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Title: Comparative Genomics of Rumen Butyrivibrio spp. Uncovers a Continuum of Polysaccharide-Degrading Capabilities

Abstract

Plant polysaccharide breakdown by microbes in the rumen is fundamental to digestion in ruminant livestock. Bacterial species belonging to the rumen genera Butyrivibrio and Pseudobutyrivibrio are important degraders and utilizers of lignocellulosic plant material. These bacteria degrade polysaccharides and ferment the released monosaccharides to yield short-chain fatty acids that are used by the ruminant for growth and the production of meat, milk, and fiber products. Although rumen Butyrivibrio and Pseudobutyrivibrio species are regarded as common rumen inhabitants, their polysaccharide-degrading and carbohydrate-utilizing enzymes are not well understood. In this study, we analyzed the genomes of 40 Butyrivibrio and 6 Pseudobutyrivibrio strains isolated from the plant-adherent fraction of New Zealand dairy cows to explore the polysaccharide-degrading potential of these important rumen bacteria. Comparative genome analyses combined with phylogenetic analysis of their 16S rRNA genes and short-chain fatty acid production patterns provide insight into the genomic diversity and physiology of these bacteria and divide Butyrivibrio into 3 species clusters. Rumen Butyrivibrio bacteria were found to encode a large and diverse spectrum of degradative carbohydrate-active enzymes (CAZymes) and binding proteins. In total, 4,421 glycoside hydrolases (GHs), 1,283 carbohydrate esterases (CEs), 110 polysaccharide lyases (PLs), 3,605 glycosyltransferases (GTs), and 1,706 carbohydrate-binding protein modules (CBM) withmore » predicted activities involved in the depolymerization and transport of the insoluble plant polysaccharides were identified. Butyrivibrio genomes had similar patterns of CAZyme families but varied greatly in the number of genes within each category in the Carbohydrate-Active Enzymes database (CAZy), suggesting some level of functional redundancy. These results suggest that rumen Butyrivibrio species occupy similar niches but apply different degradation strategies to be able to coexist in the rumen.« less

Authors:
 [1];  [2];  [1];  [3];  [1]; ORCiD logo [4];  [1]
  1. AgResearch Limited, Palmerston North (New Zealand)
  2. Donvis Limited, Palmerston North (New Zealand)
  3. Agriculture and Food (CSIRO), St. Lucia, QLD (Australia)
  4. Massey Univ., Palmerston North (New Zealand)
Publication Date:
Research Org.:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). National Energy Research Scientific Computing Center (NERSC); USDOE Joint Genome Institute (JGI), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC); New Zealand Ministry of Business, Innovation and Employment New Economy Research Fund; New Zealand Government
OSTI Identifier:
1626066
Grant/Contract Number:  
AC02-05CH11231; C10X0803
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Applied and Environmental Microbiology
Additional Journal Information:
Journal Volume: 86; Journal Issue: 1; Journal ID: ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
biotechnology & applied microbiology; microbiology; rumen; bacteria; polysaccharide; butyrivibrio; pseudobutyrivibrio; genome; cazy; enolase

Citation Formats

Palevich, Nikola, Kelly, William J., Leahy, Sinead C., Denman, Stuart, Altermann, Eric, Rakonjac, Jasna, and Attwood, Graeme T. Comparative Genomics of Rumen Butyrivibrio spp. Uncovers a Continuum of Polysaccharide-Degrading Capabilities. United States: N. p., 2019. Web. doi:10.1128/aem.01993-19.
Palevich, Nikola, Kelly, William J., Leahy, Sinead C., Denman, Stuart, Altermann, Eric, Rakonjac, Jasna, & Attwood, Graeme T. Comparative Genomics of Rumen Butyrivibrio spp. Uncovers a Continuum of Polysaccharide-Degrading Capabilities. United States. doi:10.1128/aem.01993-19.
Palevich, Nikola, Kelly, William J., Leahy, Sinead C., Denman, Stuart, Altermann, Eric, Rakonjac, Jasna, and Attwood, Graeme T. Fri . "Comparative Genomics of Rumen Butyrivibrio spp. Uncovers a Continuum of Polysaccharide-Degrading Capabilities". United States. doi:10.1128/aem.01993-19. https://www.osti.gov/servlets/purl/1626066.
@article{osti_1626066,
title = {Comparative Genomics of Rumen Butyrivibrio spp. Uncovers a Continuum of Polysaccharide-Degrading Capabilities},
author = {Palevich, Nikola and Kelly, William J. and Leahy, Sinead C. and Denman, Stuart and Altermann, Eric and Rakonjac, Jasna and Attwood, Graeme T.},
abstractNote = {Plant polysaccharide breakdown by microbes in the rumen is fundamental to digestion in ruminant livestock. Bacterial species belonging to the rumen genera Butyrivibrio and Pseudobutyrivibrio are important degraders and utilizers of lignocellulosic plant material. These bacteria degrade polysaccharides and ferment the released monosaccharides to yield short-chain fatty acids that are used by the ruminant for growth and the production of meat, milk, and fiber products. Although rumen Butyrivibrio and Pseudobutyrivibrio species are regarded as common rumen inhabitants, their polysaccharide-degrading and carbohydrate-utilizing enzymes are not well understood. In this study, we analyzed the genomes of 40 Butyrivibrio and 6 Pseudobutyrivibrio strains isolated from the plant-adherent fraction of New Zealand dairy cows to explore the polysaccharide-degrading potential of these important rumen bacteria. Comparative genome analyses combined with phylogenetic analysis of their 16S rRNA genes and short-chain fatty acid production patterns provide insight into the genomic diversity and physiology of these bacteria and divide Butyrivibrio into 3 species clusters. Rumen Butyrivibrio bacteria were found to encode a large and diverse spectrum of degradative carbohydrate-active enzymes (CAZymes) and binding proteins. In total, 4,421 glycoside hydrolases (GHs), 1,283 carbohydrate esterases (CEs), 110 polysaccharide lyases (PLs), 3,605 glycosyltransferases (GTs), and 1,706 carbohydrate-binding protein modules (CBM) with predicted activities involved in the depolymerization and transport of the insoluble plant polysaccharides were identified. Butyrivibrio genomes had similar patterns of CAZyme families but varied greatly in the number of genes within each category in the Carbohydrate-Active Enzymes database (CAZy), suggesting some level of functional redundancy. These results suggest that rumen Butyrivibrio species occupy similar niches but apply different degradation strategies to be able to coexist in the rumen.},
doi = {10.1128/aem.01993-19},
journal = {Applied and Environmental Microbiology},
issn = {0099-2240},
number = 1,
volume = 86,
place = {United States},
year = {2019},
month = {12}
}

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Works referenced in this record:

Food Security: The Challenge of Feeding 9 Billion People
journal, January 2010


Agriculture: Steps to sustainable livestock
journal, March 2014

  • Eisler, Mark C.; Lee, Michael R. F.; Tarlton, John F.
  • Nature, Vol. 507, Issue 7490
  • DOI: 10.1038/507032a

Metagenomic Discovery of Biomass-Degrading Genes and Genomes from Cow Rumen
journal, January 2011


Phylogenetic analysis of fiber-associated rumen bacterial community and PCR detection of uncultured bacteria
journal, December 2003


Microbial attachment and feed digestion in the rumen
journal, November 1994

  • McAllister, T. A.; Bae, H. D.; Jones, G. A.
  • Journal of Animal Science, Vol. 72, Issue 11
  • DOI: 10.2527/1994.72113004x

Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range
journal, October 2015

  • Henderson, Gemma; Cox, Faith; Ganesh, Siva
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep14567

Cultivation and sequencing of rumen microbiome members from the Hungate1000 Collection
journal, March 2018

  • Seshadri, Rekha; Leahy, Sinead C.; Attwood, Graeme T.
  • Nature Biotechnology, Vol. 36, Issue 4
  • DOI: 10.1038/nbt.4110

Pseudobutyrivibrio ruminis gen. nov., sp. nov., a Butyrate-Producing Bacterium from the Rumen That Closely Resembles Butyrivibrio fibrisolvens in Phenotype
journal, April 1996

  • Van Gylswyk, N. O.; Hippe, H.; Rainey, F. A.
  • International Journal of Systematic Bacteriology, Vol. 46, Issue 2
  • DOI: 10.1099/00207713-46-2-559

Alternative schemes of butyrate production in Butyrivibrio fibrisolvens and their relationship to acetate utilization, lactate production, and phylogeny
journal, April 1999

  • Diez-Gonzalez, Francisco; Bond, Daniel R.; Jennings, Elizabeth
  • Archives of Microbiology, Vol. 171, Issue 5
  • DOI: 10.1007/s002030050717

Quantification of ruminal Clostridium proteoclasticum by real-time PCR using a molecular beacon approach
journal, October 2007


Isolation and characteristics of a wheatbran-degrading Butyrivibrio from human faeces
journal, April 1995


Digestion of cell-wall monosaccharides of ryegrass and alfalfa hays by the ruminal bacteria Fibrobacter succinogenes and Butyrivibrio fibrisolvens
journal, August 1993

  • Miron, Joshua; Ben-Ghedalia, Daniel
  • Canadian Journal of Microbiology, Vol. 39, Issue 8
  • DOI: 10.1139/m93-115

Induction of xylan-degrading enzymes inButyrivibrio fibrisolvens
journal, November 1992

  • Williams, Alan G.; Withers, Susan E.
  • Current Microbiology, Vol. 25, Issue 5
  • DOI: 10.1007/BF01575865

Further Studies on the Isolation of Proteolytic Bacteria from the Sheep Rumen
journal, September 1962


Metabolism of conjugated linoleic acids and 18 : 1 fatty acids by ruminal bacteria: products and mechanisms
journal, November 2009


Metabolism of polyunsaturated fatty acids and their toxicity to the microflora of the rumen
journal, October 2006

  • Maia, Margarida R. G.; Chaudhary, Lal C.; Figueres, Lauren
  • Antonie van Leeuwenhoek, Vol. 91, Issue 4
  • DOI: 10.1007/s10482-006-9118-2

Reclassification of Clostridium proteoclasticum as Butyrivibrio proteoclasticus comb. nov., a butyrate-producing ruminal bacterium
journal, September 2008

  • Moon, C. D.; Pacheco, D. M.; Kelly, W. J.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 58, Issue 9
  • DOI: 10.1099/ijs.0.65845-0

Phylogenetic Analysis of Butyrivibrio Strains Reveals Three Distinct Groups of Species within the Clostridium Subphylum of the Gram-Positive Bacteria
journal, January 1996

  • Willems, A.; Amat-Marco, M.; Collins, M. D.
  • International Journal of Systematic Bacteriology, Vol. 46, Issue 1
  • DOI: 10.1099/00207713-46-1-195

Butyrivibrio hungatei sp. nov. and Pseudobutyrivibrio xylanivorans sp. nov., butyrate-producing bacteria from the rumen
journal, January 2003

  • Kopečný, Jan; Zorec, Maša; Mrázek, Jakub
  • International Journal of Systematic and Evolutionary Microbiology, Vol. 53, Issue 1
  • DOI: 10.1099/ijs.0.02345-0

Cell wall and plasma membrane architecture of Butyrivibrio spp.
journal, March 1985


The Growth Response of Cellulolytic Acetate-utilizing and Acetate-producing Butyrivibrios to Volatile Fatty Acids and Other Nutrients
journal, October 1973

  • Roche, C.; Albertyn, H.; Van Gylswyk, N. O.
  • Journal of General Microbiology, Vol. 78, Issue 2
  • DOI: 10.1099/00221287-78-2-253

Cellulolytic Bacteria Occurring in the Rumen of Sheep Conditioned to Low-protein Teff Hay
journal, March 1969


Towards a taxonomic coherence between average nucleotide identity and 16S rRNA gene sequence similarity for species demarcation of prokaryotes
journal, February 2014

  • Kim, M.; Oh, H. -S.; Park, S. -C.
  • INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 64, Issue Pt 2
  • DOI: 10.1099/ijs.0.059774-0

Shifting the genomic gold standard for the prokaryotic species definition
journal, October 2009

  • Richter, Michael; Rosselló-Móra, Ramon
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 45
  • DOI: 10.1073/pnas.0906412106

Bacterial Na+-translocating ferredoxin:NAD+ oxidoreductase
journal, October 2010

  • Biegel, E.; Muller, V.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 42
  • DOI: 10.1073/pnas.1010318107

The Rnf Complex of Clostridium ljungdahlii Is a Proton-Translocating Ferredoxin:NAD+ Oxidoreductase Essential for Autotrophic Growth
journal, December 2012


Electron transport phosphorylation in rumen butyrivibrios: unprecedented ATP yield for glucose fermentation to butyrate
journal, June 2015


Divergences in gene repertoire among the reference Prevotella genomes derived from distinct body sites of human
journal, January 2015

  • Gupta, Vinod; Chaudhari, Narendrakumar M.; Iskepalli, Suchismitha
  • BMC Genomics, Vol. 16, Issue 1
  • DOI: 10.1186/s12864-015-1350-6

Why prokaryotes have pangenomes
journal, March 2017


The fate of laterally transferred genes: Life in the fast lane to adaptation or death
journal, May 2006


The Glycobiome of the Rumen Bacterium Butyrivibrio proteoclasticus B316T Highlights Adaptation to a Polysaccharide-Rich Environment
journal, August 2010


The complete genome sequence of the rumen bacterium Butyrivibrio hungatei MB2003
journal, December 2017

  • Palevich, Nikola; Kelly, William J.; Leahy, Sinead C.
  • Standards in Genomic Sciences, Vol. 12, Issue 1
  • DOI: 10.1186/s40793-017-0285-8

Introducing the bacterial ‘chromid’: not a chromosome, not a plasmid
journal, April 2010

  • Harrison, Peter W.; Lower, Ryan P. J.; Kim, Nayoung K. D.
  • Trends in Microbiology, Vol. 18, Issue 4
  • DOI: 10.1016/j.tim.2009.12.010

Do Ruminal Bacteria Exchange Genetic Material?
journal, August 1996


Insights into the bovine rumen plasmidome
journal, March 2012

  • Kav, A. B.; Sasson, G.; Jami, E.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 14
  • DOI: 10.1073/pnas.1116410109

Horizontal Gene Transfer Accelerates Genome Innovation and Evolution
journal, June 2003


The Rumen: A Unique Source of Enzymes for Enhancing Livestock Production
journal, October 1996


The formation of microcolonies by rumen bacteria
journal, September 1980

  • Cheng, K. -J.; Costerton, J. W.
  • Canadian Journal of Microbiology, Vol. 26, Issue 9
  • DOI: 10.1139/m80-183

Are Ruminal Bacteria Armed with Bacteriocins?
journal, December 1996


Butyrivibrio hungatei MB2003 Competes Effectively for Soluble Sugars Released by Butyrivibrio proteoclasticus B316 T during Growth on Xylan or Pectin
journal, November 2018

  • Palevich, Nikola; Kelly, William J.; Ganesh, Siva
  • Applied and Environmental Microbiology, Vol. 85, Issue 3
  • DOI: 10.1128/AEM.02056-18

Involvement of Ech hydrogenase in energy conservation of Methanosarcina mazei: Function of Ech in energy conservation
journal, July 2010


Energy conservation via electron bifurcating ferredoxin reduction and proton/Na+ translocating ferredoxin oxidation
journal, February 2013

  • Buckel, Wolfgang; Thauer, Rudolf K.
  • Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1827, Issue 2
  • DOI: 10.1016/j.bbabio.2012.07.002

The Bidirectional NiFe-hydrogenase in Synechocystis sp. PCC 6803 Is Reduced by Flavodoxin and Ferredoxin and Is Essential under Mixotrophic, Nitrate-limiting Conditions
journal, December 2013

  • Gutekunst, Kirstin; Chen, Xi; Schreiber, Karoline
  • Journal of Biological Chemistry, Vol. 289, Issue 4
  • DOI: 10.1074/jbc.M113.526376

A Comparative Genomic Analysis of Energy Metabolism in Sulfate Reducing Bacteria and Archaea
journal, January 2011

  • Pereira, Inês A. Cardoso; Ramos, Ana Raquel; Grein, Fabian
  • Frontiers in Microbiology, Vol. 2
  • DOI: 10.3389/fmicb.2011.00069

A novel mode of lactate metabolism in strictly anaerobic bacteria: A novel mode of lactate metabolism in anaerobes
journal, May 2014

  • Weghoff, Marie Charlotte; Bertsch, Johannes; Müller, Volker
  • Environmental Microbiology, Vol. 17, Issue 3
  • DOI: 10.1111/1462-2920.12493

Metabolism of Methylglyoxal in Microorganisms
journal, January 1984


Isolation of previously uncultured rumen bacteria by dilution to extinction using a new liquid culture medium
journal, January 2011

  • Kenters, Nikki; Henderson, Gemma; Jeyanathan, Jeyamalar
  • Journal of Microbiological Methods, Vol. 84, Issue 1
  • DOI: 10.1016/j.mimet.2010.10.011

Bacterial Community Dynamics during Production of Registered Designation of Origin Salers Cheese as Evaluated by 16S rRNA Gene Single-Strand Conformation Polymorphism Analysis
journal, July 2003

  • Duthoit, Frédérique; Godon, Jean-Jacques; Montel, Marie-Christine
  • Applied and Environmental Microbiology, Vol. 69, Issue 7
  • DOI: 10.1128/aem.69.7.3840-3848.2003

Lactic acid bacterial diversity in the traditional Mexican fermented dough pozol as determined by 16S rDNA sequence analysis
journal, February 2001

  • Escalante, Adelfo; Wacher, Carmen; Farrés, Amelia
  • International Journal of Food Microbiology, Vol. 64, Issue 1-2
  • DOI: 10.1016/s0168-1605(00)00428-1

Some modifications in the procedure of direct sequencing of PCR amplified 16S rDNA
journal, December 1992


The under-recognized dominance of Verrucomicrobia in soil bacterial communities
journal, July 2011


NCBI Reference Sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins
journal, December 2004

  • Pruitt, K. D.
  • Nucleic Acids Research, Vol. 33, Issue Database issue
  • DOI: 10.1093/nar/gki025

NCBI BLAST: a better web interface
journal, May 2008

  • Johnson, M.; Zaretskaya, I.; Raytselis, Y.
  • Nucleic Acids Research, Vol. 36, Issue Web Server
  • DOI: 10.1093/nar/gkn201

The RDP-II (Ribosomal Database Project)
journal, January 2001


Multiple Sequence Alignment Using ClustalW and ClustalX
journal, August 2002

  • Thompson, Julie D.; Gibson, Toby. J.; Higgins, Des G.
  • Current Protocols in Bioinformatics, Vol. 00, Issue 1
  • DOI: 10.1002/0471250953.bi0203s00

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
  • DOI: 10.1093/molbev/mst197

The neighbor-joining method: a new method for reconstructing phylogenetic trees.
journal, July 1987


Clostridium proteoclasticum sp. nov., a Novel Proteolytic Bacterium from the Bovine Rumen
journal, July 1996

  • Attwood, G. T.; Reilly, K.; Patel, B. K. C.
  • International Journal of Systematic Bacteriology, Vol. 46, Issue 3
  • DOI: 10.1099/00207713-46-3-753

Genetic Diversity and Phylogenetic Relationships among Strains of Prevotella (Bacteroides) ruminicola from the Rumen
journal, April 1994

  • Avgustin, G.; Wright, F.; Flint, H. J.
  • International Journal of Systematic Bacteriology, Vol. 44, Issue 2
  • DOI: 10.1099/00207713-44-2-246

Characterization of Streptococcus bovis bacteriophages
journal, June 1976

  • Iverson, W. G.; Millis, Nancy F.
  • Canadian Journal of Microbiology, Vol. 22, Issue 6
  • DOI: 10.1139/m76-122

Flagellum Mediates Symbiosis
journal, March 2009


IMG/M: integrated genome and metagenome comparative data analysis system
journal, October 2016

  • Chen, I-Min A.; Markowitz, Victor M.; Chu, Ken
  • Nucleic Acids Research, Vol. 45, Issue D1
  • DOI: 10.1093/nar/gkw929

Gapped BLAST and PSI-BLAST: a new generation of protein database search programs
journal, September 1997

  • Altschul, Stephen F.; Madden, Thomas L.; Schäffer, Alejandro A.
  • Nucleic Acids Research, Vol. 25, Issue 17, p. 3389-3402
  • DOI: 10.1093/nar/25.17.3389

Simultaneous determination of volatile and non-volatile acidic fermentation products of anaerobes by capillary gas chromatography
journal, July 1989


Statistical Methods for Detecting Differentially Abundant Features in Clinical Metagenomic Samples
journal, April 2009


The Fast Changing Landscape of Sequencing Technologies and Their Impact on Microbial Genome Assemblies and Annotation
journal, December 2012


Real-Time DNA Sequencing from Single Polymerase Molecules
journal, January 2009


Velvet: Algorithms for de novo short read assembly using de Bruijn graphs
journal, February 2008


ALLPATHS: De novo assembly of whole-genome shotgun microreads
journal, February 2008

  • Butler, J.; MacCallum, I.; Kleber, M.
  • Genome Research, Vol. 18, Issue 5
  • DOI: 10.1101/gr.7337908

Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data
journal, May 2013

  • Chin, Chen-Shan; Alexander, David H.; Marks, Patrick
  • Nature Methods, Vol. 10, Issue 6
  • DOI: 10.1038/nmeth.2474

The standard operating procedure of the DOE-JGI Metagenome Annotation Pipeline (MAP v.4)
journal, February 2016

  • Huntemann, Marcel; Ivanova, Natalia N.; Mavromatis, Konstantinos
  • Standards in Genomic Sciences, Vol. 11, Issue 1
  • DOI: 10.1186/s40793-016-0138-x

Toward a standard in structural genome annotation for prokaryotes
journal, July 2015

  • Tripp, H. James; Sutton, Granger; White, Owen
  • Standards in Genomic Sciences, Vol. 10, Issue 1
  • DOI: 10.1186/s40793-015-0034-9

Prodigal: prokaryotic gene recognition and translation initiation site identification
journal, March 2010


GenePRIMP: a gene prediction improvement pipeline for prokaryotic genomes
journal, May 2010

  • Pati, Amrita; Ivanova, Natalia N.; Mikhailova, Natalia
  • Nature Methods, Vol. 7, Issue 6
  • DOI: 10.1038/nmeth.1457

dbCAN: a web resource for automated carbohydrate-active enzyme annotation
journal, May 2012

  • Yin, Yanbin; Mao, Xizeng; Yang, Jincai
  • Nucleic Acids Research, Vol. 40, Issue W1
  • DOI: 10.1093/nar/gks479

CDD: conserved domains and protein three-dimensional structure
journal, November 2012

  • Marchler-Bauer, Aron; Zheng, Chanjuan; Chitsaz, Farideh
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1243

The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics
journal, January 2009

  • Cantarel, B. L.; Coutinho, P. M.; Rancurel, C.
  • Nucleic Acids Research, Vol. 37, Issue Database
  • DOI: 10.1093/nar/gkn663

Pfam: the protein families database
journal, November 2013

  • Finn, Robert D.; Bateman, Alex; Clements, Jody
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1223

The RCSB Protein Data Bank: new resources for research and education
journal, November 2012

  • Rose, Peter W.; Bi, Chunxiao; Bluhm, Wolfgang F.
  • Nucleic Acids Research, Vol. 41, Issue D1
  • DOI: 10.1093/nar/gks1200

PSimScan: Algorithm and Utility for Fast Protein Similarity Search
journal, March 2013


Tracing Lifestyle Adaptation in Prokaryotic Genomes
journal, January 2012


IMG 4 version of the integrated microbial genomes comparative analysis system
journal, October 2013

  • Markowitz, Victor M.; Chen, I-Min A.; Palaniappan, Krishna
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt963

GAMOLA2, a Comprehensive Software Package for the Annotation and Curation of Draft and Complete Microbial Genomes
journal, March 2017


Numerical Taxonomy
journal, March 1962

  • Sneath, P. H. A.; Sokal, Robert R.
  • Nature, Vol. 193, Issue 4818
  • DOI: 10.1038/193855a0

The rapid generation of mutation data matrices from protein sequences
journal, January 1992


Alignment of whole genomes
journal, January 1999

  • Delcher, A. L.; Kasif, S.; Fleischmann, R. D.
  • Nucleic Acids Research, Vol. 27, Issue 11
  • DOI: 10.1093/nar/27.11.2369

CMG-Biotools, a Free Workbench for Basic Comparative Microbial Genomics
journal, April 2013


R: A Language for Data Analysis and Graphics
journal, September 1996

  • Ihaka, Ross; Gentleman, Robert
  • Journal of Computational and Graphical Statistics, Vol. 5, Issue 3
  • DOI: 10.2307/1390807

An Ordination of the Upland Forest Communities of Southern Wisconsin
journal, February 1957

  • Bray, J. Roger; Curtis, J. T.
  • Ecological Monographs, Vol. 27, Issue 4
  • DOI: 10.2307/1942268

Hierarchical Grouping to Optimize an Objective Function
journal, March 1963

  • Ward, Joe H.
  • Journal of the American Statistical Association, Vol. 58, Issue 301
  • DOI: 10.2307/2282967

The MetaCyc database of metabolic pathways and enzymes and the BioCyc collection of pathway/genome databases
journal, November 2011

  • Caspi, R.; Altman, T.; Dreher, K.
  • Nucleic Acids Research, Vol. 40, Issue D1
  • DOI: 10.1093/nar/gkr1014

KEGG: Kyoto Encyclopedia of Genes and Genomes
journal, January 2000

  • Kanehisa, Minoru; Goto, Susumu
  • Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30
  • DOI: 10.1093/nar/28.1.27