Sequence-based analysis of the genus Ruminococcus resolves its phylogeny and reveals strong host association
Abstract
It has become increasingly clear that the composition of mammalian gut microbial communities is substantially diet driven. These microbiota form intricate mutualisms with their hosts, which have profound implications on overall health. For example, many gut microbes are involved in the conversion of host-ingested dietary polysaccharides into host-usable nutrients. One group of important gut microbial symbionts are bacteria in the genus Ruminococcus. Originally isolated from the bovine rumen, ruminococci have been found in numerous mammalian hosts, including other ruminants, and non-ruminants such as horses, pigs and humans. All ruminococci require fermentable carbohydrates for growth, and their substrate preferences appear to be based on the diet of their particular host. Most ruminococci that have been studied are those capable of degrading cellulose, much less is known about non-cellulolytic non-ruminant-associated species, and even less is known about the environmental distribution of ruminococci as a whole. For this study, we capitalized on the wealth of publicly available 16S rRNA gene sequences, genomes and large-scale microbiota studies to both resolve the phylogenetic placement of described species in the genus Ruminococcus, and further demonstrate that this genus has largely unexplored diversity and a staggering host distribution. We present evidence that ruminococci are predominantly associated withmore »
- Authors:
-
- Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology
- Leibniz Inst. German Collection of Microorganisms and Cell Cultures (DSMZ), Braunschweig (Germany)
- Publication Date:
- Research Org.:
- Univ. of Wisconsin, Madison, WI (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1463886
- Grant/Contract Number:
- SC0008104
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Microbial Genomics
- Additional Journal Information:
- Journal Volume: 2; Journal Issue: 12; Journal ID: ISSN 2057-5858
- Publisher:
- Society for General Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; phylogeny; 16S rRNA; host diet; Ruminococcus; host range; phylogenomics
Citation Formats
La Reau, Alex J., Meier-Kolthoff, Jan P., and Suen, Garret. Sequence-based analysis of the genus Ruminococcus resolves its phylogeny and reveals strong host association. United States: N. p., 2016.
Web. doi:10.1099/mgen.0.000099.
La Reau, Alex J., Meier-Kolthoff, Jan P., & Suen, Garret. Sequence-based analysis of the genus Ruminococcus resolves its phylogeny and reveals strong host association. United States. https://doi.org/10.1099/mgen.0.000099
La Reau, Alex J., Meier-Kolthoff, Jan P., and Suen, Garret. Thu .
"Sequence-based analysis of the genus Ruminococcus resolves its phylogeny and reveals strong host association". United States. https://doi.org/10.1099/mgen.0.000099. https://www.osti.gov/servlets/purl/1463886.
@article{osti_1463886,
title = {Sequence-based analysis of the genus Ruminococcus resolves its phylogeny and reveals strong host association},
author = {La Reau, Alex J. and Meier-Kolthoff, Jan P. and Suen, Garret},
abstractNote = {It has become increasingly clear that the composition of mammalian gut microbial communities is substantially diet driven. These microbiota form intricate mutualisms with their hosts, which have profound implications on overall health. For example, many gut microbes are involved in the conversion of host-ingested dietary polysaccharides into host-usable nutrients. One group of important gut microbial symbionts are bacteria in the genus Ruminococcus. Originally isolated from the bovine rumen, ruminococci have been found in numerous mammalian hosts, including other ruminants, and non-ruminants such as horses, pigs and humans. All ruminococci require fermentable carbohydrates for growth, and their substrate preferences appear to be based on the diet of their particular host. Most ruminococci that have been studied are those capable of degrading cellulose, much less is known about non-cellulolytic non-ruminant-associated species, and even less is known about the environmental distribution of ruminococci as a whole. For this study, we capitalized on the wealth of publicly available 16S rRNA gene sequences, genomes and large-scale microbiota studies to both resolve the phylogenetic placement of described species in the genus Ruminococcus, and further demonstrate that this genus has largely unexplored diversity and a staggering host distribution. We present evidence that ruminococci are predominantly associated with herbivores and omnivores, and our data supports the hypothesis that very few ruminococci are found consistently in non-host-associated environments. This study not only helps to resolve the phylogeny of this important genus, but also provides a framework for understanding its distribution in natural systems.},
doi = {10.1099/mgen.0.000099},
journal = {Microbial Genomics},
number = 12,
volume = 2,
place = {United States},
year = {Thu Dec 01 00:00:00 EST 2016},
month = {Thu Dec 01 00:00:00 EST 2016}
}
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Works referenced in this record:
16S rDNA sequencing of Ruminococcus albus and Ruminococcus flavefaciens: design of a signature probe and its application in adult sheep
journal, July 1999
- Krause, D. O.; Dalrymple, B. P.; Smith, W. J.
- Microbiology, Vol. 145, Issue 7
Ruminococcus champanellensis sp. nov., a cellulose-degrading bacterium from human gut microbiota
journal, February 2011
- Chassard,, C.; Delmas,, E.; Robert,, C.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 62, Issue 1
Taxonomic Note: A Place for DNA-DNA Reassociation and 16S rRNA Sequence Analysis in the Present Species Definition in Bacteriology
journal, October 1994
- Stackebrandt, E.; Goebel, B. M.
- International Journal of Systematic and Evolutionary Microbiology, Vol. 44, Issue 4
Design and validation of 16S rRNA probes to enumerate members of the Clostridium leptum subgroup in human faecal microbiota
journal, July 2005
- Lay, Christophe; Sutren, Malene; Rochet, Violaine
- Environmental Microbiology, Vol. 7, Issue 7
Cellulose Degradation in Anaerobic Environments
journal, October 1995
- Leschine, S. B.
- Annual Review of Microbiology, Vol. 49, Issue 1
Unique Organization of Extracellular Amylases into Amylosomes in the Resistant Starch-Utilizing Human Colonic Firmicutes Bacterium Ruminococcus bromii
journal, September 2015
- Ze, Xiaolei; Ben David, Yonit; Laverde-Gomez, Jenny A.
- mBio, Vol. 6, Issue 5
Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis
journal, February 2008
- Flint, Harry J.; Bayer, Edward A.; Rincon, Marco T.
- Nature Reviews Microbiology, Vol. 6, Issue 2
Cell Surface Enzyme Attachment Is Mediated by Family 37 Carbohydrate-Binding Modules, Unique to Ruminococcus albus
journal, October 2008
- Ezer, A.; Matalon, E.; Jindou, S.
- Journal of Bacteriology, Vol. 190, Issue 24
Enzymatic profiling of cellulosomal enzymes from the human gut bacterium, R uminococcus champanellensis , reveals a fine-tuned system for cohesin-dockerin recognition : Fine-tuned cohesin-dockerin recognition
journal, October 2015
- Moraïs, Sarah; David, Yonit Ben; Bensoussan, Lizi
- Environmental Microbiology, Vol. 18, Issue 2
Worlds within worlds: evolution of the vertebrate gut microbiota
journal, October 2008
- Ley, Ruth E.; Lozupone, Catherine A.; Hamady, Micah
- Nature Reviews Microbiology, Vol. 6, Issue 10
A human gut microbial gene catalogue established by metagenomic sequencing
journal, March 2010
- Qin, Junjie; Li, Ruiqiang; Raes, Jeroen
- Nature, Vol. 464, Issue 7285
Evolution of Mammals and Their Gut Microbes
journal, June 2008
- Ley, R. E.; Hamady, M.; Lozupone, C.
- Science, Vol. 320, Issue 5883
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy
journal, June 2007
- Wang, Q.; Garrity, G. M.; Tiedje, J. M.
- Applied and Environmental Microbiology, Vol. 73, Issue 16
FastME 2.0: A Comprehensive, Accurate, and Fast Distance-Based Phylogeny Inference Program: Table 1.
journal, June 2015
- Lefort, Vincent; Desper, Richard; Gascuel, Olivier
- Molecular Biology and Evolution, Vol. 32, Issue 10
IMG: the integrated microbial genomes database and comparative analysis system
journal, December 2011
- Markowitz, V. M.; Chen, I. -M. A.; Palaniappan, K.
- Nucleic Acids Research, Vol. 40, Issue D1
Genome sequence-based species delimitation with confidence intervals and improved distance functions
journal, January 2013
- Meier-Kolthoff, Jan P.; Auch, Alexander F.; Klenk, Hans-Peter
- BMC Bioinformatics, Vol. 14, Issue 1
Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010
- Hyatt, Doug; Chen, Gwo-Liang; LoCascio, Philip F.
- BMC Bioinformatics, Vol. 11, Issue 1
Whole-genome prokaryotic phylogeny
journal, May 2004
- Henz, S. R.; Huson, D. H.; Auch, A. F.
- Bioinformatics, Vol. 21, Issue 10
MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013
- Katoh, K.; Standley, D. M.
- Molecular Biology and Evolution, Vol. 30, Issue 4
Phylogenetic analysis by 16S ribosomal DNA sequence comparison reveals two unrelated groups of species within the genus
journal, June 1995
- Rainey, F.; Janssen, P.
- FEMS Microbiology Letters, Vol. 129, Issue 1
A single genus in the gut microbiome reflects host preference and specificity
journal, June 2014
- Eren, A. Murat; Sogin, Mitchell L.; Morrison, Hilary G.
- The ISME Journal, Vol. 9, Issue 1
Cellulosome gene cluster analysis for gauging the diversity of the ruminal cellulolytic bacterium Ruminococcus flavefaciens
journal, August 2008
- Jindou, Sadanari; Brulc, Jennifer M.; Levy-Assaraf, Maly
- FEMS Microbiology Letters, Vol. 285, Issue 2
Baleen whales host a unique gut microbiome with similarities to both carnivores and herbivores
journal, September 2015
- Sanders, Jon G.; Beichman, Annabel C.; Roman, Joe
- Nature Communications, Vol. 6, Issue 1
Microorganisms in the Rumen of Cattle fed a Constant Ration
journal, March 1957
- Hungate, R. E.
- Canadian Journal of Microbiology, Vol. 3, Issue 2
MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform
journal, July 2002
- Katoh, K.
- Nucleic Acids Research, Vol. 30, Issue 14
Reclassification of Ruminococcus obeum as Blautia obeum comb. nov.
journal, December 2014
- Lawson, P. A.; Finegold, S. M.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 65, Issue Pt 3
When should a DDH experiment be mandatory in microbial taxonomy?
journal, April 2013
- Meier-Kolthoff, Jan P.; Göker, Markus; Spröer, Cathrin
- Archives of Microbiology, Vol. 195, Issue 6
MRBAYES: Bayesian inference of phylogenetic trees
journal, August 2001
- Huelsenbeck, J. P.; Ronquist, F.
- Bioinformatics, Vol. 17, Issue 8
Relationships between phyllosphere bacterial communities and plant functional traits in a neotropical forest
journal, September 2014
- Kembel, S. W.; O'Connor, T. K.; Arnold, H. K.
- Proceedings of the National Academy of Sciences, Vol. 111, Issue 38
Complete Genome of the Cellulolytic Ruminal Bacterium Ruminococcus albus 7
journal, September 2011
- Suen, G.; Stevenson, D. M.; Bruce, D. C.
- Journal of Bacteriology, Vol. 193, Issue 19
Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities
journal, October 2009
- Schloss, P. D.; Westcott, S. L.; Ryabin, T.
- Applied and Environmental Microbiology, Vol. 75, Issue 23, p. 7537-7541
BLAST+: architecture and applications
journal, January 2009
- Camacho, Christiam; Coulouris, George; Avagyan, Vahram
- BMC Bioinformatics, Vol. 10, Issue 1
Albusin B, a Bacteriocin from the Ruminal Bacterium Ruminococcus albus 7 That Inhibits Growth of Ruminococcus flavefaciens
journal, May 2004
- Chen, J.; Stevenson, D. M.; Weimer, P. J.
- Applied and Environmental Microbiology, Vol. 70, Issue 5
Complete genome of a new Firmicutes species belonging to the dominant human colonic microbiota (‘ Ruminococcus bicirculans ’) reveals two chromosomes and a selective capacity to utilize plant glucans
journal, August 2013
- Wegmann, Udo; Louis, Petra; Goesmann, Alexander
- Environmental Microbiology, Vol. 16, Issue 9
Unique aspects of fiber degradation by the ruminal ethanologen Ruminococcus albus 7 revealed by physiological and transcriptomic analysis
journal, January 2014
- Christopherson, Melissa R.; Dawson, John A.; Stevenson, David M.
- BMC Genomics, Vol. 15, Issue 1
Dominant and diet-responsive groups of bacteria within the human colonic microbiota
journal, August 2010
- Walker, Alan W.; Ince, Jennifer; Duncan, Sylvia H.
- The ISME Journal, Vol. 5, Issue 2
The gut microbiota shapes intestinal immune responses during health and disease
journal, May 2009
- Round, June L.; Mazmanian, Sarkis K.
- Nature Reviews Immunology, Vol. 9, Issue 5
The Mouse Intestinal Bacterial Collection (miBC) provides host-specific insight into cultured diversity and functional potential of the gut microbiota
journal, August 2016
- Lagkouvardos, Ilias; Pukall, Rüdiger; Abt, Birte
- Nature Microbiology, Vol. 1, Issue 10
Symbiotic gut microbes modulate human metabolic phenotypes
journal, February 2008
- Li, M.; Wang, B.; Zhang, M.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 6
Phylogenetic diversity of culturable bacteria from Antarctic sandy intertidal sediments
journal, December 2009
- Yu, Yong; Li, Huirong; Zeng, Yinxin
- Polar Biology, Vol. 33, Issue 6
MrBayes 3: Bayesian phylogenetic inference under mixed models
journal, August 2003
- Ronquist, Fredrik; Huelsenbeck, John P.
- Bioinformatics, Vol. 19, Issue 12, p. 1572-1574
Ruminococcus bromii is a keystone species for the degradation of resistant starch in the human colon
journal, February 2012
- Ze, Xiaolei; Duncan, Sylvia H.; Louis, Petra
- The ISME Journal, Vol. 6, Issue 8
MEGA6: Molecular Evolutionary Genetics Analysis Version 6.0
journal, October 2013
- Tamura, Koichiro; Stecher, Glen; Peterson, Daniel
- Molecular Biology and Evolution, Vol. 30, Issue 12
Rumen Cellulosomics: Divergent Fiber-Degrading Strategies Revealed by Comparative Genome-Wide Analysis of Six Ruminococcal Strains
journal, July 2014
- Dassa, Bareket; Borovok, Ilya; Ruimy-Israeli, Vered
- PLoS ONE, Vol. 9, Issue 7
Highly parallelized inference of large genome-based phylogenies: GENOME-BASED PHYLOGENIES
journal, August 2013
- Meier-Kolthoff, Jan P.; Auch, Alexander F.; Klenk, Hans-Peter
- Concurrency and Computation: Practice and Experience, Vol. 26, Issue 10
Reclassification of Clostridium coccoides, Ruminococcus hansenii, Ruminococcus hydrogenotrophicus, Ruminococcus luti, Ruminococcus productus and Ruminococcus schinkii as Blautia coccoides gen. nov., comb. nov., Blautia hansenii comb. nov., Blautia hydrogenotrophica comb. nov., Blautia luti comb. nov., Blautia producta comb. nov., Blautia schinkii comb. nov. and description of Blautia wexlerae sp. nov., isolated from human faeces
journal, August 2008
- Liu, C.; Finegold, S. M.; Song, Y.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 58, Issue 8
Identification of Ruminococcus flavefaciens as the Predominant Cellulolytic Bacterial Species of the Equine Cecum
journal, August 1999
- Julliand, Veronique; de Vaux, Albane; Millet, Liliane
- Applied and Environmental Microbiology, Vol. 65, Issue 8
Seasonal changes in the ruminal microflora of the high-arctic Svalbard reindeer (Rangifer tarandus platyrhynchus).
journal, January 1985
- Orpin, C. G.; Mathiesen, S. D.; Greenwood, Y.
- Applied and Environmental Microbiology, Vol. 50, Issue 1
Kinetics of Insoluble Cellulose Fermentation by Continuous Cultures of Ruminococcus albus
journal, January 1988
- Pavlostathis, Spyros G.; Miller, Terry L.; Wolin, Meyer J.
- Applied and Environmental Microbiology, Vol. 54, Issue 11
Competition for cellulose among three predominant ruminal cellulolytic bacteria under substrate-excess and substrate-limited conditions.
journal, January 1997
- Shi, Y.; Odt, C. L.; Weimer, P. J.
- Applied and environmental microbiology, Vol. 63, Issue 2
Systematic discovery of pseudomonad genetic factors involved in sensitivity to tailocins
journal, March 2021
- Carim, Sean; Azadeh, Ashley L.; Kazakov, Alexey E.
- The ISME Journal, Vol. 15, Issue 8
Coriander Genomics Database: a genomic, transcriptomic, and metabolic database for coriander
journal, April 2020
- Song, Xiaoming; Nie, Fulei; Chen, Wei
- Horticulture Research, Vol. 7, Issue 1
Species identification, phylogenetic analysis and detection of herbicide-resistant biotypes of Amaranthus based on ALS and ITS
journal, July 2020
- Xu, Han; Pan, Xubin; Wang, Cong
- Scientific Reports, Vol. 10, Issue 1
Works referencing / citing this record:
The Ruminococci: key symbionts of the gut ecosystem
journal, February 2018
- La Reau, Alex J.; Suen, Garret
- Journal of Microbiology, Vol. 56, Issue 3
Hass Avocado Inclusion in a Weight-Loss Diet Supported Weight Loss and Altered Gut Microbiota: A 12-Week Randomized, Parallel-Controlled Trial
journal, June 2019
- Henning, Susanne M.; Yang, Jieping; Woo, Shih Lung
- Current Developments in Nutrition, Vol. 3, Issue 8
Response of Beef Cattle Fecal Microbiota to Grazing on Toxic Tall Fescue
journal, May 2019
- Mote, Ryan S.; Hill, Nicholas S.; Skarlupka, Joseph H.
- Applied and Environmental Microbiology, Vol. 85, Issue 15
The Pacific harbor seal gut microbiota in Mexico: Its relationship with diet and functional inferences
journal, August 2019
- Pacheco-Sandoval, Arlette; Schramm, Yolanda; Heckel, Gisela
- PLOS ONE, Vol. 14, Issue 8
Detection of Increased Plasma Interleukin-6 Levels and Prevalence of Prevotella copri and Bacteroides vulgatus in the Feces of Type 2 Diabetes Patients
journal, September 2017
- Leite, Aline Zazeri; Rodrigues, Nathália de Campos; Gonzaga, Marina Ignácio
- Frontiers in Immunology, Vol. 8
Intestinal Dysbiosis in Autoimmune Diabetes Is Correlated With Poor Glycemic Control and Increased Interleukin-6: A Pilot Study
journal, July 2018
- Higuchi, Bruna Stevanato; Rodrigues, Nathália; Gonzaga, Marina Ignácio
- Frontiers in Immunology, Vol. 9
The Impact of Cholecystectomy on the Gut Microbiota: A Case-Control Study
journal, January 2019
- Yoon, Won; Kim, Han-Na; Park, Eunkyo
- Journal of Clinical Medicine, Vol. 8, Issue 1