Interspecies cross-feeding orchestrates carbon degradation in the rumen ecosystem

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.

doi:10.1038/s41564-018-0225-4

Title: Interspecies cross-feeding orchestrates carbon degradation in the rumen ecosystem

Journal Article · 23 October 2018 · Nature Microbiology

DOI: https://doi.org/10.1038/s41564-018-0225-4 · OSTI ID:1491408

Solden, Lindsey M. ^[1]; Naas, Adrian E. ^[2];

^[1]; Daly, Rebecca A. ^[1]; Collins, William B. ^[3];

^[4];

^[4]; Schückel, Julia ^[5]; Jørgensen, Bodil ^[5]; Willats, William ^[6]; Spalinger, Donald E. ^[7]; Firkins, Jeffrey L. ^[1];

^[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)

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 first of its kind 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 (MAGs), 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 MAGs, revealing a genome-resolved three-tiered carbohydrate fueled 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 demonstrate that phage are active controllers of rumen ecosystem function. In conclusion, our findings elucidate the microbial and viral members, as well as their metabolic interdependencies, that support in situ carbon degradation in the rumen ecosystem.

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Research Organization:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States); Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC02-05CH11231; AC05-76RL01830

OSTI ID:: 1491408

Report Number(s):: PNNL-SA-131180

Journal Information:: Nature Microbiology, Journal Name: Nature Microbiology Journal Issue: 11 Vol. 3; ISSN 2058-5276

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Metagenomic Discovery of Biomass-Degrading Genes and Genomes from Cow Rumen Hess, M.; Sczyrba, A.; Egan, R. Science, Vol. 331, Issue 6016 https://doi.org/10.1126/science.1200387	journal	January 2011
Fermentation, Hydrogen, and Sulfur Metabolism in Multiple Uncultivated Bacterial Phyla Wrighton, K. C.; Thomas, B. C.; Sharon, I. Science, Vol. 337, Issue 6102 https://doi.org/10.1126/science.1224041	journal	September 2012
Do Rumen Bacteroidetes Utilize an Alternative Mechanism for Cellulose Degradation? Naas, A. E.; Mackenzie, A. K.; Mravec, J. mBio, Vol. 5, Issue 4 https://doi.org/10.1128/mBio.01401-14	journal	August 2014
MUSCLE: a multiple sequence alignment method with reduced time and space complexity Edgar, Robert C. BMC Bioinformatics, Vol. 5, Issue 1, p. 113 https://doi.org/10.1186/1471-2105-5-113	journal	August 2004
Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5) Aspeborg, Henrik; Coutinho, Pedro M.; Wang, Yang BMC Evolutionary Biology, Vol. 12, Issue 1 https://doi.org/10.1186/1471-2148-12-186	journal	January 2012
Metagenomics of rumen bacteriophage from thirteen lactating dairy cattle Ross, Elizabeth M.; Petrovski, Steve; Moate, Peter J. BMC Microbiology, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2180-13-242	journal	January 2013
The rumen microbial metagenome associated with high methane production in cattle Wallace, R. John; Rooke, John A.; McKain, Nest BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-2032-0	journal	October 2015
Fine-scale population structure and evidence for local adaptation in Australian giant black tiger shrimp (Penaeus monodon) using SNP analysis Vu, Nga T. T.; Zenger, Kyall R.; Guppy, Jarrod L. BMC Genomics, Vol. 21, Issue 1 https://doi.org/10.1186/s12864-020-07084-x	journal	September 2020
Ecology of bacteria in the human gastrointestinal tract—identification of keystone and foundation taxa Trosvik, Pål; de Muinck, Eric Jacques Microbiome, Vol. 3, Issue 1 https://doi.org/10.1186/s40168-015-0107-4	journal	October 2015
Dietary energy drives the dynamic response of bovine rumen viral communities Anderson, Christopher L.; Sullivan, Matthew B.; Fernando, Samodha C. Microbiome, Vol. 5, Issue 1 https://doi.org/10.1186/s40168-017-0374-3	journal	November 2017
Effects of Diet on Resource Utilization by a Model Human Gut Microbiota Containing Bacteroides cellulosilyticus WH2, a Symbiont with an Extensive Glycobiome McNulty, Nathan P.; Wu, Meng; Erickson, Alison R. PLoS Biology, Vol. 11, Issue 8 https://doi.org/10.1371/journal.pbio.1001637	journal	August 2013
Evolution, substrate specificity and subfamily classification of glycoside hydrolase family 5 (GH5) Aspeborg, Henrik; Coutinho, Pedro M.; Wang, Yang BioMed Central https://doi.org/10.14288/1.0074600	text	January 2012
Revisions of Rump Fat and Body Scoring Indices for Deer, Elk, and Moose Cook, Rachel C.; Cook, John G.; Stephenson, Thomas R. Journal of Wildlife Management, Vol. 74, Issue 4 https://doi.org/10.2193/2009-031	journal	May 2010
Toward Understanding Phage:Host Interactions in the Rumen; Complete Genome Sequences of Lytic Phages Infecting Rumen Bacteria Gilbert, Rosalind A.; Kelly, William J.; Altermann, Eric Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02340	journal	December 2017
Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range Henderson, Gemma; Cox, Faith; Ganesh, Siva ETH Zurich https://doi.org/10.3929/ethz-b-000164426	text	January 2015
Data from: Effects of diet on resource utilization by a model human gut microbiota containing Bacteroides cellulosilyticus WH2, a symbiont with an extensive glycobiome McNulty, Nathan P.; Meng, Wu; Erickson, Alison R. Dryad https://doi.org/10.5061/dryad.7fj1k	dataset	January 2013
RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies Stamatakis, A. Karlsruhe https://doi.org/10.5445/ir/1000045818	text	January 2014
Ecology of bacteria in the human gastrointestinal tract—identification of keystone and foundation taxa Trosvik, Pål; Muinck, Eric Figshare https://doi.org/10.6084/m9.figshare.c.3623996.v1	collection	January 2015
Dietary energy drives the dynamic response of bovine rumen viral communities Anderson, Christopher; Sullivan, Matthew; Fernando, Samodha Figshare https://doi.org/10.6084/m9.figshare.c.3940126	collection	January 2017
MetaBAT, an efficient tool for accurately reconstructing single genomes from complex microbial communities Kang, Dongwan D.; Froula, Jeff; Egan, Rob PeerJ, Vol. 3 https://doi.org/10.7717/peerj.1165	journal	January 2015
VirSorter: mining viral signal from microbial genomic data Roux, Simon; Enault, Francois; Hurwitz, Bonnie L. PeerJ, Vol. 3 https://doi.org/10.7717/peerj.985	journal	January 2015

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Additional file 6 of An integrated gene catalog and over 10,000 metagenome-assembled genomes from the gastrointestinal microbiome of ruminants Xie, Fei; Jin, Wei; Si, Huazhe figshare https://doi.org/10.6084/m9.figshare.14775438	dataset	January 2021
Additional file 7 of An integrated gene catalog and over 10,000 metagenome-assembled genomes from the gastrointestinal microbiome of ruminants Xie, Fei; Jin, Wei; Si, Huazhe figshare https://doi.org/10.6084/m9.figshare.14775441	dataset	January 2021
Additional file 8 of An integrated gene catalog and over 10,000 metagenome-assembled genomes from the gastrointestinal microbiome of ruminants Xie, Fei; Jin, Wei; Si, Huazhe figshare https://doi.org/10.6084/m9.figshare.14775444	dataset	January 2021
Additional file 2 of Metagenomic insights into the microbe-mediated B and K2 vitamin biosynthesis in the gastrointestinal microbiome of ruminants Jiang, Qian; Lin, Limei; Xie, Fei figshare https://doi.org/10.6084/m9.figshare.20356416.v1	dataset	January 2022
Additional file 3 of Metagenomic insights into the microbe-mediated B and K2 vitamin biosynthesis in the gastrointestinal microbiome of ruminants Jiang, Qian; Lin, Limei; Xie, Fei figshare https://doi.org/10.6084/m9.figshare.20356419	dataset	January 2022
Additional file 4 of Metagenomic insights into the microbe-mediated B and K2 vitamin biosynthesis in the gastrointestinal microbiome of ruminants Jiang, Qian; Lin, Limei; Xie, Fei figshare https://doi.org/10.6084/m9.figshare.20356422.v1	dataset	January 2022
Additional file 5 of Metagenomic insights into the microbe-mediated B and K2 vitamin biosynthesis in the gastrointestinal microbiome of ruminants Jiang, Qian; Lin, Limei; Xie, Fei figshare https://doi.org/10.6084/m9.figshare.20356425.v1	dataset	January 2022
Additional file 1 of A compendium of ruminant gastrointestinal phage genomes revealed a higher proportion of lytic phages than in any other environments Wu, Yingjian; Gao, Na; Sun, Chuqing figshare https://doi.org/10.6084/m9.figshare.25547037	dataset	January 2024
Diverse hydrogen production and consumption pathways influence methane production in ruminants Greening, Chris; Geier, Renae; Wang, Cecilia The ISME Journal, Vol. 13, Issue 10 https://doi.org/10.1038/s41396-019-0464-2	journal	June 2019
Proteome specialization of anaerobic fungi during ruminal degradation of recalcitrant plant fiber Hagen, Live H.; Brooke, Charles G.; Shaw, Claire A. The ISME Journal, Vol. 15, Issue 2 https://doi.org/10.1038/s41396-020-00769-x	journal	September 2020
Microbiota-directed fibre activates both targeted and secondary metabolic shifts in the distal gut Michalak, Leszek; Gaby, John Christian; Lagos, Leidy Nature Communications, Vol. 11, Issue 1 https://doi.org/10.1038/s41467-020-19585-0	journal	November 2020
Common principles and best practices for engineering microbiomes Lawson, Christopher E.; Harcombe, William R.; Hatzenpichler, Roland Nature Reviews Microbiology, Vol. 17, Issue 12 https://doi.org/10.1038/s41579-019-0255-9	journal	September 2019
Compendium of 4,941 rumen metagenome-assembled genomes for rumen microbiome biology and enzyme discovery Stewart, Robert D.; Auffret, Marc D.; Warr, Amanda Nature Biotechnology, Vol. 37, Issue 8 https://doi.org/10.1038/s41587-019-0202-3	journal	August 2019
To Dereplicate or Not To Dereplicate? Evans, Jacob T.; Denef, Vincent J. mSphere, Vol. 5, Issue 3 https://doi.org/10.1128/msphere.00971-19	journal	June 2020
Assignment of virus and antimicrobial resistance genes to microbial hosts in a complex microbial community by combined long-read assembly and proximity ligation Bickhart, Derek M.; Watson, Mick; Koren, Sergey Genome Biology, Vol. 20, Issue 1 https://doi.org/10.1186/s13059-019-1760-x	journal	August 2019
Impact of phages on soil bacterial communities and nitrogen availability under different assembly scenarios Braga, Lucas P. P.; Spor, Aymé; Kot, Witold Microbiome, Vol. 8, Issue 1 https://doi.org/10.1186/s40168-020-00822-z	journal	April 2020
Evidence for a multi-level trophic organization of the human gut microbiome Wang, Tong; Goyal, Akshit; Dubinkina, Veronika PLOS Computational Biology, Vol. 15, Issue 12 https://doi.org/10.1371/journal.pcbi.1007524	journal	December 2019
Metabolic Overlap in Environmentally Diverse Microbial Communities Hester, Eric R.; Jetten, Mike S. M.; Welte, Cornelia U. Frontiers in Genetics, Vol. 10 https://doi.org/10.3389/fgene.2019.00989	journal	October 2019

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