Inside cows, goats, and other ruminants, fungal enzymes break down plant matter and extract nutrients. These enzymes essentially overcome a major bottleneck in biofuel production: breaking down lignocellulose—the primary building block of plant cell walls. The parts, assembly, and diverse roles of fungal enzyme complexes, called cellulosomes, have not been clearly defined. Until now. This study offers insights into the structure and function of fungal cellulosomes. In doing so, it shows that cellulosomes are evolutionary chimaeras that co-opted parts of enzymes from bacteria that are also found in the gut.
The findings highlight the power of fungal enzymes in breaking down lignocellulose. These enzymes could be harnessed to develop novel strategies for efficient biofuel production.
Gut microbes play a major role in helping ruminants such as cows, goats, and sheep break down lignocellulose-rich plant matter in their diet. Anaerobic bacteria and fungi inhabiting the ruminant gut have evolved a suite of lignocellulose-degrading enzymes, whose activity supports microbial metabolism while supplying nutrients to ruminants. These enzymes often assemble into large, multi-protein complexes called cellulosomes, which enhance the ability of gut microbes to degrade lignocellulose by confining all the enzymes in one place. Although bacterial cellulosomes now serve as a standard model for biomass conversion and synthetic biology applications, fungal cellulosomes have not been well characterized due to the lack of genomic and proteomic data, despite their potential value for biofuel and bio-based chemical production. To address this knowledge gap, researchers combined next-generation sequencing with functional proteomics to describe the comprehensive set of proteins that play a role in fungal cellulosome assembly. The collaborative team was from the University of California, Santa Barbara; the Environmental Molecular Sciences Laboratory (EMSL); the U.S. Department of Energy Joint Genome Institute (DOE JGI); Pacific Northwest National Laboratory; Centre National de la Recherche Scientifique; French National Institute for Agricultural Research; Radboud University; King Abdulaziz University; and the University of California, Berkeley. This research was performed under the Facilities Integrating Collaborations for User Science (FICUS) initiative. The team used resources at JGI and EMSL, which are DOE Office of Science user facilities. This analysis revealed a new family of genes that likely serve as scaffolding proteins critical for cellulosome assemblies across diverse species of anaerobic gut fungi. Unlike bacterial cellulosomes, which have high species specificity, fungal cellulosomes are likely a composite of enzymes from several species of gut fungi. Although many bacterial and fungal plant biomass-degrading enzymes have shared similarities, the fungal cellulosomes were found to contain additional lignocellulose-degrading enzymes not found in bacterial cellulosomes. These additional enzymes may not only confer a selective advantage of fungi over bacteria in the ruminant gut, but also impart fungal cellulosomes with great potential for biomass conversion. Taken together, the findings highlight key differences in bacterial and fungal cellulosomes and suggest enzyme connections (known as tethering) play an important role in plant cell wall degradation.
BER Program Manager
Paul Bayer, SC-23.1
U.S. Department of Energy
Michelle A. O'Malley
University of California, Santa Barbara
Environmental Molecular Sciences Laboratory
This work was supported by the U.S. Department of Energy's (DOE's) Office of Science, Office of Biological and Environmental Research, including support of the Environmental Molecular Sciences Laboratory (EMSL) and the DOE Joint Genome Institute (JGI), DOE Office of Science user facilities; U.S. Department of Agriculture; National Science Foundation; U.S. Army; University of California, Santa Barbara and Berkeley; and California NanoSystems Institute.
C.H. Haitjema, S.P. Gilmore, J.K. Henske, K.V. Solomon, R. de Groot, A. Kuo, S.J. Mondo, A.A. Salamov, K. LaButti, Z. Zhao, J. Chiniquy, K. Barry, H.M. Brewer, S.O. Purvine, A.T. Wright, M. Hainaut, B. Boxma, T. van Alen, J.H.P. Hackstein, B. Henrissat, S.E. Baker, I.V. Grigoriev, and M.A. O'Malley, "A parts list for fungal cellulosomes revealed by comparative genomics." Nature Microbiology 2, 17087 (2017). [DOI: 10.1038/nmicrobiol.2017.87]
Environmental Molecular Sciences Laboratory science highlight: Unlocking the Potential of Fungal Enzymes to Break Down Plant Cell Walls
Joint Genome Institute science highlight: Fungal Enzymes Team Up to More Efficiently Break Down Cellulose
Environmental Molecular Sciences Laboratory science highlight: Biofuel Breakdown