Involvement of a Bacterial Microcompartment in the Metabolism of Fucose and Rhamnose by Clostridium phytofermentans

Petit, Elsa; LaTouf, W. Greg; Coppi, Maddalena V.; Warnick, Thomas A.; Currie, Devin; Romashko, Igor; Deshpande, Supriya; Haas, Kelly; Alvelo-Maurosa, Jesús G.; Wardman, Colin; Schnell, Danny J.; Leschine, Susan B.; Blanchard, Jeffrey L.

doi:10.1371/journal.pone.0054337

Title: Involvement of a Bacterial Microcompartment in the Metabolism of Fucose and Rhamnose by Clostridium phytofermentans

Journal Article · Mon Jan 28 00:00:00 EST 2013 · PLoS ONE

DOI:https://doi.org/10.1371/journal.pone.0054337· OSTI ID:1904702

Petit, Elsa ^[1]; LaTouf, W. Greg ^[1]; Coppi, Maddalena V. ^[1]; Warnick, Thomas A. ^[1]; Currie, Devin ^[1]; Romashko, Igor ^[1]; Deshpande, Supriya ^[1]; Haas, Kelly ^[1]; Alvelo-Maurosa, Jesús G. ^[1]; Wardman, Colin ^[1]; Schnell, Danny J. ^[1]; Leschine, Susan B. ^[1]; Blanchard, Jeffrey L. ^[1]

University of Massachusetts, Amherst, MA (United States)

Clostridium phytofermentans, an anaerobic soil bacterium, can directly convert plant biomass into biofuels. The genome of C. phytofermentans contains three loci with genes encoding shell proteins of bacterial microcompartments (BMC), organelles composed entirely of proteins. One of the BMC loci has homology to a BMC-encoding locus implicated in the conversion of fucose to propanol and propionate in a human gut commensal, Roseburia inulinivorans. We hypothesized that it had a similar role in C. phytofermentans. When C. phytofermentans was grown on fucose, the major products identified were ethanol, propanol and propionate. Transmission electron microscopy of fucose- and rhamnose-grown cultures revealed polyhedral structures, presumably BMCs. Microarray analysis indicated that during growth on fucose, operons coding for the BMC locus, fucose dissimilatory enzymes, and an ATP-binding cassette transporter became the dominant transcripts. These data are consistent with fucose fermentation producing a 1,2-propanediol intermediate that is further metabolized in the microcompartment encoded in the BMC locus. Growth on another deoxyhexose sugar, rhamnose, resulted in the expression of the same BMC locus and similar fermentation products. However, a different set of dissimilatory enzymes and transport system genes were induced. Quite surprisingly, growth on fucose or rhamnose also led to the expression of a diverse array of complex plant polysaccharide-degrading enzymes. Based on physiological, genomic, and microarray analyses, we propose a model for the fermentation of fucose and rhamnose in C. phytofermentans that includes enzymes encoded in the same BMC locus. Comparative genomic analysis suggests that this BMC may be present in other clostridial species.

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Research Organization:: Univ. of Massachusetts, Amherst, MA (United States)

Sponsoring Organization:: USDOE Office of Science (SC); US Department of Agriculture (USDA); National Science Foundation (NSF); Qteros

Grant/Contract Number:: FG02-02ER15330; BBS 8714235

OSTI ID:: 1904702

Journal Information:: PLoS ONE, Vol. 8, Issue 1; ISSN 1932-6203

Publisher:: Public Library of ScienceCopyright Statement

Country of Publication:: United States

Language:: English

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Title: Involvement of a Bacterial Microcompartment in the Metabolism of Fucose and Rhamnose by Clostridium phytofermentans

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