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Title: Cultivation and sequencing of rumen microbiome members from the Hungate1000 Collection

Abstract

Productivity of ruminant livestock depends on the rumen microbiota, which ferment indigestible plant polysaccharides into nutrients used for growth. Understanding the functions carried out by the rumen microbiota is important for reducing greenhouse gas production by ruminants and for developing biofuels from lignocellulose. We present 410 cultured bacteria and archaea, together with their reference genomes, representing every cultivated rumen-associated archaeal and bacterial family. We evaluate polysaccharide degradation, short-chain fatty acid production and methanogenesis pathways, and assign specific taxa to functions. A total of 336 organisms were present in available rumen metagenomic data sets, and 134 were present in human gut microbiome data sets. Comparison with the human microbiome revealed rumen-specific enrichment for genes encoding de novo synthesis of vitamin B 12, ongoing evolution by gene loss and potential vertical inheritance of the rumen microbiome based on underrepresentation of markers of environmental stress. We estimate that our Hungate genome resource represents ~75% of the genus-level bacterial and archaeal taxa present in the rumen.

Authors:
ORCiD logo; ORCiD logo; ; ; ; ; ; ; ; ; ORCiD logo; ; ; ; ; ; ; ; ; more »; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ORCiD logo; ; ; ; ; ; ; ORCiD logo; ; ORCiD logo « less
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
Contributing Org.:
Hungate1000 Project Collaborators
OSTI Identifier:
1489281
Alternate Identifier(s):
OSTI ID: 1542309
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Nature Biotechnology
Additional Journal Information:
Journal Volume: 36; Journal Issue: 4; Journal ID: ISSN 1087-0156
Publisher:
Springer Nature
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Seshadri, Rekha, Leahy, Sinead C., Attwood, Graeme T., Teh, Koon Hoong, Lambie, Suzanne C., Cookson, Adrian L., Eloe-Fadrosh, Emiley A., Pavlopoulos, Georgios A., Hadjithomas, Michalis, Varghese, Neha J., Paez-Espino, David, Palevich, Nikola, Janssen, Peter H., Ronimus, Ron S., Noel, Samantha, Soni, Priya, Reilly, Kerri, Atherly, Todd, Ziemer, Cherie, Wright, Andre-Denis, Ishaq, Suzanne, Cotta, Michael, Thompson, Stephanie, Crosley, Katie, McKain, Nest, Wallace, R. John, Flint, Harry J., Martin, Jennifer C., Forster, Robert J., Gruninger, Robert J., McAllister, Tim, Gilbert, Rosalind, Ouwerkerk, Diane, Klieve, Athol, Jassim, Rafat Al, Denman, Stuart, McSweeney, Chris, Rosewarne, Carly, Koike, Satoshi, Kobayashi, Yasuo, Mitsumori, Makoto, Shinkai, Takumi, Cravero, Silvio, Cucchi, María Cerón, Perry, Rechelle, Henderson, Gemma, Creevey, Christopher J., Terrapon, Nicolas, Lapebie, Pascal, Drula, Elodie, Lombard, Vincent, Rubin, Edward, Kyrpides, Nikos C., Henrissat, Bernard, Woyke, Tanja, Ivanova, Natalia N., and Kelly, William J. Cultivation and sequencing of rumen microbiome members from the Hungate1000 Collection. United States: N. p., 2018. Web. doi:10.1038/nbt.4110.
Seshadri, Rekha, Leahy, Sinead C., Attwood, Graeme T., Teh, Koon Hoong, Lambie, Suzanne C., Cookson, Adrian L., Eloe-Fadrosh, Emiley A., Pavlopoulos, Georgios A., Hadjithomas, Michalis, Varghese, Neha J., Paez-Espino, David, Palevich, Nikola, Janssen, Peter H., Ronimus, Ron S., Noel, Samantha, Soni, Priya, Reilly, Kerri, Atherly, Todd, Ziemer, Cherie, Wright, Andre-Denis, Ishaq, Suzanne, Cotta, Michael, Thompson, Stephanie, Crosley, Katie, McKain, Nest, Wallace, R. John, Flint, Harry J., Martin, Jennifer C., Forster, Robert J., Gruninger, Robert J., McAllister, Tim, Gilbert, Rosalind, Ouwerkerk, Diane, Klieve, Athol, Jassim, Rafat Al, Denman, Stuart, McSweeney, Chris, Rosewarne, Carly, Koike, Satoshi, Kobayashi, Yasuo, Mitsumori, Makoto, Shinkai, Takumi, Cravero, Silvio, Cucchi, María Cerón, Perry, Rechelle, Henderson, Gemma, Creevey, Christopher J., Terrapon, Nicolas, Lapebie, Pascal, Drula, Elodie, Lombard, Vincent, Rubin, Edward, Kyrpides, Nikos C., Henrissat, Bernard, Woyke, Tanja, Ivanova, Natalia N., & Kelly, William J. Cultivation and sequencing of rumen microbiome members from the Hungate1000 Collection. United States. doi:10.1038/nbt.4110.
Seshadri, Rekha, Leahy, Sinead C., Attwood, Graeme T., Teh, Koon Hoong, Lambie, Suzanne C., Cookson, Adrian L., Eloe-Fadrosh, Emiley A., Pavlopoulos, Georgios A., Hadjithomas, Michalis, Varghese, Neha J., Paez-Espino, David, Palevich, Nikola, Janssen, Peter H., Ronimus, Ron S., Noel, Samantha, Soni, Priya, Reilly, Kerri, Atherly, Todd, Ziemer, Cherie, Wright, Andre-Denis, Ishaq, Suzanne, Cotta, Michael, Thompson, Stephanie, Crosley, Katie, McKain, Nest, Wallace, R. John, Flint, Harry J., Martin, Jennifer C., Forster, Robert J., Gruninger, Robert J., McAllister, Tim, Gilbert, Rosalind, Ouwerkerk, Diane, Klieve, Athol, Jassim, Rafat Al, Denman, Stuart, McSweeney, Chris, Rosewarne, Carly, Koike, Satoshi, Kobayashi, Yasuo, Mitsumori, Makoto, Shinkai, Takumi, Cravero, Silvio, Cucchi, María Cerón, Perry, Rechelle, Henderson, Gemma, Creevey, Christopher J., Terrapon, Nicolas, Lapebie, Pascal, Drula, Elodie, Lombard, Vincent, Rubin, Edward, Kyrpides, Nikos C., Henrissat, Bernard, Woyke, Tanja, Ivanova, Natalia N., and Kelly, William J. Mon . "Cultivation and sequencing of rumen microbiome members from the Hungate1000 Collection". United States. doi:10.1038/nbt.4110. https://www.osti.gov/servlets/purl/1489281.
@article{osti_1489281,
title = {Cultivation and sequencing of rumen microbiome members from the Hungate1000 Collection},
author = {Seshadri, Rekha and Leahy, Sinead C. and Attwood, Graeme T. and Teh, Koon Hoong and Lambie, Suzanne C. and Cookson, Adrian L. and Eloe-Fadrosh, Emiley A. and Pavlopoulos, Georgios A. and Hadjithomas, Michalis and Varghese, Neha J. and Paez-Espino, David and Palevich, Nikola and Janssen, Peter H. and Ronimus, Ron S. and Noel, Samantha and Soni, Priya and Reilly, Kerri and Atherly, Todd and Ziemer, Cherie and Wright, Andre-Denis and Ishaq, Suzanne and Cotta, Michael and Thompson, Stephanie and Crosley, Katie and McKain, Nest and Wallace, R. John and Flint, Harry J. and Martin, Jennifer C. and Forster, Robert J. and Gruninger, Robert J. and McAllister, Tim and Gilbert, Rosalind and Ouwerkerk, Diane and Klieve, Athol and Jassim, Rafat Al and Denman, Stuart and McSweeney, Chris and Rosewarne, Carly and Koike, Satoshi and Kobayashi, Yasuo and Mitsumori, Makoto and Shinkai, Takumi and Cravero, Silvio and Cucchi, María Cerón and Perry, Rechelle and Henderson, Gemma and Creevey, Christopher J. and Terrapon, Nicolas and Lapebie, Pascal and Drula, Elodie and Lombard, Vincent and Rubin, Edward and Kyrpides, Nikos C. and Henrissat, Bernard and Woyke, Tanja and Ivanova, Natalia N. and Kelly, William J.},
abstractNote = {Productivity of ruminant livestock depends on the rumen microbiota, which ferment indigestible plant polysaccharides into nutrients used for growth. Understanding the functions carried out by the rumen microbiota is important for reducing greenhouse gas production by ruminants and for developing biofuels from lignocellulose. We present 410 cultured bacteria and archaea, together with their reference genomes, representing every cultivated rumen-associated archaeal and bacterial family. We evaluate polysaccharide degradation, short-chain fatty acid production and methanogenesis pathways, and assign specific taxa to functions. A total of 336 organisms were present in available rumen metagenomic data sets, and 134 were present in human gut microbiome data sets. Comparison with the human microbiome revealed rumen-specific enrichment for genes encoding de novo synthesis of vitamin B 12, ongoing evolution by gene loss and potential vertical inheritance of the rumen microbiome based on underrepresentation of markers of environmental stress. We estimate that our Hungate genome resource represents ~75% of the genus-level bacterial and archaeal taxa present in the rumen.},
doi = {10.1038/nbt.4110},
journal = {Nature Biotechnology},
issn = {1087-0156},
number = 4,
volume = 36,
place = {United States},
year = {2018},
month = {3}
}

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    • DOI: 10.1073/pnas.1914939117

    A Targetron-Recombinase System for Large-Scale Genome Engineering of Clostridia
    journal, December 2019


    Islands in the stream: from individual to communal fiber degradation in the rumen ecosystem
    journal, April 2019


    Temporal stability of the rumen microbiota in beef cattle, and response to diet and supplements
    journal, November 2019

    • Snelling, Timothy J.; Auffret, Marc D.; Duthie, Carol-Anne
    • Animal Microbiome, Vol. 1, Issue 1
    • DOI: 10.1186/s42523-019-0018-y

    Comparing the Microbial Community in Four Stomach of Dairy Cattle, Yellow Cattle and Three Yak Herds in Qinghai-Tibetan Plateau
    journal, July 2019


    Islands in the stream: from individual to communal fiber degradation in the rumen ecosystem
    journal, April 2019


    Diverse hydrogen production and consumption pathways influence methane production in ruminants
    journal, June 2019


    Bacterial colonisation of reeds and cottonseed hulls in the rumen of Tarim red deer (Cervus elaphus yarkandensis)
    journal, April 2019


    Exploring the rumen fluid metabolome using liquid chromatography-high-resolution mass spectrometry and Molecular Networking
    journal, December 2018

    • de Almeida, Rafaela Takako Ribeiro; do Prado, Rodolpho Martin; Porto, Carla
    • Scientific Reports, Vol. 8, Issue 1
    • DOI: 10.1038/s41598-018-36196-4

    Occurrence and expression of genes encoding methyl-compound production in rumen bacteria
    journal, November 2019


    Comparing the Microbial Community in Four Stomach of Dairy Cattle, Yellow Cattle and Three Yak Herds in Qinghai-Tibetan Plateau
    journal, July 2019


    Occurrence and expression of genes encoding methyl-compound production in rumen bacteria
    journal, November 2019


    Development and characterization of stable anaerobic thermophilic methanogenic microbiomes fermenting switchgrass at decreasing residence times
    journal, September 2018

    • Liang, Xiaoyu; Whitham, Jason M.; Holwerda, Evert K.
    • Biotechnology for Biofuels, Vol. 11, Issue 1
    • DOI: 10.1186/s13068-018-1238-1

    Characterization of antibiotic resistance genes in the species of the rumen microbiota
    journal, November 2019

    • Sabino, Yasmin Neves Vieira; Santana, Mateus Ferreira; Oyama, Linda Boniface
    • Nature Communications, Vol. 10, Issue 1
    • DOI: 10.1038/s41467-019-13118-0

    Review: The application of omics to rumen microbiota function
    journal, September 2018


    Ruminal microbiome-host crosstalk stimulates the development of the ruminal epithelium in a lamb model
    journal, June 2019


    Temporal stability of the rumen microbiota in beef cattle, and response to diet and supplements
    journal, November 2019

    • Snelling, Timothy J.; Auffret, Marc D.; Duthie, Carol-Anne
    • Animal Microbiome, Vol. 1, Issue 1
    • DOI: 10.1186/s42523-019-0018-y

    Cowpi: A Rumen Microbiome Focussed Version Of The Picrust Functional Inference Software
    text, January 2018


    Insights Into Culturomics of the Rumen Microbiome
    journal, August 2018


    Ruminal microbiome-host crosstalk stimulates the development of the ruminal epithelium in a lamb model
    journal, June 2019


    Metatranscriptomics: an approach for retrieving novel eukaryotic genes from polluted and related environments
    journal, January 2020


    Comparative Genomics Analysis of Lactobacillus mucosae from Different Niches
    journal, January 2020


    Common principles and best practices for engineering microbiomes
    journal, September 2019

    • Lawson, Christopher E.; Harcombe, William R.; Hatzenpichler, Roland
    • Nature Reviews Microbiology, Vol. 17, Issue 12
    • DOI: 10.1038/s41579-019-0255-9

    Diversity and community of methanogens in the large intestine of finishing pigs
    journal, April 2019


    Can rumen bacteria communicate to each other?
    journal, February 2020


    Use of a Fluorescent Analog of Glucose (2-NBDG) To Identify Uncultured Rumen Bacteria That Take Up Glucose
    journal, February 2019

    • Tao, Junyi; McCourt, Courtney; Sultana, Halima
    • Applied and Environmental Microbiology, Vol. 85, Issue 7
    • DOI: 10.1128/aem.03018-18