Lignin deconstruction by anaerobic fungi

Lankiewicz, Thomas S.; Choudhary, Hemant; Gao, Yu; Amer, Bashar; Lillington, Stephen P.; Leggieri, Patrick A.; Brown, Jennifer L.; Swift, Candice L.; Lipzen, Anna; Na, Hyunsoo; Amirebrahimi, Mojgan; Theodorou, Michael K.; Baidoo, Edward E. K.; Barry, Kerrie; Grigoriev, Igor V.; Timokhin, Vitaliy I.; Gladden, John; Singh, Seema; Mortimer, Jenny C.; Ralph, John; Simmons, Blake A.; Singer, Steven W.; O’Malley, Michelle A.

doi:10.1038/s41564-023-01336-8

Title: Lignin deconstruction by anaerobic fungi

Journal Article · Thu Mar 09 00:00:00 UTC 2023 · Nature Microbiology

DOI: https://doi.org/10.1038/s41564-023-01336-8 · OSTI ID:1960618

; Choudhary, Hemant;

; Amer, Bashar;

; Leggieri, Patrick A.; Brown, Jennifer L.;

; Lipzen, Anna; Na, Hyunsoo; Amirebrahimi, Mojgan; Theodorou, Michael K.; Baidoo, Edward E. K.; Barry, Kerrie;

; Timokhin, Vitaliy I.; Gladden, John; Singh, Seema;

;

Abstract Lignocellulose forms plant cell walls, and its three constituent polymers, cellulose, hemicellulose and lignin, represent the largest renewable organic carbon pool in the terrestrial biosphere. Insights into biological lignocellulose deconstruction inform understandings of global carbon sequestration dynamics and provide inspiration for biotechnologies seeking to address the current climate crisis by producing renewable chemicals from plant biomass. Organisms in diverse environments disassemble lignocellulose, and carbohydrate degradation processes are well defined, but biological lignin deconstruction is described only in aerobic systems. It is currently unclear whether anaerobic lignin deconstruction is impossible because of biochemical constraints or, alternatively, has not yet been measured. We applied whole cell-wall nuclear magnetic resonance, gel-permeation chromatography and transcriptome sequencing to interrogate the apparent paradox that anaerobic fungi (Neocallimastigomycetes), well-documented lignocellulose degradation specialists, are unable to modify lignin. We find that Neocallimastigomycetes anaerobically break chemical bonds in grass and hardwood lignins, and we further associate upregulated gene products with the observed lignocellulose deconstruction. These findings alter perceptions of lignin deconstruction by anaerobes and provide opportunities to advance decarbonization biotechnologies that depend on depolymerizing lignocellulose.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Sandia National Laboratories (SNL-CA), Livermore, CA (United States); USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)

Sponsoring Organization:: National Science Foundation (NSF); US Army Research Office (ARO); USDOE; USDOE National Nuclear Security Administration (NNSA); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; NA0003525; SC0018409; SC0020420

OSTI ID:: 1960618

Report Number(s):: SAND--2023-00851J; PII: 1336

Journal Information:: Nature Microbiology, Journal Name: Nature Microbiology Journal Issue: 4 Vol. 8; ISSN 2058-5276

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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