Convergent evolution of processivity in bacterial and fungal cellulases

Taku Uchiyama (Corresponding Author), Takayuki Uchihashi, Akihiko Nakamura, Hiroki Watanabe, Satoshi Kaneko, Masahiro Samejima, Kiyohiko Igarashi

Research output: Contribution to journalArticleScientificpeer-review

Abstract

Cellulose is the most abundant biomass on Earth, and many microorganisms depend on it as a source of energy. It consists mainly of crystalline and amorphous regions, and natural degradation of the crystalline part is highly dependent on the degree of processivity of the degrading enzymes (i.e., the extent of continuous hydrolysis without detachment from the substrate cellulose). Here, we report high-speed atomic force microscopic (HS-AFM) observations of the movement of four types of cellulases derived from the cellulolytic bacteria Cellulomonas fimi on various insoluble cellulose substrates. The HS-AFM images clearly demonstrated that two of them (CfCel6B and CfCel48A) slide on crystalline cellulose. The direction of processive movement of CfCel6B is from the nonreducing to the reducing end of the substrate, which is opposite that of processive cellulase Cel7A of the fungus Trichoderma reesei (TrCel7A), whose movement was first observed by this technique, while CfCel48A moves in the same direction as TrCel7A. When CfCel6B and TrCel7A were mixed on the same substrate, "traffic accidents" were observed, in which the two cellulases blocked each other's progress. The processivity of CfCel6B was similar to those of fungal family 7 cellulases but considerably higher than those of fungal family 6 cellulases. The results indicate that bacteria utilize family 6 cellulases as high-processivity enzymes for efficient degradation of crystalline cellulose, whereas family 7 enzymes have the same function in fungi. This is consistent with the idea of convergent evolution of processive cellulases in fungi and bacteria to achieve similar functionality using different protein foldings.

Original languageEnglish
Pages (from-to)19896-19903
Number of pages8
JournalProceedings of the National Academy of Sciences of the United States of America
Volume117
Issue number33
DOIs
Publication statusPublished - 18 Aug 2020
MoE publication typeA1 Journal article-refereed

Keywords

  • biomass utilization
  • cellobiohydrolase
  • cellulase
  • crystalline cellulose
  • processivity

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    Uchiyama, T., Uchihashi, T., Nakamura, A., Watanabe, H., Kaneko, S., Samejima, M., & Igarashi, K. (2020). Convergent evolution of processivity in bacterial and fungal cellulases. Proceedings of the National Academy of Sciences of the United States of America, 117(33), 19896-19903. https://doi.org/10.1073/pnas.2011366117