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Nat Microbiol. 2017 May 30;2:17087. doi: 10.1038/nmicrobiol.2017.87.

A parts list for fungal cellulosomes revealed by comparative genomics.

Author information

1
Department of Chemical Engineering, University of California, Santa Barbara, California 93106, USA.
2
US Department of Energy Joint Genome Institute, 2800 Mitchell Drive, Walnut Creek, California 94598, USA.
3
Environmental Molecular Sciences Laboratory, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington 99354, USA.
4
Biological Sciences Division, Earth and Biological Sciences Directorate, Pacific Northwest National Laboratory, Richland, Washington 99354, USA.
5
Architecture et Fonction des Macromolécules Biologiques, Centre National de la Recherche Scientifique, Aix-Marseille Université, 13288 Marseille, France.
6
INRA, USC 1408 AFMB, Marseille, France.
7
Department of Evolutionary Microbiology, Radboud University, 6525 AJ Nijmegen, The Netherlands.
8
Department of Biological Sciences, King Abdulaziz University, 23218 Jeddah, Saudi Arabia.
9
Department of Plant and Microbial Biology, University of California, Berkeley, California 94720, USA.

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.

PMID:
28555641
DOI:
10.1038/nmicrobiol.2017.87
[Indexed for MEDLINE]

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