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

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

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55 Scopus citations

Abstract

Background: 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. Methodology and Principal Findings: 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. Conclusions/Significance: 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.

Original languageEnglish (US)
Article numbere54337
JournalPLoS One
Volume8
Issue number1
DOIs
StatePublished - Jan 28 2013
Externally publishedYes

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

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    Petit, E., LaTouf, W. G., Coppi, M. V., Warnick, T. A., Currie, D., Romashko, I., Deshpande, S., Haas, K., Alvelo-Maurosa, J. G., Wardman, C., Schnell, D. J., Leschine, S. B., & Blanchard, J. L. (2013). Involvement of a Bacterial Microcompartment in the Metabolism of Fucose and Rhamnose by Clostridium phytofermentans. PLoS One, 8(1), [e54337]. https://doi.org/10.1371/journal.pone.0054337