Metaproteomics reveals enzymatic strategies deployed by anaerobic microbiomes to maintain lignocellulose deconstruction at high solids

Payal Chirania, Evert K. Holwerda, Richard J. Giannone, Xiaoyu Liang, Suresh Poudel, Joseph C. Ellis, Yannick J. Bomble, Robert L. Hettich, Lee R. Lynd

Research output: Contribution to journalArticlepeer-review

22 Scopus citations

Abstract

Economically viable production of cellulosic biofuels requires operation at high solids loadings—on the order of 15 wt%. To this end we characterize Nature’s ability to deconstruct and utilize mid-season switchgrass at increasing solid loadings using an anaerobic methanogenic microbiome. This community exhibits undiminished fractional carbohydrate solubilization at loadings ranging from 30 g/L to 150 g/L. Metaproteomic interrogation reveals marked increases in the abundance of specific carbohydrate-active enzyme classes. Significant enrichment of auxiliary activity family 6 enzymes at higher solids suggests a role for Fenton chemistry. Stress-response proteins accompanying these reactions are similarly upregulated at higher solids, as are β-glucosidases, xylosidases, carbohydrate-debranching, and pectin-acting enzymes—all of which indicate that removal of deconstruction inhibitors is important for observed undiminished solubilization. Our work provides insights into the mechanisms by which natural microbiomes effectively deconstruct and utilize lignocellulose at high solids loadings, informing the future development of defined cultures for efficient bioconversion.

Original languageEnglish
Article number3870
JournalNature Communications
Volume13
Issue number1
DOIs
StatePublished - Dec 2022

Funding

Oak Ridge National Laboratory: Jason Witham (bioinformatics), Dawn M. Klingeman (sample preparation), Steven D. Brown (coordination) and James Elkins (microbial community insights). The Pennsylvania State University: Tom Richard (microbial enrichment insights). Dartmouth College: Xiongjun Shao (assistance in experimental and method design), Sean Murphy, Jules Wheaton, Lion Herfort, Liang Tian and Anela Arifi (assistance with sample analysis and microbiome operation). Funding was provided by the BioEnergy Science Center and the Center for Bioenergy Innovation, both at the U.S. Department of Energy (DOE) Research Center supported by the Office of Biological and Environmental Research in the DOE Office of Science. Oak Ridge National Laboratory: Jason Witham (bioinformatics), Dawn M. Klingeman (sample preparation), Steven D. Brown (coordination) and James Elkins (microbial community insights). The Pennsylvania State University: Tom Richard (microbial enrichment insights). Dartmouth College: Xiongjun Shao (assistance in experimental and method design), Sean Murphy, Jules Wheaton, Lion Herfort, Liang Tian and Anela Arifi (assistance with sample analysis and microbiome operation). Funding was provided by the BioEnergy Science Center and the Center for Bioenergy Innovation, both at the U.S. Department of Energy (DOE) Research Center supported by the Office of Biological and Environmental Research in the DOE Office of Science.

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