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

Abstract

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. Inmore » 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.« less

Authors:
 [1];  [1];  [2];  [3];  [3];  [3];  [4]; ORCiD logo [1]
  1. Univ. of California, Santa Barbara, CA (United States). Department of Chemical Engineering
  2. Univ. of California, Santa Barbara, CA (United States). Department of Chemical Engineering; Purdue Univ., West Lafayette, IN (United States). Agriculture and Biological Engineering
  3. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
  4. Harper Adams University, Newport, Shropshire (United Kingdom). Animal Production, Welfare and Veterinary Sciences
Publication Date:
Research Org.:
Univ. of California, Santa Barbara, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1485153
Alternate Identifier(s):
OSTI ID: 1416400
Grant/Contract Number:  
SC0010352; AC02-05CH11231; AC05-76RL01830; W911NF-09-0001
Resource Type:
Accepted Manuscript
Journal Name:
Biotechnology and Bioengineering
Additional Journal Information:
Journal Volume: 115; Journal Issue: 4; Journal ID: ISSN 0006-3592
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; 59 BASIC BIOLOGICAL SCIENCES; anaerobic fungi; biomass hydrolysis; bioprocessing; cellulase; sugar metabolism

Citation Formats

Henske, John K., Wilken, St. Elmo, Solomon, Kevin V., Smallwood, Chuck R., Shutthanandan, Vaithiyalingam, Evans, James E., Theodorou, Michael K., and O'Malley, Michelle A. Metabolic characterization of anaerobic fungi provides a path forward for bioprocessing of crude lignocellulose. United States: N. p., 2017. Web. doi:10.1002/bit.26515.
Henske, John K., Wilken, St. Elmo, Solomon, Kevin V., Smallwood, Chuck R., Shutthanandan, Vaithiyalingam, Evans, James E., Theodorou, Michael K., & O'Malley, Michelle A. Metabolic characterization of anaerobic fungi provides a path forward for bioprocessing of crude lignocellulose. United States. doi:10.1002/bit.26515.
Henske, John K., Wilken, St. Elmo, Solomon, Kevin V., Smallwood, Chuck R., Shutthanandan, Vaithiyalingam, Evans, James E., Theodorou, Michael K., and O'Malley, Michelle A. Thu . "Metabolic characterization of anaerobic fungi provides a path forward for bioprocessing of crude lignocellulose". United States. doi:10.1002/bit.26515. https://www.osti.gov/servlets/purl/1485153.
@article{osti_1485153,
title = {Metabolic characterization of anaerobic fungi provides a path forward for bioprocessing of crude lignocellulose},
author = {Henske, John K. and Wilken, St. Elmo and Solomon, Kevin V. and Smallwood, Chuck R. and Shutthanandan, Vaithiyalingam and Evans, James E. and Theodorou, Michael K. and O'Malley, Michelle A.},
abstractNote = {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.},
doi = {10.1002/bit.26515},
journal = {Biotechnology and Bioengineering},
number = 4,
volume = 115,
place = {United States},
year = {2017},
month = {12}
}

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