Metabolic characterization of anaerobic fungi provides a path forward for bioprocessing of crude lignocellulose

Henske, John K.; Wilken, St. Elmo; Solomon, Kevin V.; Smallwood, Chuck R.; Shutthanandan, Vaithiyalingam; Evans, James E.; Theodorou, Michael K.; O'Malley, Michelle A.

doi:10.1002/bit.26515

Title: Metabolic characterization of anaerobic fungi provides a path forward for bioprocessing of crude lignocellulose

Journal Article · Thu Dec 14 00:00:00 EST 2017 · Biotechnology and Bioengineering

DOI:https://doi.org/10.1002/bit.26515· OSTI ID:1485153

Henske, John K. ^[1]; Wilken, St. Elmo ^[1]; Solomon, Kevin V. ^[2]; Smallwood, Chuck R. ^[3]; Shutthanandan, Vaithiyalingam ^[3]; Evans, James E. ^[3]; Theodorou, Michael K. ^[4];

^[1]

Univ. of California, Santa Barbara, CA (United States). Department of Chemical Engineering
Univ. of California, Santa Barbara, CA (United States). Department of Chemical Engineering; Purdue Univ., West Lafayette, IN (United States). Agriculture and Biological Engineering
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
Harper Adams University, Newport, Shropshire (United Kingdom). Animal Production, Welfare and Veterinary Sciences

The conversion of lignocellulose-rich biomass to bio-based chemicals and higher order fuels remains a grand challenge, as single-microbe approaches often cannot drive both deconstruction and chemical production steps. In contrast, consortia based bioprocessing leverages the strengths of different microbes to distribute metabolic loads and achieve process synergy, product diversity, and bolster yields. In this paper, we describe a biphasic fermentation scheme that combines the lignocellulolytic action of anaerobic fungi isolated from large herbivores with domesticated microbes for bioproduction. When grown in batch culture, anaerobic fungi release excess sugars from both cellulose and crude biomass due to a wealth of highly expressed carbohydrate active enzymes (CAZymes), converting as much as 49% of cellulose to free glucose. This sugar-rich hydrolysate readily supports growth of Saccharomyces cerevisiae, which can be engineered to produce a range of value-added chemicals. Further, construction of metabolic pathways from transcriptomic data reveals that anaerobic fungi do not catabolize all sugars that their enzymes hydrolyze from biomass, leaving other carbohydrates such as galactose, arabinose, and mannose available as nutritional links to other microbes in their consortium. Although basal expression of CAZymes in anaerobic fungi is high, it is drastically amplified by cellobiose breakout products encountered during biomass hydrolysis. In conclusion, these results suggest that anaerobic fungi provide a nutritional benefit to the rumen microbiome, which can be harnessed to design synthetic microbial communities that compartmentalize biomass degradation and bioproduct formation.

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Research Organization:: Univ. of California, Santa Barbara, CA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: SC0010352; AC02-05CH11231; AC05-76RL01830; W911NF-09-0001

OSTI ID:: 1485153

Alternate ID(s):: OSTI ID: 1416400

Journal Information:: Biotechnology and Bioengineering, Vol. 115, Issue 4; ISSN 0006-3592

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 41 works

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Biomass-degrading enzymes are catabolite repressed in anaerobic gut fungi Henske, John K.; Gilmore, Sean P.; Haitjema, Charles H. AIChE Journal, Vol. 64, Issue 12 https://doi.org/10.1002/aic.16395	journal	October 2018
From molecules to multispecies ecosystems: the roles of structure in bacterial biofilms Gordon, Vernita; Bakhtiari, Layla; Kovach, Kristin Physical Biology, Vol. 16, Issue 4 https://doi.org/10.1088/1478-3975/ab1384	journal	April 2019
Hydrolysis of untreated lignocellulosic feedstock is independent of S-lignin composition in newly classified anaerobic fungal isolate, Piromyces sp. UH3-1 Hooker, Casey A.; Hillman, Ethan T.; Overton, Jonathan C. Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1292-8	journal	October 2018
Effects of Piromyces sp. CN6 CGMCC 14449 on fermentation quality, nutrient composition and the in vitro degradation rate of whole crop maize silage Wang, Dangdang; Zhao, Congcong; Liu, Shimin AMB Express, Vol. 9, Issue 1 https://doi.org/10.1186/s13568-019-0846-x	journal	July 2019
Transcriptomic characterization of Caecomyces churrovis: a novel, non-rhizoid-forming lignocellulolytic anaerobic fungus Henske, John K.; Gilmore, Sean P.; Knop, Doriv Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0997-4	journal	December 2017
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Genomic and proteomic biases inform metabolic engineering strategies for anaerobic fungi Wilken, St. Elmo; Seppälä, Susanna; Lankiewicz, Thomas S. Metabolic Engineering Communications, Vol. 10 https://doi.org/10.1016/j.mec.2019.e00107	journal	June 2020
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Related Subjects

09 BIOMASS FUELS
59 BASIC BIOLOGICAL SCIENCES
anaerobic fungi
biomass hydrolysis
bioprocessing
cellulase
sugar metabolism

Title: Metabolic characterization of anaerobic fungi provides a path forward for bioprocessing of crude lignocellulose

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