Proteome specialization of anaerobic fungi during ruminal degradation of recalcitrant plant fiber
Abstract
The rumen harbors a complex microbial mixture of archaea, bacteria, protozoa, and fungi that efficiently breakdown plant biomass and its complex dietary carbohydrates into soluble sugars that can be fermented and subsequently converted into metabolites and nutrients utilized by the host animal. While rumen bacterial populations have been well documented, only a fraction of the rumen eukarya are taxonomically and functionally characterized, despite the recognition that they contribute to the cellulolytic phenotype of the rumen microbiota. To investigate how anaerobic fungi actively engage in digestion of recalcitrant fiber that is resistant to degradation, we resolved genome-centric metaproteome and metatranscriptome datasets generated from switchgrass samples incubated for 48 h in nylon bags within the rumen of cannulated dairy cows. Across a gene catalog covering anaerobic rumen bacteria, fungi and viruses, a significant portion of the detected proteins originated from fungal populations. Intriguingly, the carbohydrate-active enzyme (CAZyme) profile suggested a domain-specific functional specialization, with bacterial populations primarily engaged in the degradation of hemicelluloses, whereas fungi were inferred to target recalcitrant cellulose structures via the detection of a number of endo- and exo-acting enzymes belonging to the glycoside hydrolase (GH) family 5, 6, 8, and 48. Notably, members of the GH48 family weremore »
- Authors:
-
[1];
[1];
[5];
[6];
[8];
[9];
[10];
[6];
[5];
[1];
[2]
- Norwegian Univ. of Life Sciences, Aas (Norway)
- Univ. of California, Davis, CA (United States)
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Washington State Univ., Richland, WA (United States)
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
- Université Aix-Marseille (France)
- Université Aix-Marseille (France); King Abdulaziz Univ., Jeddah (Saudi Arabia)
- Univ. of California, Santa Barbara, CA (United States)
- Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
- Univ. of Illinois at Urbana-Champaign, IL (United States)
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); Research Council of Norway; European Research Council (ERC)
- OSTI Identifier:
- 1756378
- Grant/Contract Number:
- AC02-05CH11231; 336355-MicroDE
- Resource Type:
- Accepted Manuscript
- Journal Name:
- The ISME Journal
- Additional Journal Information:
- Journal Volume: 15; Journal ID: ISSN 1751-7362
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Fungi; Microbial ecology; Microbiome
Citation Formats
Hagen, Live H., Brooke, Charles G., Shaw, Claire A., Norbeck, Angela D., Piao, Hailan, Arntzen, Magnus Ø., Olson, Heather M., Copeland, Alex, Isern, Nancy, Shukla, Anil, Roux, Simon, Lombard, Vincent, Henrissat, Bernard, O’Malley, Michelle A., Grigoriev, Igor V., Tringe, Susannah G., Mackie, Roderick I., Pasa-Tolic, Ljiljana, Pope, Phillip B., and Hess, Matthias. Proteome specialization of anaerobic fungi during ruminal degradation of recalcitrant plant fiber. United States: N. p., 2020.
Web. doi:10.1038/s41396-020-00769-x.
Hagen, Live H., Brooke, Charles G., Shaw, Claire A., Norbeck, Angela D., Piao, Hailan, Arntzen, Magnus Ø., Olson, Heather M., Copeland, Alex, Isern, Nancy, Shukla, Anil, Roux, Simon, Lombard, Vincent, Henrissat, Bernard, O’Malley, Michelle A., Grigoriev, Igor V., Tringe, Susannah G., Mackie, Roderick I., Pasa-Tolic, Ljiljana, Pope, Phillip B., & Hess, Matthias. Proteome specialization of anaerobic fungi during ruminal degradation of recalcitrant plant fiber. United States. https://doi.org/10.1038/s41396-020-00769-x
Hagen, Live H., Brooke, Charles G., Shaw, Claire A., Norbeck, Angela D., Piao, Hailan, Arntzen, Magnus Ø., Olson, Heather M., Copeland, Alex, Isern, Nancy, Shukla, Anil, Roux, Simon, Lombard, Vincent, Henrissat, Bernard, O’Malley, Michelle A., Grigoriev, Igor V., Tringe, Susannah G., Mackie, Roderick I., Pasa-Tolic, Ljiljana, Pope, Phillip B., and Hess, Matthias. Mon .
"Proteome specialization of anaerobic fungi during ruminal degradation of recalcitrant plant fiber". United States. https://doi.org/10.1038/s41396-020-00769-x. https://www.osti.gov/servlets/purl/1756378.
@article{osti_1756378,
title = {Proteome specialization of anaerobic fungi during ruminal degradation of recalcitrant plant fiber},
author = {Hagen, Live H. and Brooke, Charles G. and Shaw, Claire A. and Norbeck, Angela D. and Piao, Hailan and Arntzen, Magnus Ø. and Olson, Heather M. and Copeland, Alex and Isern, Nancy and Shukla, Anil and Roux, Simon and Lombard, Vincent and Henrissat, Bernard and O’Malley, Michelle A. and Grigoriev, Igor V. and Tringe, Susannah G. and Mackie, Roderick I. and Pasa-Tolic, Ljiljana and Pope, Phillip B. and Hess, Matthias},
abstractNote = {The rumen harbors a complex microbial mixture of archaea, bacteria, protozoa, and fungi that efficiently breakdown plant biomass and its complex dietary carbohydrates into soluble sugars that can be fermented and subsequently converted into metabolites and nutrients utilized by the host animal. While rumen bacterial populations have been well documented, only a fraction of the rumen eukarya are taxonomically and functionally characterized, despite the recognition that they contribute to the cellulolytic phenotype of the rumen microbiota. To investigate how anaerobic fungi actively engage in digestion of recalcitrant fiber that is resistant to degradation, we resolved genome-centric metaproteome and metatranscriptome datasets generated from switchgrass samples incubated for 48 h in nylon bags within the rumen of cannulated dairy cows. Across a gene catalog covering anaerobic rumen bacteria, fungi and viruses, a significant portion of the detected proteins originated from fungal populations. Intriguingly, the carbohydrate-active enzyme (CAZyme) profile suggested a domain-specific functional specialization, with bacterial populations primarily engaged in the degradation of hemicelluloses, whereas fungi were inferred to target recalcitrant cellulose structures via the detection of a number of endo- and exo-acting enzymes belonging to the glycoside hydrolase (GH) family 5, 6, 8, and 48. Notably, members of the GH48 family were amongst the highest abundant CAZymes and detected representatives from this family also included dockerin domains that are associated with fungal cellulosomes. A eukaryote-selected metatranscriptome further reinforced the contribution of uncultured fungi in the ruminal degradation of recalcitrant fibers. These findings elucidate the intricate networks of in situ recalcitrant fiber deconstruction, and importantly, suggest that the anaerobic rumen fungi contribute a specific set of CAZymes that complement the enzyme repertoire provided by the specialized plant cell wall degrading rumen bacteria.},
doi = {10.1038/s41396-020-00769-x},
journal = {The ISME Journal},
number = ,
volume = 15,
place = {United States},
year = {Mon Sep 14 00:00:00 EDT 2020},
month = {Mon Sep 14 00:00:00 EDT 2020}
}
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