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Title: A parts list for fungal cellulosomes revealed by comparative genomics

Abstract

Cellulosomes are large, multiprotein complexes that tether plant biomass-degrading enzymes together for improved hydrolysis1. These complexes were first described in anaerobic bacteria, where species-specific dockerin domains mediate the assembly of enzymes onto cohesin motifs interspersed within protein scaffolds1. The versatile protein assembly mechanism conferred by the bacterial cohesin-dockerin interaction is now a standard design principle for synthetic biology2,3. For decades, analogous structures have been reported in anaerobic fungi, which are known to assemble by sequence-divergent non-catalytic dockerin domains (NCDDs)4. However, the components, modular assembly mechanism and functional role of fungal cellulosomes remain unknown5,6. Here, we describe a comprehensive set of proteins critical to fungal cellulosome assembly, including conserved scaffolding proteins unique to the Neocallimastigomycota. High-quality genomes of the anaerobic fungi Anaeromyces robustus, Neocallimastix californiae and Piromyces finnis were assembled with long-read, single-molecule technology. Genomic analysis coupled with proteomic validation revealed an average of 312 NCDD-containing proteins per fungal strain, which were overwhelmingly carbohydrate active enzymes (CAZymes), with 95 large fungal scaffoldins identified across four genera that bind to NCDDs. Fungal dockerin and scaffoldin domains have no similarity to their bacterial counterparts, yet several catalytic domains originated via horizontal gene transfer with gut bacteria. However, the biocatalytic activity of anaerobic fungalmore » cellulosomes is expanded by the inclusion of GH3, GH6 and GH45 enzymes. These findings suggest that the fungal cellulosome is an evolutionarily chimaeric structure-an independently evolved fungal complex that co-opted useful activities from bacterial neighbours within the gut microbiome.« less

Authors:
 [1];  [1];  [1]; ORCiD logo [2];  [1];  [3];  [3];  [3];  [3];  [3];  [3];  [3];  [4];  [4];  [4];  [5];  [6];  [7];  [6];  [8] more »; ORCiD logo [4];  [9];  [1] « less
+ Show Author Affiliations
  1. Univ. of California, Santa Barbara, CA (United States)
  2. Univ. of California, Santa Barbara, CA (United States); Purdue Univ., West Lafayette, IN (United States); Radboud Univ. (The Netherlands)
  3. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
  4. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  5. Aix-Marseille Univ., Marseille (France); INRA, USC, Marseille (France)
  6. Radboud Univ. (The Netherlands)
  7. Radboud Univ. (The Netherlands); Purdue Univ., West Lafayette, IN (United States)
  8. Aix-Marseille Univ., Marseille (France); INRA, USC, Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
  9. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States); Univ. of California, Berkeley, CA (United States)
Publication Date:
Research Org.:
Univ. of California, Santa Barbara, CA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division
OSTI Identifier:
1485163
Alternate Identifier(s):
OSTI ID: 1619077
Grant/Contract Number:  
SC0010352; AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Nature Microbiology
Additional Journal Information:
Journal Volume: 2; Journal ID: ISSN 2058-5276
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS

Citation Formats

Haitjema, Charles H., Gilmore, Sean P., Henske, John K., Solomon, Kevin V., de Groot, Randall, Kuo, Alan, Mondo, Stephen J., Salamov, Asaf A., LaButti, Kurt, Zhao, Zhiying, Chiniquy, Jennifer, Barry, Kerrie, Brewer, Heather M., Purvine, Samuel O., Wright, Aaron T., Hainaut, Matthieu, Boxma, Brigitte, van Alen, Theo, Hackstein, Johannes H. P., Henrissat, Bernard, Baker, Scott E., Grigoriev, Igor V., and O'Malley, Michelle A. A parts list for fungal cellulosomes revealed by comparative genomics. United States: N. p., 2017. Web. doi:10.1038/nmicrobiol.2017.87.
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Haitjema, Charles H., Gilmore, Sean P., Henske, John K., Solomon, Kevin V., de Groot, Randall, Kuo, Alan, Mondo, Stephen J., Salamov, Asaf A., LaButti, Kurt, Zhao, Zhiying, Chiniquy, Jennifer, Barry, Kerrie, Brewer, Heather M., Purvine, Samuel O., Wright, Aaron T., Hainaut, Matthieu, Boxma, Brigitte, van Alen, Theo, Hackstein, Johannes H. P., Henrissat, Bernard, Baker, Scott E., Grigoriev, Igor V., & O'Malley, Michelle A. A parts list for fungal cellulosomes revealed by comparative genomics. United States. https://doi.org/10.1038/nmicrobiol.2017.87
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Haitjema, Charles H., Gilmore, Sean P., Henske, John K., Solomon, Kevin V., de Groot, Randall, Kuo, Alan, Mondo, Stephen J., Salamov, Asaf A., LaButti, Kurt, Zhao, Zhiying, Chiniquy, Jennifer, Barry, Kerrie, Brewer, Heather M., Purvine, Samuel O., Wright, Aaron T., Hainaut, Matthieu, Boxma, Brigitte, van Alen, Theo, Hackstein, Johannes H. P., Henrissat, Bernard, Baker, Scott E., Grigoriev, Igor V., and O'Malley, Michelle A. Tue . "A parts list for fungal cellulosomes revealed by comparative genomics". United States. https://doi.org/10.1038/nmicrobiol.2017.87. https://www.osti.gov/servlets/purl/1485163.
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@article{osti_1485163,
title = {A parts list for fungal cellulosomes revealed by comparative genomics},
author = {Haitjema, Charles H. and Gilmore, Sean P. and Henske, John K. and Solomon, Kevin V. and de Groot, Randall and Kuo, Alan and Mondo, Stephen J. and Salamov, Asaf A. and LaButti, Kurt and Zhao, Zhiying and Chiniquy, Jennifer and Barry, Kerrie and Brewer, Heather M. and Purvine, Samuel O. and Wright, Aaron T. and Hainaut, Matthieu and Boxma, Brigitte and van Alen, Theo and Hackstein, Johannes H. P. and Henrissat, Bernard and Baker, Scott E. and Grigoriev, Igor V. and O'Malley, Michelle A.},
abstractNote = {Cellulosomes are large, multiprotein complexes that tether plant biomass-degrading enzymes together for improved hydrolysis1. These complexes were first described in anaerobic bacteria, where species-specific dockerin domains mediate the assembly of enzymes onto cohesin motifs interspersed within protein scaffolds1. The versatile protein assembly mechanism conferred by the bacterial cohesin-dockerin interaction is now a standard design principle for synthetic biology2,3. For decades, analogous structures have been reported in anaerobic fungi, which are known to assemble by sequence-divergent non-catalytic dockerin domains (NCDDs)4. However, the components, modular assembly mechanism and functional role of fungal cellulosomes remain unknown5,6. Here, we describe a comprehensive set of proteins critical to fungal cellulosome assembly, including conserved scaffolding proteins unique to the Neocallimastigomycota. High-quality genomes of the anaerobic fungi Anaeromyces robustus, Neocallimastix californiae and Piromyces finnis were assembled with long-read, single-molecule technology. Genomic analysis coupled with proteomic validation revealed an average of 312 NCDD-containing proteins per fungal strain, which were overwhelmingly carbohydrate active enzymes (CAZymes), with 95 large fungal scaffoldins identified across four genera that bind to NCDDs. Fungal dockerin and scaffoldin domains have no similarity to their bacterial counterparts, yet several catalytic domains originated via horizontal gene transfer with gut bacteria. However, the biocatalytic activity of anaerobic fungal cellulosomes is expanded by the inclusion of GH3, GH6 and GH45 enzymes. These findings suggest that the fungal cellulosome is an evolutionarily chimaeric structure-an independently evolved fungal complex that co-opted useful activities from bacterial neighbours within the gut microbiome.},
doi = {10.1038/nmicrobiol.2017.87},
journal = {Nature Microbiology},
number = ,
volume = 2,
place = {United States},
year = {Tue May 30 00:00:00 EDT 2017},
month = {Tue May 30 00:00:00 EDT 2017}
}
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https://doi.org/10.1038/nmicrobiol.2017.87
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    Biomass-degrading enzymes are catabolite repressed in anaerobic gut fungi
    journal, October 2018

    • Henske, John K.; Gilmore, Sean P.; Haitjema, Charles H.
    • AIChE Journal, Vol. 64, Issue 12
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    Co-cultivation of the anaerobic fungus Anaeromyces robustus with Methanobacterium bryantii enhances transcription of carbohydrate active enzymes
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    Transcriptomic characterization of Caecomyces churrovis: a novel, non-rhizoid-forming lignocellulolytic anaerobic fungus
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    Genome expansion by allopolyploidization in the fungal strain Coniochaeta 2T2.1 and its exceptional lignocellulolytic machinery
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    • Mondo, Stephen J.; Jiménez, Diego Javier; Hector, Ronald E.
    • Biotechnology for Biofuels, Vol. 12, Issue 1
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    PCR and Omics Based Techniques to Study the Diversity, Ecology and Biology of Anaerobic Fungi: Insights, Challenges and Opportunities
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    • Mondo, Stephen J.; Jiménez, Diego Javier; Hector, Ronald E.
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    PCR and Omics Based Techniques to Study the Diversity, Ecology and Biology of Anaerobic Fungi: Insights, Challenges and Opportunities
    journal, September 2017

    • Edwards, Joan E.; Forster, Robert J.; Callaghan, Tony M.
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    • DOI: 10.3389/fmicb.2017.01657
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