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

Abstract

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.

Authors:
 [1];  [1];  [1]
  1. Univ. of Oklahoma, Norman, OK (United States)
Publication Date:
Research Org.:
Univ. of Oklahoma, Norman, OK (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division
OSTI Identifier:
1604793
Grant/Contract Number:  
FG02-96ER20214
Resource Type:
Accepted Manuscript
Journal Name:
Environmental Microbiology
Additional Journal Information:
Journal Volume: 16; Journal Issue: 1; Journal ID: ISSN 1462-2912
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; syntrophy; methanogenesis; bioenergy

Citation Formats

Sieber, Jessica R., Le, Huynh M., and McInerney, Michael J. The importance of hydrogen and formate transfer for syntrophic fatty, aromatic and alicyclic metabolism [plus supplemental information]. United States: N. p., 2013. Web. doi:10.1111/1462-2920.12269.
Sieber, Jessica R., Le, Huynh M., & McInerney, Michael J. The importance of hydrogen and formate transfer for syntrophic fatty, aromatic and alicyclic metabolism [plus supplemental information]. United States. https://doi.org/10.1111/1462-2920.12269
Sieber, Jessica R., Le, Huynh M., and McInerney, Michael J. Wed . "The importance of hydrogen and formate transfer for syntrophic fatty, aromatic and alicyclic metabolism [plus supplemental information]". United States. https://doi.org/10.1111/1462-2920.12269. https://www.osti.gov/servlets/purl/1604793.
@article{osti_1604793,
title = {The importance of hydrogen and formate transfer for syntrophic fatty, aromatic and alicyclic metabolism [plus supplemental information]},
author = {Sieber, Jessica R. and Le, Huynh M. and McInerney, Michael J.},
abstractNote = {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.},
doi = {10.1111/1462-2920.12269},
journal = {Environmental Microbiology},
number = 1,
volume = 16,
place = {United States},
year = {Wed Sep 04 00:00:00 EDT 2013},
month = {Wed Sep 04 00:00:00 EDT 2013}
}

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