A parts list for fungal cellulosomes revealed by comparative genomics View Full Text


Ontology type: schema:ScholarlyArticle      Open Access: True


Article Info

DATE

2017-05-30

AUTHORS

Charles H. Haitjema, Sean P. Gilmore, John K. Henske, Kevin V. Solomon, Randall de Groot, Alan Kuo, Stephen J. Mondo, Asaf A. Salamov, Kurt LaButti, Zhiying Zhao, Jennifer Chiniquy, Kerrie Barry, Heather M. Brewer, Samuel O. Purvine, Aaron T. Wright, Matthieu Hainaut, Brigitte Boxma, Theo van Alen, Johannes H. P. Hackstein, Bernard Henrissat, Scott E. Baker, Igor V. Grigoriev, Michelle A. O'Malley

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 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. More... »

PAGES

17087

Identifiers

URI

http://scigraph.springernature.com/pub.10.1038/nmicrobiol.2017.87

DOI

http://dx.doi.org/10.1038/nmicrobiol.2017.87

DIMENSIONS

https://app.dimensions.ai/details/publication/pub.1085662601

PUBMED

https://www.ncbi.nlm.nih.gov/pubmed/28555641


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360 Department of Chemical Engineering, University of California, 93106, Santa Barbara, California, USA
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363 schema:name Architecture et Fonction des Macromolécules Biologiques, Centre National de la Recherche Scientifique, Aix-Marseille Université, 13288 Marseille, France
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365 INRA, USC 1408 AFMB, Marseille, France
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375 grid-institutes:grid.47840.3f schema:alternateName Department of Plant and Microbial Biology, University of California, 94720, Berkeley, California, USA
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377 US Department of Energy Joint Genome Institute, 2800 Mitchell Drive, 94598, Walnut Creek, California, USA
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380 Department of Microbiology, Faculty of Science, Radboud University, PO Box 9010, 6500 GL, Nijmegen, The Netherlands
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