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Title: Genomic analysis of three Bifidobacterium species isolated from the calf gastrointestinal tract

Abstract

Ruminant animals contribute significantly to the global value of agriculture and rely on a complex microbial community for efficient digestion. However, little is known of how this microbial-host relationship develops and is maintained. To begin to address this, we have determined the ability of three Bifidobacterium species isolated from the faeces of newborn calves to grow on carbohydrates typical of a newborn ruminant diet. Genome sequences have been determined for these bacteria with analysis of the genomes providing insights into the host association and identification of several genes that may mediate interactions with the ruminant gastrointestinal tract. The present study provides a starting point from which we can define the role of potential beneficial microbes in the nutrition of young ruminants and begin to influence the interactions between the microbiota and the host. The differences observed in genomic content hint at niche partitioning among the bifidobacterial species analysed and the different strategies they employ to successfully adapt to this habitat.

Authors:
 [1];  [1];  [1];  [1];  [1];  [1];  [1];  [2];  [2];  [1]
  1. Grasslands Research Centre, Palmerston North (New Zealand)
  2. USDOE Joint Genome Institute (JGI), Walnut Creek, CA (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1379531
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Scientific Reports
Additional Journal Information:
Journal Volume: 6; Journal Issue: 1; Journal ID: ISSN 2045-2322
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; bacterial genomics; bacteriology

Citation Formats

Kelly, William J., Cookson, Adrian L., Altermann, Eric, Lambie, Suzanne C., Perry, Rechelle, Teh, Koon Hoong, Otter, Don E., Shapiro, Nicole, Woyke, Tanja, and Leahy, Sinead C. Genomic analysis of three Bifidobacterium species isolated from the calf gastrointestinal tract. United States: N. p., 2016. Web. doi:10.1038/srep30768.
Kelly, William J., Cookson, Adrian L., Altermann, Eric, Lambie, Suzanne C., Perry, Rechelle, Teh, Koon Hoong, Otter, Don E., Shapiro, Nicole, Woyke, Tanja, & Leahy, Sinead C. Genomic analysis of three Bifidobacterium species isolated from the calf gastrointestinal tract. United States. https://doi.org/10.1038/srep30768
Kelly, William J., Cookson, Adrian L., Altermann, Eric, Lambie, Suzanne C., Perry, Rechelle, Teh, Koon Hoong, Otter, Don E., Shapiro, Nicole, Woyke, Tanja, and Leahy, Sinead C. Fri . "Genomic analysis of three Bifidobacterium species isolated from the calf gastrointestinal tract". United States. https://doi.org/10.1038/srep30768. https://www.osti.gov/servlets/purl/1379531.
@article{osti_1379531,
title = {Genomic analysis of three Bifidobacterium species isolated from the calf gastrointestinal tract},
author = {Kelly, William J. and Cookson, Adrian L. and Altermann, Eric and Lambie, Suzanne C. and Perry, Rechelle and Teh, Koon Hoong and Otter, Don E. and Shapiro, Nicole and Woyke, Tanja and Leahy, Sinead C.},
abstractNote = {Ruminant animals contribute significantly to the global value of agriculture and rely on a complex microbial community for efficient digestion. However, little is known of how this microbial-host relationship develops and is maintained. To begin to address this, we have determined the ability of three Bifidobacterium species isolated from the faeces of newborn calves to grow on carbohydrates typical of a newborn ruminant diet. Genome sequences have been determined for these bacteria with analysis of the genomes providing insights into the host association and identification of several genes that may mediate interactions with the ruminant gastrointestinal tract. The present study provides a starting point from which we can define the role of potential beneficial microbes in the nutrition of young ruminants and begin to influence the interactions between the microbiota and the host. The differences observed in genomic content hint at niche partitioning among the bifidobacterial species analysed and the different strategies they employ to successfully adapt to this habitat.},
doi = {10.1038/srep30768},
journal = {Scientific Reports},
number = 1,
volume = 6,
place = {United States},
year = {Fri Jul 29 00:00:00 EDT 2016},
month = {Fri Jul 29 00:00:00 EDT 2016}
}

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Works referenced in this record:

Supporting community annotation and user collaboration in the integrated microbial genomes (IMG) system
journal, April 2016


Structural basis for arabinoxylo-oligosaccharide capture by the probiotic Bifidobacterium animalis subsp. lactis  Bl-04 : Arabinoxylo-oligosaccharide capture in
journal, October 2013

  • Ejby, Morten; Fredslund, Folmer; Vujicic-Zagar, Andreja
  • Molecular Microbiology, Vol. 90, Issue 5
  • DOI: 10.1111/mmi.12419

Exploring Vertical Transmission of Bifidobacteria from Mother to Child
journal, July 2015

  • Milani, Christian; Mancabelli, Leonardo; Lugli, Gabriele Andrea
  • Applied and Environmental Microbiology, Vol. 81, Issue 20
  • DOI: 10.1128/AEM.02037-15

Identification of Bifidobacterium strains from faeces of lambs
journal, June 2012


Metabolism of Four α-Glycosidic Linkage-Containing Oligosaccharides by Bifidobacterium breve UCC2003
journal, August 2013

  • O'Connell, Kerry Joan; O'Connell Motherway, Mary; O'Callaghan, John
  • Applied and Environmental Microbiology, Vol. 79, Issue 20
  • DOI: 10.1128/AEM.01775-13

Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging
journal, October 2010

  • Turroni, F.; Bottacini, F.; Foroni, E.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 45
  • DOI: 10.1073/pnas.1011100107

Genomic Overview and Biological Functions of Exopolysaccharide Biosynthesis in Bifidobacterium spp.
journal, October 2013

  • Hidalgo-Cantabrana, Claudio; Sánchez, Borja; Milani, Christian
  • Applied and Environmental Microbiology, Vol. 80, Issue 1
  • DOI: 10.1128/AEM.02977-13

Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor
journal, June 2011

  • O'Connell Motherway, M.; Zomer, A.; Leahy, S. C.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 27
  • DOI: 10.1073/pnas.1105380108

Tracing Lifestyle Adaptation in Prokaryotic Genomes
journal, January 2012


Transcriptional analysis of oligosaccharide utilization by Bifidobacterium lactis Bl-04
journal, January 2013

  • Andersen, Joakim Mark; Barrangou, Rodolphe; Abou Hachem, Maher
  • BMC Genomics, Vol. 14, Issue 1
  • DOI: 10.1186/1471-2164-14-312

Bifidobacteria: their impact on gut microbiota composition and their applications as probiotics in infants
journal, November 2013

  • Di Gioia, Diana; Aloisio, Irene; Mazzola, Giuseppe
  • Applied Microbiology and Biotechnology, Vol. 98, Issue 2
  • DOI: 10.1007/s00253-013-5405-9

OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes
journal, September 2003


Getting better with bifidobacteria
journal, June 2005


Bifidobacteria can protect from enteropathogenic infection through production of acetate
journal, January 2011

  • Fukuda, Shinji; Toh, Hidehiro; Hase, Koji
  • Nature, Vol. 469, Issue 7331
  • DOI: 10.1038/nature09646

Bifidobacterium cuniculi, Bifidobacterium choerinum, Bifidobacterium boum, and Bifidobacterium pseudocatenulatum: Four New Species and Their Deoxyribonucleic Acid Homology Relationships
journal, October 1979

  • Scardovi, V.; Trovatelli, L. D.; Biavati, B.
  • International Journal of Systematic Bacteriology, Vol. 29, Issue 4
  • DOI: 10.1099/00207713-29-4-291

16S rRNA gene-based profiling of the human infant gut microbiota is strongly influenced by sample processing and PCR primer choice
journal, June 2015


Global Survey of the Bovine Salivary Proteome: Integrating Multidimensional Prefractionation, Targeted, and Glycocapture Strategies
journal, November 2011

  • Ang, Ching-Seng; Binos, Steve; Knight, Matthew I.
  • Journal of Proteome Research, Vol. 10, Issue 11
  • DOI: 10.1021/pr200516d

Bifidobacterial Enzymes Involved in the Metabolism of Human Milk Oligosaccharides
journal, May 2012


Structural and functional characteristics of bovine milk protein glycosylation
journal, January 2014


Impact of probiotic administration on the health and fecal microbiota of young calves: A meta-analysis of randomized controlled trials of lactic acid bacteria
journal, August 2012


Evolutionary adaptations of ruminants and their potential relevance for modern production systems
journal, March 2010


Cloning and expression of sucrose phosphorylase gene from Bifidobacterium longum in E. coli and characterization of the recombinant enzyme
journal, January 2003

  • Kim, Mijin; Kwon, Taeyeon; Joo Lee, Hyong
  • Biotechnology Letters, Vol. 25, Issue 15, p. 1211-1217
  • DOI: 10.1023/A:1025035320983

Invited review: Transitioning from milk to solid feed in dairy heifers
journal, February 2016

  • Khan, M. A.; Bach, A.; Weary, D. M.
  • Journal of Dairy Science, Vol. 99, Issue 2
  • DOI: 10.3168/jds.2015-9975

Crystallographic and Mutational Analyses of Substrate Recognition of Endo-α-N-acetylgalactosaminidase from Bifidobacterium longum
journal, June 2009

  • Suzuki, Ryuichiro; Katayama, Takane; Kitaoka, Motomitsu
  • The Journal of Biochemistry, Vol. 146, Issue 3
  • DOI: 10.1093/jb/mvp086

The interaction between bacteria and bile
journal, September 2005


Comparative Genomics Revealed Genetic Diversity and Species/Strain-Level Differences in Carbohydrate Metabolism of Three Probiotic Bifidobacterial Species
journal, January 2015

  • Odamaki, Toshitaka; Horigome, Ayako; Sugahara, Hirosuke
  • International Journal of Genomics, Vol. 2015
  • DOI: 10.1155/2015/567809

The ESX System in Bacillus subtilis Mediates Protein Secretion
journal, May 2014


Genomic Encyclopedia of Type Strains of the Genus Bifidobacterium
journal, August 2014

  • Milani, Christian; Lugli, Gabriele Andrea; Duranti, Sabrina
  • Applied and Environmental Microbiology, Vol. 80, Issue 20
  • DOI: 10.1128/AEM.02308-14

Expression of sortase-dependent pili of Bifidobacterium bifidum PRL2010 in response to environmental gut conditions
journal, July 2014

  • Turroni, Francesca; Serafini, Fausta; Mangifesta, Marta
  • FEMS Microbiology Letters, Vol. 357, Issue 1
  • DOI: 10.1111/1574-6968.12509

Modulation of the eps -ome transcription of bifidobacteria through simulation of human intestinal environment
journal, March 2016

  • Ferrario, Chiara; Milani, Christian; Mancabelli, Leonardo
  • FEMS Microbiology Ecology, Vol. 92, Issue 4
  • DOI: 10.1093/femsec/fiw056

Type VII secretion — mycobacteria show the way
journal, November 2007

  • Abdallah, Abdallah M.; Gey van Pittius, Nicolaas C.; DiGiuseppe Champion, Patricia A.
  • Nature Reviews Microbiology, Vol. 5, Issue 11
  • DOI: 10.1038/nrmicro1773

A bile-inducible membrane protein mediates bifidobacterial bile resistance: Bile resistance in bifidobacteria
journal, February 2012


Bifidobacteria exhibit social behavior through carbohydrate resource sharing in the gut
journal, October 2015

  • Milani, Christian; Lugli, Gabriele Andrea; Duranti, Sabrina
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep15782

Survival of bifidobacteria administered to calves
journal, July 2010


Prophage-Like Elements in Bifidobacteria: Insights from Genomics, Transcription, Integration, Distribution, and Phylogenetic Analysis
journal, December 2005


Genomics of the Genus Bifidobacterium Reveals Species-Specific Adaptation to the Glycan-Rich Gut Environment
journal, November 2015

  • Milani, Christian; Turroni, Francesca; Duranti, Sabrina
  • Applied and Environmental Microbiology, Vol. 82, Issue 4
  • DOI: 10.1128/AEM.03500-15

Prophages of the genus B ifidobacterium as modulating agents of the infant gut microbiota : Bifidobacterial prophages and infant gut microbiota
journal, January 2016

  • Lugli, Gabriele Andrea; Milani, Christian; Turroni, Francesca
  • Environmental Microbiology, Vol. 18, Issue 7
  • DOI: 10.1111/1462-2920.13154

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

Role of sortase-dependent pili of Bifidobacterium bifidum PRL2010 in modulating bacterium-host interactions
journal, June 2013

  • Turroni, F.; Serafini, F.; Foroni, E.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 27
  • DOI: 10.1073/pnas.1303897110

The Impact of the Milk Glycobiome on the Neonate Gut Microbiota
journal, February 2015


Bifidobacteria: their impact on gut microbiota composition and their applications as probiotics in infants
journal, November 2013

  • Di Gioia, Diana; Aloisio, Irene; Mazzola, Giuseppe
  • Applied Microbiology and Biotechnology, Vol. 98, Issue 2
  • DOI: 10.1007/s00253-013-5405-9

Survival of bifidobacteria administered to calves
journal, July 2010


Impact of probiotic administration on the health and fecal microbiota of young calves: A meta-analysis of randomized controlled trials of lactic acid bacteria
journal, August 2012


A collaborative study of a method for the enumeration of probiotic bifidobacteria in animal feed
journal, June 2003


A comparative study of free oligosaccharides in the milk of domestic animals
journal, March 2014

  • Albrecht, Simone; Lane, Jonathan A.; Mariño, Karina
  • British Journal of Nutrition, Vol. 111, Issue 7
  • DOI: 10.1017/s0007114513003772

Global Survey of the Bovine Salivary Proteome: Integrating Multidimensional Prefractionation, Targeted, and Glycocapture Strategies
journal, November 2011

  • Ang, Ching-Seng; Binos, Steve; Knight, Matthew I.
  • Journal of Proteome Research, Vol. 10, Issue 11
  • DOI: 10.1021/pr200516d

Bifidobacteria can protect from enteropathogenic infection through production of acetate
journal, January 2011

  • Fukuda, Shinji; Toh, Hidehiro; Hase, Koji
  • Nature, Vol. 469, Issue 7331
  • DOI: 10.1038/nature09646

Type VII secretion — mycobacteria show the way
journal, November 2007

  • Abdallah, Abdallah M.; Gey van Pittius, Nicolaas C.; DiGiuseppe Champion, Patricia A.
  • Nature Reviews Microbiology, Vol. 5, Issue 11
  • DOI: 10.1038/nrmicro1773

Bifidobacteria exhibit social behavior through carbohydrate resource sharing in the gut
journal, October 2015

  • Milani, Christian; Lugli, Gabriele Andrea; Duranti, Sabrina
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep15782

Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging
journal, October 2010

  • Turroni, F.; Bottacini, F.; Foroni, E.
  • Proceedings of the National Academy of Sciences, Vol. 107, Issue 45
  • DOI: 10.1073/pnas.1011100107

Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor
journal, June 2011

  • O'Connell Motherway, M.; Zomer, A.; Leahy, S. C.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue 27
  • DOI: 10.1073/pnas.1105380108

Role of sortase-dependent pili of Bifidobacterium bifidum PRL2010 in modulating bacterium-host interactions
journal, June 2013

  • Turroni, F.; Serafini, F.; Foroni, E.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 27
  • DOI: 10.1073/pnas.1303897110

α- N -Acetylgalactosaminidase from Infant-associated Bifidobacteria Belonging to Novel Glycoside Hydrolase Family 129 Is Implicated in Alternative Mucin Degradation Pathway
journal, November 2011

  • Kiyohara, Masashi; Nakatomi, Takashi; Kurihara, Shin
  • Journal of Biological Chemistry, Vol. 287, Issue 1
  • DOI: 10.1074/jbc.m111.277384

Modulation of the eps -ome transcription of bifidobacteria through simulation of human intestinal environment
journal, March 2016

  • Ferrario, Chiara; Milani, Christian; Mancabelli, Leonardo
  • FEMS Microbiology Ecology, Vol. 92, Issue 4
  • DOI: 10.1093/femsec/fiw056

Structural and functional characteristics of bovine milk protein glycosylation
journal, January 2014


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

OrthoMCL: Identification of Ortholog Groups for Eukaryotic Genomes
journal, September 2003


Evaluation of bifidobacterial community composition in the human gut by means of a targeted amplicon sequencing (ITS) protocol
journal, September 2014


Expression of sortase-dependent pili of Bifidobacterium bifidum PRL2010 in response to environmental gut conditions
journal, July 2014

  • Turroni, Francesca; Serafini, Fausta; Mangifesta, Marta
  • FEMS Microbiology Letters, Vol. 357, Issue 1
  • DOI: 10.1111/1574-6968.12509

Getting better with bifidobacteria
journal, June 2005


Bile-Inducible Efflux Transporter from Bifidobacterium longum NCC2705, Conferring Bile Resistance
journal, March 2009

  • Gueimonde, M.; Garrigues, C.; van Sinderen, D.
  • Applied and Environmental Microbiology, Vol. 75, Issue 10
  • DOI: 10.1128/aem.00172-09

Screening for and Identification of Starch-, Amylopectin-, and Pullulan-Degrading Activities in Bifidobacterial Strains
journal, August 2006

  • Ryan, S. M.; Fitzgerald, G. F.; van Sinderen, D.
  • Applied and Environmental Microbiology, Vol. 72, Issue 8
  • DOI: 10.1128/aem.00257-06

Identification of N-Acetylhexosamine 1-Kinase in the Complete Lacto-N-Biose I/Galacto-N-Biose Metabolic Pathway in Bifidobacterium longum
journal, August 2007

  • Nishimoto, M.; Kitaoka, M.
  • Applied and Environmental Microbiology, Vol. 73, Issue 20
  • DOI: 10.1128/aem.01425-07

Distribution of In Vitro Fermentation Ability of Lacto-N-Biose I, a Major Building Block of Human Milk Oligosaccharides, in Bifidobacterial Strains
journal, October 2009

  • Xiao, J. -z.; Takahashi, S.; Nishimoto, M.
  • Applied and Environmental Microbiology, Vol. 76, Issue 1
  • DOI: 10.1128/aem.01683-09

Characterization of the Serpin-Encoding Gene of Bifidobacterium breve 210B
journal, March 2010

  • Turroni, F.; Foroni, E.; O'Connell Motherway, M.
  • Applied and Environmental Microbiology, Vol. 76, Issue 10
  • DOI: 10.1128/aem.02938-09

Bile Salt Hydrolase of Bifidobacterium longum---Biochemical and Genetic Characterization
journal, June 2000


The Impact of the Milk Glycobiome on the Neonate Gut Microbiota
journal, February 2015


Transcriptional analysis of oligosaccharide utilization by Bifidobacterium lactis Bl-04
journal, January 2013

  • Andersen, Joakim Mark; Barrangou, Rodolphe; Abou Hachem, Maher
  • BMC Genomics, Vol. 14, Issue 1
  • DOI: 10.1186/1471-2164-14-312

Genetic analysis and morphological identification of pilus-like structures in members of the genus Bifidobacterium
journal, January 2011


16S rRNA gene-based profiling of the human infant gut microbiota is strongly influenced by sample processing and PCR primer choice
journal, June 2015


The ESX System in Bacillus subtilis Mediates Protein Secretion
journal, May 2014


Invited review: Transitioning from milk to solid feed in dairy heifers
journal, February 2016

  • Khan, M. A.; Bach, A.; Weary, D. M.
  • Journal of Dairy Science, Vol. 99, Issue 2
  • DOI: 10.3168/jds.2015-9975

Calf Intestinal Mucin: Isolation, Partial Characterization, and Measurement in Ileal Digesta with an Enzyme-Linked Immunosorbent Assay
journal, March 2000


Tracing Lifestyle Adaptation in Prokaryotic Genomes
journal, January 2012


Bifidobacterial Enzymes Involved in the Metabolism of Human Milk Oligosaccharides
journal, May 2012


Score-based prediction of genomic islands in prokaryotic genomes using hidden Markov models
text, January 2006

  • Waack, Stephan; Keller, Oliver; Asper, Roman
  • Universität Regensburg
  • DOI: 10.5283/epub.10938

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journal, February 2018

  • Mathew, Sindhu; Aronsson, Anna; Karlsson, Eva Nordberg
  • Applied Microbiology and Biotechnology, Vol. 102, Issue 7
  • DOI: 10.1007/s00253-018-8823-x

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journal, November 2018

  • Ru, Xiao; Zhang, Chuang-Chuang; Yuan, Ya-Hong
  • Applied Microbiology and Biotechnology, Vol. 103, Issue 2
  • DOI: 10.1007/s00253-018-9492-5

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journal, January 2018

  • Arboleya, Silvia; Bottacini, Francesca; O’Connell-Motherway, Mary
  • BMC Genomics, Vol. 19, Issue 1
  • DOI: 10.1186/s12864-017-4388-9

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journal, September 2017

  • Hidalgo-Cantabrana, Claudio; Crawley, Alexandra B.; Sanchez, Borja
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.01851

Culture independent analysis using gnd as a target gene to assess Escherichia coli diversity and community structure
journal, April 2017

  • Cookson, Adrian L.; Biggs, Patrick J.; Marshall, Jonathan C.
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/s41598-017-00890-6

Gene-trait matching across the Bifidobacterium longum pan-genome reveals considerable diversity in carbohydrate catabolism among human infant strains
journal, January 2018

  • Arboleya, Silvia; Bottacini, Francesca; O’Connell-Motherway, Mary
  • BMC Genomics, Vol. 19, Issue 1
  • DOI: 10.1186/s12864-017-4388-9

Characterization and Exploitation of CRISPR Loci in Bifidobacterium longum
journal, September 2017

  • Hidalgo-Cantabrana, Claudio; Crawley, Alexandra B.; Sanchez, Borja
  • Frontiers in Microbiology, Vol. 8
  • DOI: 10.3389/fmicb.2017.01851