The genome sequences of Cellulomonas fimi and "Cellvibrio gilvus" reveal the cellulolytic strategies of two facultative anaerobes, transfer of "Cellvibrio gilvus" to the genus Cellulomonas, and proposal of Cellulomonas gilvus sp. nov

PLoS One. 2013;8(1):e53954. doi: 10.1371/journal.pone.0053954. Epub 2013 Jan 14.

Abstract

Actinobacteria in the genus Cellulomonas are the only known and reported cellulolytic facultative anaerobes. To better understand the cellulolytic strategy employed by these bacteria, we sequenced the genome of the Cellulomonas fimi ATCC 484(T). For comparative purposes, we also sequenced the genome of the aerobic cellulolytic "Cellvibrio gilvus" ATCC 13127(T). An initial analysis of these genomes using phylogenetic and whole-genome comparison revealed that "Cellvibrio gilvus" belongs to the genus Cellulomonas. We thus propose to assign "Cellvibrio gilvus" to the genus Cellulomonas. A comparative genomics analysis between these two Cellulomonas genome sequences and the recently completed genome for Cellulomonas flavigena ATCC 482(T) showed that these cellulomonads do not encode cellulosomes but appear to degrade cellulose by secreting multi-domain glycoside hydrolases. Despite the minimal number of carbohydrate-active enzymes encoded by these genomes, as compared to other known cellulolytic organisms, these bacteria were found to be proficient at degrading and utilizing a diverse set of carbohydrates, including crystalline cellulose. Moreover, they also encode for proteins required for the fermentation of hexose and xylose sugars into products such as ethanol. Finally, we found relatively few significant differences between the predicted carbohydrate-active enzymes encoded by these Cellulomonas genomes, in contrast to previous studies reporting differences in physiological approaches for carbohydrate degradation. Our sequencing and analysis of these genomes sheds light onto the mechanism through which these facultative anaerobes degrade cellulose, suggesting that the sequenced cellulomonads use secreted, multidomain enzymes to degrade cellulose in a way that is distinct from known anaerobic cellulolytic strategies.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Cellulomonas / classification
  • Cellulomonas / genetics*
  • Cellulomonas / metabolism*
  • Cellulose / metabolism*
  • Cellvibrio / classification
  • Cellvibrio / genetics*
  • Cellvibrio / metabolism*
  • Energy Metabolism / genetics
  • Fermentation / genetics
  • Genome, Bacterial / genetics*
  • Hydrolysis
  • Phylogeny
  • Polysaccharides / metabolism
  • Sequence Homology, Nucleic Acid

Substances

  • Polysaccharides
  • hemicellulose
  • Cellulose

Grants and funding

This work was funded in part by the DOE Great Lakes Bioenergy Research Center (GLBRC) (DOE BER Office of Science DE-FC02–07ER64494) supporting FOA, DM, and PJB. This work was also supported by a DOE BER Early Career Research Program Award DE–SC0008104 and funding from the Wisconsin Bioenergy Initiative to GS. MRC was supported by a DOE GLBRC/BACTER Post-doctoral Research Fellowship. The work conducted by the US Department of Energy Joint Genome Institute is supported by the Office of Science of the US Department of Energy under Contract No. DE-AC02-05CH11231. All work performed by employees of Lucigen or C5–6 Technologies was performed under and supported by subcontract to the GLBRC. Neither corporation was a funder of the work; no funds of either corporation was used for this research or to support the researchers during performance of this work. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.