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Title: 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];  [2]; ORCiD logo [1];  [1];  [3]; ORCiD logo [4]; ORCiD logo [4]; ORCiD logo [4];  [5];  [5];  [6];  [7];  [1]; ORCiD logo [4]; ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [1]
  1. The Ohio State Univ., Columbus, OH (United States)
  2. Norwegian Univ. of Life Sciences, Aas (Norway)
  3. Alaska Dept. of Fish and Game, Palmer, AK (United States)
  4. Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
  5. Univ. of Copenhagen, Copenhagen (Denmark)
  6. Newcastle Univ., Newcastle upon Tyne (United Kingdom)
  7. Univ. of Alaska Anchorage, Anchorage, AK (United States)
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Lawrence Berkeley National Lab. (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. 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., and Wrighton, Kelly C. Wed . "Interspecies cross-feeding orchestrates carbon degradation in the rumen ecosystem". United States. doi: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 = {2018},
month = {10}
}

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