Interspecies cross-feeding orchestrates carbon degradation in the rumen ecosystem
Abstract
Because of their agricultural value, there is a great body of research dedicated to understanding the microorganisms responsible for rumen carbon degradation. However, we lack a holistic view of the microbial food web responsible for carbon processing in this ecosystem. Here, we sampled rumen-fistulated moose, allowing access to rumen microbial communities actively degrading woody plant biomass in real time. We resolved 1,193 viral contigs and 77 unique, near-complete microbial metagenome-assembled genomes, many of which lacked previous metabolic insights. Plant-derived metabolites were measured with NMR and carbohydrate microarrays to quantify the carbon nutrient landscape. Network analyses directly linked measured metabolites to expressed proteins from these unique metagenome-assembled genomes, revealing a genome-resolved three-tiered carbohydrate-fuelled trophic system. This provided a glimpse into microbial specialization into functional guilds defined by specific metabolites. To validate our proteomic inferences, the catalytic activity of a polysaccharide utilization locus from a highly connected metabolic hub genome was confirmed using heterologous gene expression. Viral detected proteins and linkages to microbial hosts demonstrated that phage are active controllers of rumen ecosystem function. Our findings elucidate the microbial and viral members, as well as their metabolic interdependencies, that support in situ carbon degradation in the rumen ecosystem.
- Authors:
-
[1];
[4];
[4];
[4];
[4];
[1];
[2];
[1]
- The Ohio State Univ., Columbus, OH (United States)
- Norwegian Univ. of Life Sciences, Aas (Norway)
- Alaska Dept. of Fish and Game, Palmer, AK (United States)
- Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
- Univ. of Copenhagen, Copenhagen (Denmark)
- Newcastle Univ., Newcastle upon Tyne (United Kingdom)
- Univ. of Alaska Anchorage, Anchorage, AK (United States)
- Publication Date:
- Research Org.:
- Pacific Northwest National Laboratory (PNNL), Richland, WA (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1491408
- Alternate Identifier(s):
- OSTI ID: 1580338
- Report Number(s):
- PNNL-SA-131180
Journal ID: ISSN 2058-5276
- Grant/Contract Number:
- AC05-76RL01830; AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Nature Microbiology
- Additional Journal Information:
- Journal Volume: 3; Journal Issue: 11; Journal ID: ISSN 2058-5276
- Publisher:
- Nature Publishing Group
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES
Citation Formats
Solden, Lindsey M., Naas, Adrian E., Roux, Simon, Daly, Rebecca A., Collins, William B., Nicora, Carrie D., Purvine, Sam O., Hoyt, David W., Schückel, Julia, Jørgensen, Bodil, Willats, William, Spalinger, Donald E., Firkins, Jeffrey L., Lipton, Mary S., Sullivan, Matthew B., Pope, Phillip B., and Wrighton, Kelly C. Interspecies cross-feeding orchestrates carbon degradation in the rumen ecosystem. United States: N. p., 2018.
Web. doi:10.1038/s41564-018-0225-4.
Solden, Lindsey M., Naas, Adrian E., Roux, Simon, Daly, Rebecca A., Collins, William B., Nicora, Carrie D., Purvine, Sam O., Hoyt, David W., Schückel, Julia, Jørgensen, Bodil, Willats, William, Spalinger, Donald E., Firkins, Jeffrey L., Lipton, Mary S., Sullivan, Matthew B., Pope, Phillip B., & Wrighton, Kelly C. Interspecies cross-feeding orchestrates carbon degradation in the rumen ecosystem. United States. https://doi.org/10.1038/s41564-018-0225-4
Solden, Lindsey M., Naas, Adrian E., Roux, Simon, Daly, Rebecca A., Collins, William B., Nicora, Carrie D., Purvine, Sam O., Hoyt, David W., Schückel, Julia, Jørgensen, Bodil, Willats, William, Spalinger, Donald E., Firkins, Jeffrey L., Lipton, Mary S., Sullivan, Matthew B., Pope, Phillip B., and Wrighton, Kelly C. Wed .
"Interspecies cross-feeding orchestrates carbon degradation in the rumen ecosystem". United States. https://doi.org/10.1038/s41564-018-0225-4. https://www.osti.gov/servlets/purl/1491408.
@article{osti_1491408,
title = {Interspecies cross-feeding orchestrates carbon degradation in the rumen ecosystem},
author = {Solden, Lindsey M. and Naas, Adrian E. and Roux, Simon and Daly, Rebecca A. and Collins, William B. and Nicora, Carrie D. and Purvine, Sam O. and Hoyt, David W. and Schückel, Julia and Jørgensen, Bodil and Willats, William and Spalinger, Donald E. and Firkins, Jeffrey L. and Lipton, Mary S. and Sullivan, Matthew B. and Pope, Phillip B. and Wrighton, Kelly C.},
abstractNote = {Because of their agricultural value, there is a great body of research dedicated to understanding the microorganisms responsible for rumen carbon degradation. However, we lack a holistic view of the microbial food web responsible for carbon processing in this ecosystem. Here, we sampled rumen-fistulated moose, allowing access to rumen microbial communities actively degrading woody plant biomass in real time. We resolved 1,193 viral contigs and 77 unique, near-complete microbial metagenome-assembled genomes, many of which lacked previous metabolic insights. Plant-derived metabolites were measured with NMR and carbohydrate microarrays to quantify the carbon nutrient landscape. Network analyses directly linked measured metabolites to expressed proteins from these unique metagenome-assembled genomes, revealing a genome-resolved three-tiered carbohydrate-fuelled trophic system. This provided a glimpse into microbial specialization into functional guilds defined by specific metabolites. To validate our proteomic inferences, the catalytic activity of a polysaccharide utilization locus from a highly connected metabolic hub genome was confirmed using heterologous gene expression. Viral detected proteins and linkages to microbial hosts demonstrated that phage are active controllers of rumen ecosystem function. Our findings elucidate the microbial and viral members, as well as their metabolic interdependencies, that support in situ carbon degradation in the rumen ecosystem.},
doi = {10.1038/s41564-018-0225-4},
journal = {Nature Microbiology},
number = 11,
volume = 3,
place = {United States},
year = {Wed Oct 24 00:00:00 EDT 2018},
month = {Wed Oct 24 00:00:00 EDT 2018}
}
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Search and clustering orders of magnitude faster than BLAST
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