Comparative Genomics of Early-Diverging <italic toggle="yes">Brucella</italic> Strains Reveals a Novel Lipopolysaccharide Biosynthesis Pathway

ABSTRACT Brucella species are Gram-negative bacteria that infect mammals. Recently, two unusual strains (Brucella inopinata BO1T and B. inopinata-like BO2) have been isolated from human patients, and their similarity to some atypical brucellae isolated from Australian native rodent species was noted...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Alice R. Wattam, Thomas J. Inzana, Kelly P. Williams, Shrinivasrao P. Mane, Maulik Shukla, Nalvo F. Almeida, Allan W. Dickerman, Steven Mason, Ignacio Moriyón, David O’Callaghan, Adrian M. Whatmore, Bruno W. Sobral, Rebekah V. Tiller, Alex R. Hoffmaster, Michael A. Frace, Cristina De Castro, Antonio Molinaro, Stephen M. Boyle, Barun K. De, João C. Setubal
Formato: article
Lenguaje:EN
Publicado: American Society for Microbiology 2012
Materias:
Acceso en línea:https://doaj.org/article/917da65e0f394b86a9e8d26345cca254
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:917da65e0f394b86a9e8d26345cca254
record_format dspace
spelling oai:doaj.org-article:917da65e0f394b86a9e8d26345cca2542021-11-15T15:39:12ZComparative Genomics of Early-Diverging <italic toggle="yes">Brucella</italic> Strains Reveals a Novel Lipopolysaccharide Biosynthesis Pathway10.1128/mBio.00246-122150-7511https://doaj.org/article/917da65e0f394b86a9e8d26345cca2542012-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00246-12https://doaj.org/toc/2150-7511ABSTRACT Brucella species are Gram-negative bacteria that infect mammals. Recently, two unusual strains (Brucella inopinata BO1T and B. inopinata-like BO2) have been isolated from human patients, and their similarity to some atypical brucellae isolated from Australian native rodent species was noted. Here we present a phylogenomic analysis of the draft genome sequences of BO1T and BO2 and of the Australian rodent strains 83-13 and NF2653 that shows that they form two groups well separated from the other sequenced Brucella spp. Several important differences were noted. Both BO1T and BO2 did not agglutinate significantly when live or inactivated cells were exposed to monospecific A and M antisera against O-side chain sugars composed of N-formyl-perosamine. While BO1T maintained the genes required to synthesize a typical Brucella O-antigen, BO2 lacked many of these genes but still produced a smooth LPS (lipopolysaccharide). Most missing genes were found in the wbk region involved in O-antigen synthesis in classic smooth Brucella spp. In their place, BO2 carries four genes that other bacteria use for making a rhamnose-based O-antigen. Electrophoretic, immunoblot, and chemical analyses showed that BO2 carries an antigenically different O-antigen made of repeating hexose-rich oligosaccharide units that made the LPS water-soluble, which contrasts with the homopolymeric O-antigen of other smooth brucellae that have a phenol-soluble LPS. The results demonstrate the existence of a group of early-diverging brucellae with traits that depart significantly from those of the Brucella species described thus far. IMPORTANCE This report examines differences between genomes from four new Brucella strains and those from the classic Brucella spp. Our results show that the four new strains are outliers with respect to the previously known Brucella strains and yet are part of the genus, forming two new clades. The analysis revealed important information about the evolution and survival mechanisms of Brucella species, helping reshape our knowledge of this important zoonotic pathogen. One discovery of special importance is that one of the strains, BO2, produces an O-antigen distinct from any that has been seen in any other Brucella isolates to date.Alice R. WattamThomas J. InzanaKelly P. WilliamsShrinivasrao P. ManeMaulik ShuklaNalvo F. AlmeidaAllan W. DickermanSteven MasonIgnacio MoriyónDavid O’CallaghanAdrian M. WhatmoreBruno W. SobralRebekah V. TillerAlex R. HoffmasterMichael A. FraceCristina De CastroAntonio MolinaroStephen M. BoyleBarun K. DeJoão C. SetubalAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 3, Iss 5 (2012)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Alice R. Wattam
Thomas J. Inzana
Kelly P. Williams
Shrinivasrao P. Mane
Maulik Shukla
Nalvo F. Almeida
Allan W. Dickerman
Steven Mason
Ignacio Moriyón
David O’Callaghan
Adrian M. Whatmore
Bruno W. Sobral
Rebekah V. Tiller
Alex R. Hoffmaster
Michael A. Frace
Cristina De Castro
Antonio Molinaro
Stephen M. Boyle
Barun K. De
João C. Setubal
Comparative Genomics of Early-Diverging <italic toggle="yes">Brucella</italic> Strains Reveals a Novel Lipopolysaccharide Biosynthesis Pathway
description ABSTRACT Brucella species are Gram-negative bacteria that infect mammals. Recently, two unusual strains (Brucella inopinata BO1T and B. inopinata-like BO2) have been isolated from human patients, and their similarity to some atypical brucellae isolated from Australian native rodent species was noted. Here we present a phylogenomic analysis of the draft genome sequences of BO1T and BO2 and of the Australian rodent strains 83-13 and NF2653 that shows that they form two groups well separated from the other sequenced Brucella spp. Several important differences were noted. Both BO1T and BO2 did not agglutinate significantly when live or inactivated cells were exposed to monospecific A and M antisera against O-side chain sugars composed of N-formyl-perosamine. While BO1T maintained the genes required to synthesize a typical Brucella O-antigen, BO2 lacked many of these genes but still produced a smooth LPS (lipopolysaccharide). Most missing genes were found in the wbk region involved in O-antigen synthesis in classic smooth Brucella spp. In their place, BO2 carries four genes that other bacteria use for making a rhamnose-based O-antigen. Electrophoretic, immunoblot, and chemical analyses showed that BO2 carries an antigenically different O-antigen made of repeating hexose-rich oligosaccharide units that made the LPS water-soluble, which contrasts with the homopolymeric O-antigen of other smooth brucellae that have a phenol-soluble LPS. The results demonstrate the existence of a group of early-diverging brucellae with traits that depart significantly from those of the Brucella species described thus far. IMPORTANCE This report examines differences between genomes from four new Brucella strains and those from the classic Brucella spp. Our results show that the four new strains are outliers with respect to the previously known Brucella strains and yet are part of the genus, forming two new clades. The analysis revealed important information about the evolution and survival mechanisms of Brucella species, helping reshape our knowledge of this important zoonotic pathogen. One discovery of special importance is that one of the strains, BO2, produces an O-antigen distinct from any that has been seen in any other Brucella isolates to date.
format article
author Alice R. Wattam
Thomas J. Inzana
Kelly P. Williams
Shrinivasrao P. Mane
Maulik Shukla
Nalvo F. Almeida
Allan W. Dickerman
Steven Mason
Ignacio Moriyón
David O’Callaghan
Adrian M. Whatmore
Bruno W. Sobral
Rebekah V. Tiller
Alex R. Hoffmaster
Michael A. Frace
Cristina De Castro
Antonio Molinaro
Stephen M. Boyle
Barun K. De
João C. Setubal
author_facet Alice R. Wattam
Thomas J. Inzana
Kelly P. Williams
Shrinivasrao P. Mane
Maulik Shukla
Nalvo F. Almeida
Allan W. Dickerman
Steven Mason
Ignacio Moriyón
David O’Callaghan
Adrian M. Whatmore
Bruno W. Sobral
Rebekah V. Tiller
Alex R. Hoffmaster
Michael A. Frace
Cristina De Castro
Antonio Molinaro
Stephen M. Boyle
Barun K. De
João C. Setubal
author_sort Alice R. Wattam
title Comparative Genomics of Early-Diverging <italic toggle="yes">Brucella</italic> Strains Reveals a Novel Lipopolysaccharide Biosynthesis Pathway
title_short Comparative Genomics of Early-Diverging <italic toggle="yes">Brucella</italic> Strains Reveals a Novel Lipopolysaccharide Biosynthesis Pathway
title_full Comparative Genomics of Early-Diverging <italic toggle="yes">Brucella</italic> Strains Reveals a Novel Lipopolysaccharide Biosynthesis Pathway
title_fullStr Comparative Genomics of Early-Diverging <italic toggle="yes">Brucella</italic> Strains Reveals a Novel Lipopolysaccharide Biosynthesis Pathway
title_full_unstemmed Comparative Genomics of Early-Diverging <italic toggle="yes">Brucella</italic> Strains Reveals a Novel Lipopolysaccharide Biosynthesis Pathway
title_sort comparative genomics of early-diverging <italic toggle="yes">brucella</italic> strains reveals a novel lipopolysaccharide biosynthesis pathway
publisher American Society for Microbiology
publishDate 2012
url https://doaj.org/article/917da65e0f394b86a9e8d26345cca254
work_keys_str_mv AT alicerwattam comparativegenomicsofearlydivergingitalictoggleyesbrucellaitalicstrainsrevealsanovellipopolysaccharidebiosynthesispathway
AT thomasjinzana comparativegenomicsofearlydivergingitalictoggleyesbrucellaitalicstrainsrevealsanovellipopolysaccharidebiosynthesispathway
AT kellypwilliams comparativegenomicsofearlydivergingitalictoggleyesbrucellaitalicstrainsrevealsanovellipopolysaccharidebiosynthesispathway
AT shrinivasraopmane comparativegenomicsofearlydivergingitalictoggleyesbrucellaitalicstrainsrevealsanovellipopolysaccharidebiosynthesispathway
AT maulikshukla comparativegenomicsofearlydivergingitalictoggleyesbrucellaitalicstrainsrevealsanovellipopolysaccharidebiosynthesispathway
AT nalvofalmeida comparativegenomicsofearlydivergingitalictoggleyesbrucellaitalicstrainsrevealsanovellipopolysaccharidebiosynthesispathway
AT allanwdickerman comparativegenomicsofearlydivergingitalictoggleyesbrucellaitalicstrainsrevealsanovellipopolysaccharidebiosynthesispathway
AT stevenmason comparativegenomicsofearlydivergingitalictoggleyesbrucellaitalicstrainsrevealsanovellipopolysaccharidebiosynthesispathway
AT ignaciomoriyon comparativegenomicsofearlydivergingitalictoggleyesbrucellaitalicstrainsrevealsanovellipopolysaccharidebiosynthesispathway
AT davidocallaghan comparativegenomicsofearlydivergingitalictoggleyesbrucellaitalicstrainsrevealsanovellipopolysaccharidebiosynthesispathway
AT adrianmwhatmore comparativegenomicsofearlydivergingitalictoggleyesbrucellaitalicstrainsrevealsanovellipopolysaccharidebiosynthesispathway
AT brunowsobral comparativegenomicsofearlydivergingitalictoggleyesbrucellaitalicstrainsrevealsanovellipopolysaccharidebiosynthesispathway
AT rebekahvtiller comparativegenomicsofearlydivergingitalictoggleyesbrucellaitalicstrainsrevealsanovellipopolysaccharidebiosynthesispathway
AT alexrhoffmaster comparativegenomicsofearlydivergingitalictoggleyesbrucellaitalicstrainsrevealsanovellipopolysaccharidebiosynthesispathway
AT michaelafrace comparativegenomicsofearlydivergingitalictoggleyesbrucellaitalicstrainsrevealsanovellipopolysaccharidebiosynthesispathway
AT cristinadecastro comparativegenomicsofearlydivergingitalictoggleyesbrucellaitalicstrainsrevealsanovellipopolysaccharidebiosynthesispathway
AT antoniomolinaro comparativegenomicsofearlydivergingitalictoggleyesbrucellaitalicstrainsrevealsanovellipopolysaccharidebiosynthesispathway
AT stephenmboyle comparativegenomicsofearlydivergingitalictoggleyesbrucellaitalicstrainsrevealsanovellipopolysaccharidebiosynthesispathway
AT barunkde comparativegenomicsofearlydivergingitalictoggleyesbrucellaitalicstrainsrevealsanovellipopolysaccharidebiosynthesispathway
AT joaocsetubal comparativegenomicsofearlydivergingitalictoggleyesbrucellaitalicstrainsrevealsanovellipopolysaccharidebiosynthesispathway
_version_ 1718427778907373568