Comparative analysis of extremely thermophilic Caldicellulosiruptor species reveals common and unique cellular strategies for plant biomass utilization

Jeffrey V. Zurawski, Jonathan M. Conway, Laura L. Lee, Hunter J. Simpson, Javier A. Izquierdo, Sara Blumer-Schuette, Intawat Nookaew, Michael W.W. Adams, Robert M. Kelly

Research output: Contribution to journalArticlepeer-review

28 Scopus citations

Abstract

Microbiological, genomic and transcriptomic analyses were used to examine three species from the bacterial genus Caldicellulosiruptor with respect to their capacity to convert the carbohydrate content of lignocellulosic biomass at 70°C to simple sugars, acetate, lactate, CO2, and H2. Caldicellulosiruptor bescii, C. kronotskyensis, and C. saccharolyticus solubilized 38%, 36%, and 29% (by weight) of unpretreated switchgrass (Panicum virgatum) (5 g/liter), respectively, which was about half of the amount of crystalline cellulose (Avicel; 5 g/liter) that was solubilized under the same conditions. The lower yields with C. saccharolyticus, not appreciably greater than the thermal control for switchgrass, were unexpected, given that its genome encodes the same glycoside hydrolase 9 (GH9)-GH48 multidomain cellulase (CelA) found in the other two species. However, the genome of C. saccharolyticus lacks two other cellulases with GH48 domains, which could be responsible for its lower levels of solubilization. Transcriptomes for growth of each species comparing cellulose to switchgrass showed that many carbohydrate ABC transporters and multidomain extracellular glycoside hydrolases were differentially regulated, reflecting the heterogeneity of lignocellulose. However, significant differences in transcription levels for conserved genes among the three species were noted, indicating unexpectedly diverse regulatory strategies for deconstruction for these closely related bacteria. Genes encoding the Che-type chemotaxis system and flagellum biosynthesis were upregulated in C. kronotskyensis and C. bescii during growth on cellulose, implicating motility in substrate utilization. The results here show that capacity for plant biomass deconstruction varies across Caldicellulosiruptor species and depends in a complex way on GH genome inventory, substrate composition, and gene regulation.

Original languageEnglish (US)
Pages (from-to)7159-7170
Number of pages12
JournalApplied and Environmental Microbiology
Volume81
Issue number20
DOIs
StatePublished - 2015
Externally publishedYes

All Science Journal Classification (ASJC) codes

  • Biotechnology
  • Food Science
  • Ecology
  • Applied Microbiology and Biotechnology

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