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

Mary O'Connell Motherway; Aldert Zomer; Sinead C Leahy; Justus Reunanen; Francesca Bottacini; Marcus J Claesson; Frances O'Brien; Kiera Flynn; Patrick G Casey; Jose Antonio Moreno Munoz; Breda Kearney; Aileen M Houston; Caitlin O'Mahony; Des G Higgins; Fergus Shanahan; Airi Palva; Willem M de Vos; Gerald F Fitzgerald; Marco Ventura; Paul W O'Toole; Douwe van Sinderen

doi:10.1073/pnas.1105380108

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

Mary O'Connell Motherway, Aldert Zomer, Sinead C Leahy, Justus Reunanen, Francesca Bottacini, Marcus J Claesson, Frances O'Brien, Kiera Flynn, Patrick G Casey, Jose Antonio Moreno Munoz, Breda Kearney, Aileen M Houston, Caitlin O'Mahony, Des G Higgins, Fergus Shanahan, Airi Palva, Willem M de Vos, Gerald F Fitzgerald, Marco Ventura, Paul W O'TooleDouwe van Sinderen

National University of Ireland, Galway

Research output: Contribution to journal › Article › Academic › peer-review

Abstract

Development of the human gut microbiota commences at birth, with bifidobacteria being among the first colonizers of the sterile newborn gastrointestinal tract. To date, the genetic basis of Bifidobacterium colonization and persistence remains poorly understood. Transcriptome analysis of the Bifidobacterium breve UCC2003 2.42-Mb genome in a murine colonization model revealed differential expression of a type IVb tight adherence (Tad) pilus-encoding gene cluster designated "tad(2003)." Mutational analysis demonstrated that the tad(2003) gene cluster is essential for efficient in vivo murine gut colonization, and immunogold transmission electron microscopy confirmed the presence of Tad pili at the poles of B. breve UCC2003 cells. Conservation of the Tad pilus-encoding locus among other B. breve strains and among sequenced Bifidobacterium genomes supports the notion of a ubiquitous pili-mediated host colonization and persistence mechanism for bifidobacteria.

Original language	English
Pages (from-to)	11217-22
Number of pages	6
Journal	Proceedings of the National Academy of Sciences of the United States of America
Volume	108
Issue number	27
DOIs	https://doi.org/10.1073/pnas.1105380108
Publication status	Published - 5 Jul 2011

Keywords

Amino Acid Sequence
Animals
Bacterial Proteins
Base Sequence
Bifidobacterium
Comparative Genomic Hybridization
DNA, Bacterial
Female
Fimbriae, Bacterial
Gastrointestinal Tract
Gene Expression Regulation, Bacterial
Genome, Bacterial
Germ-Free Life
Humans
Male
Metagenome
Mice
Mice, Inbred BALB C
Microscopy, Electron, Transmission
Microscopy, Immunoelectron
Molecular Sequence Data
Multigene Family
Mutation
Sequence Homology, Amino Acid

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10.1073/pnas.1105380108

Cite this

O'Connell Motherway, M., Zomer, A., Leahy, S. C., Reunanen, J., Bottacini, F., Claesson, M. J., O'Brien, F., Flynn, K., Casey, P. G., Munoz, J. A. M., Kearney, B., Houston, A. M., O'Mahony, C., Higgins, D. G., Shanahan, F., Palva, A., de Vos, W. M., Fitzgerald, G. F., Ventura, M., ... van Sinderen, D. (2011). Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. Proceedings of the National Academy of Sciences of the United States of America, 108(27), 11217-22. https://doi.org/10.1073/pnas.1105380108

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

abstract = "Development of the human gut microbiota commences at birth, with bifidobacteria being among the first colonizers of the sterile newborn gastrointestinal tract. To date, the genetic basis of Bifidobacterium colonization and persistence remains poorly understood. Transcriptome analysis of the Bifidobacterium breve UCC2003 2.42-Mb genome in a murine colonization model revealed differential expression of a type IVb tight adherence (Tad) pilus-encoding gene cluster designated {"}tad(2003).{"} Mutational analysis demonstrated that the tad(2003) gene cluster is essential for efficient in vivo murine gut colonization, and immunogold transmission electron microscopy confirmed the presence of Tad pili at the poles of B. breve UCC2003 cells. Conservation of the Tad pilus-encoding locus among other B. breve strains and among sequenced Bifidobacterium genomes supports the notion of a ubiquitous pili-mediated host colonization and persistence mechanism for bifidobacteria.",

keywords = "Amino Acid Sequence, Animals, Bacterial Proteins, Base Sequence, Bifidobacterium, Comparative Genomic Hybridization, DNA, Bacterial, Female, Fimbriae, Bacterial, Gastrointestinal Tract, Gene Expression Regulation, Bacterial, Genome, Bacterial, Germ-Free Life, Humans, Male, Metagenome, Mice, Mice, Inbred BALB C, Microscopy, Electron, Transmission, Microscopy, Immunoelectron, Molecular Sequence Data, Multigene Family, Mutation, Sequence Homology, Amino Acid",

author = "{O'Connell Motherway}, Mary and Aldert Zomer and Leahy, {Sinead C} and Justus Reunanen and Francesca Bottacini and Claesson, {Marcus J} and Frances O'Brien and Kiera Flynn and Casey, {Patrick G} and Munoz, {Jose Antonio Moreno} and Breda Kearney and Houston, {Aileen M} and Caitlin O'Mahony and Higgins, {Des G} and Fergus Shanahan and Airi Palva and {de Vos}, {Willem M} and Fitzgerald, {Gerald F} and Marco Ventura and O'Toole, {Paul W} and {van Sinderen}, Douwe",

year = "2011",

month = jul,

day = "5",

doi = "10.1073/pnas.1105380108",

language = "English",

volume = "108",

pages = "11217--22",

journal = "Proceedings of the National Academy of Sciences of the United States of America",

issn = "0027-8424",

publisher = "National Academy of Sciences",

number = "27",

}

O'Connell Motherway, M, Zomer, A, Leahy, SC, Reunanen, J, Bottacini, F, Claesson, MJ, O'Brien, F, Flynn, K, Casey, PG, Munoz, JAM, Kearney, B, Houston, AM, O'Mahony, C, Higgins, DG, Shanahan, F, Palva, A, de Vos, WM, Fitzgerald, GF, Ventura, M, O'Toole, PW & van Sinderen, D 2011, 'Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor', Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 27, pp. 11217-22. https://doi.org/10.1073/pnas.1105380108

Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. / O'Connell Motherway, Mary; Zomer, Aldert; Leahy, Sinead C et al.
In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 108, No. 27, 05.07.2011, p. 11217-22.

Research output: Contribution to journal › Article › Academic › peer-review

TY - JOUR

T1 - Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor

AU - O'Connell Motherway, Mary

AU - Zomer, Aldert

AU - Leahy, Sinead C

AU - Reunanen, Justus

AU - Bottacini, Francesca

AU - Claesson, Marcus J

AU - O'Brien, Frances

AU - Flynn, Kiera

AU - Casey, Patrick G

AU - Munoz, Jose Antonio Moreno

AU - Kearney, Breda

AU - Houston, Aileen M

AU - O'Mahony, Caitlin

AU - Higgins, Des G

AU - Shanahan, Fergus

AU - Palva, Airi

AU - de Vos, Willem M

AU - Fitzgerald, Gerald F

AU - Ventura, Marco

AU - O'Toole, Paul W

AU - van Sinderen, Douwe

PY - 2011/7/5

Y1 - 2011/7/5

N2 - Development of the human gut microbiota commences at birth, with bifidobacteria being among the first colonizers of the sterile newborn gastrointestinal tract. To date, the genetic basis of Bifidobacterium colonization and persistence remains poorly understood. Transcriptome analysis of the Bifidobacterium breve UCC2003 2.42-Mb genome in a murine colonization model revealed differential expression of a type IVb tight adherence (Tad) pilus-encoding gene cluster designated "tad(2003)." Mutational analysis demonstrated that the tad(2003) gene cluster is essential for efficient in vivo murine gut colonization, and immunogold transmission electron microscopy confirmed the presence of Tad pili at the poles of B. breve UCC2003 cells. Conservation of the Tad pilus-encoding locus among other B. breve strains and among sequenced Bifidobacterium genomes supports the notion of a ubiquitous pili-mediated host colonization and persistence mechanism for bifidobacteria.

AB - Development of the human gut microbiota commences at birth, with bifidobacteria being among the first colonizers of the sterile newborn gastrointestinal tract. To date, the genetic basis of Bifidobacterium colonization and persistence remains poorly understood. Transcriptome analysis of the Bifidobacterium breve UCC2003 2.42-Mb genome in a murine colonization model revealed differential expression of a type IVb tight adherence (Tad) pilus-encoding gene cluster designated "tad(2003)." Mutational analysis demonstrated that the tad(2003) gene cluster is essential for efficient in vivo murine gut colonization, and immunogold transmission electron microscopy confirmed the presence of Tad pili at the poles of B. breve UCC2003 cells. Conservation of the Tad pilus-encoding locus among other B. breve strains and among sequenced Bifidobacterium genomes supports the notion of a ubiquitous pili-mediated host colonization and persistence mechanism for bifidobacteria.

KW - Amino Acid Sequence

KW - Animals

KW - Bacterial Proteins

KW - Base Sequence

KW - Bifidobacterium

KW - Comparative Genomic Hybridization

KW - DNA, Bacterial

KW - Female

KW - Fimbriae, Bacterial

KW - Gastrointestinal Tract

KW - Gene Expression Regulation, Bacterial

KW - Genome, Bacterial

KW - Germ-Free Life

KW - Humans

KW - Male

KW - Metagenome

KW - Mice

KW - Mice, Inbred BALB C

KW - Microscopy, Electron, Transmission

KW - Microscopy, Immunoelectron

KW - Molecular Sequence Data

KW - Multigene Family

KW - Mutation

KW - Sequence Homology, Amino Acid

U2 - 10.1073/pnas.1105380108

DO - 10.1073/pnas.1105380108

M3 - Article

C2 - 21690406

SN - 0027-8424

VL - 108

SP - 11217

EP - 11222

JO - Proceedings of the National Academy of Sciences of the United States of America

JF - Proceedings of the National Academy of Sciences of the United States of America

IS - 27

ER -

O'Connell Motherway M, Zomer A, Leahy SC, Reunanen J, Bottacini F, Claesson MJ et al. Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. Proceedings of the National Academy of Sciences of the United States of America. 2011 Jul 5;108(27):11217-22. doi: 10.1073/pnas.1105380108

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

Abstract

Keywords

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