Genomes of rumen bacteria encode atypical pathways for fermenting hexoses to short-chain fatty acids

Handle URI:
http://hdl.handle.net/10754/625456
Title:
Genomes of rumen bacteria encode atypical pathways for fermenting hexoses to short-chain fatty acids
Authors:
Hackmann, Timothy J.; Ngugi, David ( 0000-0002-0442-4279 ) ; Firkins, Jeffrey L.; Tao, Junyi
Abstract:
Bacteria have been thought to follow only a few well-recognized biochemical pathways when fermenting glucose or other hexoses. These pathways have been chiseled in the stone of textbooks for decades, with most sources rendering them as they appear in the classic 1986 text by Gottschalk. Still, it is unclear how broadly these pathways apply, given that they were established and delineated biochemically with only a few model organisms. Here we show that well-recognized pathways often cannot explain fermentation products formed by bacteria. In the most extensive analysis of its kind, we reconstructed pathways for glucose fermentation from genomes of 48 species and subspecies of bacteria from one environment (the rumen). In total, 44% of these bacteria had atypical pathways, including several that are completely unprecedented for bacteria or any organism. In detail, 8% of bacteria had an atypical pathway for acetate formation; 21% for propionate or succinate formation; 6% for butyrate formation; and 33% had an atypical or incomplete Embden-Meyerhof-Parnas pathway. This study shows that reconstruction of metabolic pathways-a common goal of omics studies-could be incorrect if well-recognized pathways are used for reference. Further, it calls for renewed efforts to delineate fermentation pathways biochemically. This article is protected by copyright. All rights reserved.
KAUST Department:
Red Sea Research Center (RSRC)
Citation:
Hackmann TJ, Ngugi DK, Firkins JL, Tao J (2017) Genomes of rumen bacteria encode atypical pathways for fermenting hexoses to short-chain fatty acids. Environmental Microbiology. Available: http://dx.doi.org/10.1111/1462-2920.13929.
Publisher:
Wiley-Blackwell
Journal:
Environmental Microbiology
Issue Date:
11-Sep-2017
DOI:
10.1111/1462-2920.13929
Type:
Article
ISSN:
1462-2912
Sponsors:
We thank G. Suen (University of Wisconsin-Madison), A. Neumann (University of Wisconsin-Madison), and P. Weimer (USDA-ARS, Madison, WI) for conservations on missing pyruvate kinase in Fibrobacter. We also thank S. Hackmann (University of Florida) for reviewing the manuscript. This work was supported by U.S. Department of Agriculture (USDA) National Institute of Food and Agriculture (NIFA) Hatch Project FLA-ANS-005307 and USDA-NIFA Hatch/Multi-State Project FLA-ANS-005304.
Additional Links:
http://onlinelibrary.wiley.com/doi/10.1111/1462-2920.13929/abstract
Appears in Collections:
Articles; Red Sea Research Center (RSRC)

Full metadata record

DC FieldValue Language
dc.contributor.authorHackmann, Timothy J.en
dc.contributor.authorNgugi, Daviden
dc.contributor.authorFirkins, Jeffrey L.en
dc.contributor.authorTao, Junyien
dc.date.accessioned2017-09-14T06:03:52Z-
dc.date.available2017-09-14T06:03:52Z-
dc.date.issued2017-09-11en
dc.identifier.citationHackmann TJ, Ngugi DK, Firkins JL, Tao J (2017) Genomes of rumen bacteria encode atypical pathways for fermenting hexoses to short-chain fatty acids. Environmental Microbiology. Available: http://dx.doi.org/10.1111/1462-2920.13929.en
dc.identifier.issn1462-2912en
dc.identifier.doi10.1111/1462-2920.13929en
dc.identifier.urihttp://hdl.handle.net/10754/625456-
dc.description.abstractBacteria have been thought to follow only a few well-recognized biochemical pathways when fermenting glucose or other hexoses. These pathways have been chiseled in the stone of textbooks for decades, with most sources rendering them as they appear in the classic 1986 text by Gottschalk. Still, it is unclear how broadly these pathways apply, given that they were established and delineated biochemically with only a few model organisms. Here we show that well-recognized pathways often cannot explain fermentation products formed by bacteria. In the most extensive analysis of its kind, we reconstructed pathways for glucose fermentation from genomes of 48 species and subspecies of bacteria from one environment (the rumen). In total, 44% of these bacteria had atypical pathways, including several that are completely unprecedented for bacteria or any organism. In detail, 8% of bacteria had an atypical pathway for acetate formation; 21% for propionate or succinate formation; 6% for butyrate formation; and 33% had an atypical or incomplete Embden-Meyerhof-Parnas pathway. This study shows that reconstruction of metabolic pathways-a common goal of omics studies-could be incorrect if well-recognized pathways are used for reference. Further, it calls for renewed efforts to delineate fermentation pathways biochemically. This article is protected by copyright. All rights reserved.en
dc.description.sponsorshipWe thank G. Suen (University of Wisconsin-Madison), A. Neumann (University of Wisconsin-Madison), and P. Weimer (USDA-ARS, Madison, WI) for conservations on missing pyruvate kinase in Fibrobacter. We also thank S. Hackmann (University of Florida) for reviewing the manuscript. This work was supported by U.S. Department of Agriculture (USDA) National Institute of Food and Agriculture (NIFA) Hatch Project FLA-ANS-005307 and USDA-NIFA Hatch/Multi-State Project FLA-ANS-005304.en
dc.publisherWiley-Blackwellen
dc.relation.urlhttp://onlinelibrary.wiley.com/doi/10.1111/1462-2920.13929/abstracten
dc.rightsThis is the peer reviewed version of the following article: Genomes of rumen bacteria encode atypical pathways for fermenting hexoses to short-chain fatty acids, which has been published in final form at http://doi.org/10.1111/1462-2920.13929. This article may be used for non-commercial purposes in accordance With Wiley Terms and Conditions for self-archiving.en
dc.titleGenomes of rumen bacteria encode atypical pathways for fermenting hexoses to short-chain fatty acidsen
dc.typeArticleen
dc.contributor.departmentRed Sea Research Center (RSRC)en
dc.identifier.journalEnvironmental Microbiologyen
dc.eprint.versionPost-printen
dc.contributor.institutionDepartment of Animal Science; University of Florida, P.O. Box 110910; Gainesville Florida 32611 USAen
dc.contributor.institutionDepartment of Animal Science; The Ohio State University, 2029 Fyffe Rd; Columbus Ohio 43210 USAen
kaust.authorNgugi, Daviden
All Items in KAUST are protected by copyright, with all rights reserved, unless otherwise indicated.