journal February 2015
Trace Elements Induce Predominance among Methanogenic Activity in Anaerobic Digestion journal December 2016
Obligate sugar oxidation in Mesotoga spp., phylum Thermotogae , in the presence of either elemental sulfur or hydrogenotrophic sulfate-reducers as electron acceptor: Obligate sugar oxidation by Mesotoga spp. journal December 2017
Syntrophic growth via quinone-mediated interspecies electron transfer journal February 2015
Use of Acetate, Propionate, and Butyrate for Reduction of Nitrate and Sulfate and Methanogenesis in Microcosms and Bioreactors Simulating an Oil Reservoir journal January 2017
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DNA-SIP based genome-centric metagenomics identifies key long-chain fatty acid-degrading populations in anaerobic digesters with different feeding frequencies journal September 2017
Microbial dark matter ecogenomics reveals complex synergistic networks in a methanogenic bioreactor journal January 2015
Carbon nanotubes accelerate methane production in pure cultures of methanogens and in a syntrophic coculture: CNT accelerate methanogenesis in pure cultures journal June 2017