Evolution of the U.S. Biological Select Agent <named-content content-type="genus-species">Rathayibacter toxicus</named-content>

ABSTRACT Rathayibacter toxicus is a species of Gram-positive, corynetoxin-producing bacteria that causes annual ryegrass toxicity, a disease often fatal to grazing animals. A phylogenomic approach was employed to model the evolution of R. toxicus to explain the low genetic diversity observed among i...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Edward W. Davis, Javier F. Tabima, Alexandra J. Weisberg, Lucas Dantas Lopes, Michele S. Wiseman, Michael S. Wiseman, Tal Pupko, Michael S. Belcher, Aaron J. Sechler, Matt A. Tancos, Brenda K. Schroeder, Timothy D. Murray, Douglas G. Luster, William L. Schneider, Elizabeth E. Rogers, Fernando D. Andreote, Niklaus J. Grünwald, Melodie L. Putnam, Jeff H. Chang
Formato: article
Lenguaje:EN
Publicado: American Society for Microbiology 2018
Materias:
Acceso en línea:https://doaj.org/article/6a8c1015c1894d8f9d68a3cb5fc24206
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:6a8c1015c1894d8f9d68a3cb5fc24206
record_format dspace
spelling oai:doaj.org-article:6a8c1015c1894d8f9d68a3cb5fc242062021-11-15T16:00:15ZEvolution of the U.S. Biological Select Agent <named-content content-type="genus-species">Rathayibacter toxicus</named-content>10.1128/mBio.01280-182150-7511https://doaj.org/article/6a8c1015c1894d8f9d68a3cb5fc242062018-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01280-18https://doaj.org/toc/2150-7511ABSTRACT Rathayibacter toxicus is a species of Gram-positive, corynetoxin-producing bacteria that causes annual ryegrass toxicity, a disease often fatal to grazing animals. A phylogenomic approach was employed to model the evolution of R. toxicus to explain the low genetic diversity observed among isolates collected during a 30-year period of sampling in three regions of Australia, gain insight into the taxonomy of Rathayibacter, and provide a framework for studying these bacteria. Analyses of a data set of more than 100 sequenced Rathayibacter genomes indicated that Rathayibacter forms nine species-level groups. R. toxicus is the most genetically distant, and evidence suggested that this species experienced a dramatic event in its evolution. Its genome is significantly reduced in size but is colinear to those of sister species. Moreover, R. toxicus has low intergroup genomic diversity and almost no intragroup genomic diversity between ecologically separated isolates. R. toxicus is the only species of the genus that encodes a clustered regularly interspaced short palindromic repeat (CRISPR) locus and that is known to host a bacteriophage parasite. The spacers, which represent a chronological history of infections, were characterized for information on past events. We propose a three-stage process that emphasizes the importance of the bacteriophage and CRISPR in the genome reduction and low genetic diversity of the R. toxicus species. IMPORTANCE Rathayibacter toxicus is a toxin-producing species found in Australia and is often fatal to grazing animals. The threat of introduction of the species into the United States led to its inclusion in the Federal Select Agent Program, which makes R. toxicus a highly regulated species. This work provides novel insights into the evolution of R. toxicus. R. toxicus is the only species in the genus to have acquired a CRISPR adaptive immune system to protect against bacteriophages. Results suggest that coexistence with the bacteriophage NCPPB3778 led to the massive shrinkage of the R. toxicus genome, species divergence, and the maintenance of low genetic diversity in extant bacterial groups. This work contributes to an understanding of the evolution and ecology of an agriculturally important species of bacteria.Edward W. DavisJavier F. TabimaAlexandra J. WeisbergLucas Dantas LopesMichele S. WisemanMichael S. WisemanTal PupkoMichael S. BelcherAaron J. SechlerMatt A. TancosBrenda K. SchroederTimothy D. MurrayDouglas G. LusterWilliam L. SchneiderElizabeth E. RogersFernando D. AndreoteNiklaus J. GrünwaldMelodie L. PutnamJeff H. ChangAmerican Society for MicrobiologyarticleCRISPRevolutionspeciationbacteriophagesplant pathogensMicrobiologyQR1-502ENmBio, Vol 9, Iss 4 (2018)
institution DOAJ
collection DOAJ
language EN
topic CRISPR
evolution
speciation
bacteriophages
plant pathogens
Microbiology
QR1-502
spellingShingle CRISPR
evolution
speciation
bacteriophages
plant pathogens
Microbiology
QR1-502
Edward W. Davis
Javier F. Tabima
Alexandra J. Weisberg
Lucas Dantas Lopes
Michele S. Wiseman
Michael S. Wiseman
Tal Pupko
Michael S. Belcher
Aaron J. Sechler
Matt A. Tancos
Brenda K. Schroeder
Timothy D. Murray
Douglas G. Luster
William L. Schneider
Elizabeth E. Rogers
Fernando D. Andreote
Niklaus J. Grünwald
Melodie L. Putnam
Jeff H. Chang
Evolution of the U.S. Biological Select Agent <named-content content-type="genus-species">Rathayibacter toxicus</named-content>
description ABSTRACT Rathayibacter toxicus is a species of Gram-positive, corynetoxin-producing bacteria that causes annual ryegrass toxicity, a disease often fatal to grazing animals. A phylogenomic approach was employed to model the evolution of R. toxicus to explain the low genetic diversity observed among isolates collected during a 30-year period of sampling in three regions of Australia, gain insight into the taxonomy of Rathayibacter, and provide a framework for studying these bacteria. Analyses of a data set of more than 100 sequenced Rathayibacter genomes indicated that Rathayibacter forms nine species-level groups. R. toxicus is the most genetically distant, and evidence suggested that this species experienced a dramatic event in its evolution. Its genome is significantly reduced in size but is colinear to those of sister species. Moreover, R. toxicus has low intergroup genomic diversity and almost no intragroup genomic diversity between ecologically separated isolates. R. toxicus is the only species of the genus that encodes a clustered regularly interspaced short palindromic repeat (CRISPR) locus and that is known to host a bacteriophage parasite. The spacers, which represent a chronological history of infections, were characterized for information on past events. We propose a three-stage process that emphasizes the importance of the bacteriophage and CRISPR in the genome reduction and low genetic diversity of the R. toxicus species. IMPORTANCE Rathayibacter toxicus is a toxin-producing species found in Australia and is often fatal to grazing animals. The threat of introduction of the species into the United States led to its inclusion in the Federal Select Agent Program, which makes R. toxicus a highly regulated species. This work provides novel insights into the evolution of R. toxicus. R. toxicus is the only species in the genus to have acquired a CRISPR adaptive immune system to protect against bacteriophages. Results suggest that coexistence with the bacteriophage NCPPB3778 led to the massive shrinkage of the R. toxicus genome, species divergence, and the maintenance of low genetic diversity in extant bacterial groups. This work contributes to an understanding of the evolution and ecology of an agriculturally important species of bacteria.
format article
author Edward W. Davis
Javier F. Tabima
Alexandra J. Weisberg
Lucas Dantas Lopes
Michele S. Wiseman
Michael S. Wiseman
Tal Pupko
Michael S. Belcher
Aaron J. Sechler
Matt A. Tancos
Brenda K. Schroeder
Timothy D. Murray
Douglas G. Luster
William L. Schneider
Elizabeth E. Rogers
Fernando D. Andreote
Niklaus J. Grünwald
Melodie L. Putnam
Jeff H. Chang
author_facet Edward W. Davis
Javier F. Tabima
Alexandra J. Weisberg
Lucas Dantas Lopes
Michele S. Wiseman
Michael S. Wiseman
Tal Pupko
Michael S. Belcher
Aaron J. Sechler
Matt A. Tancos
Brenda K. Schroeder
Timothy D. Murray
Douglas G. Luster
William L. Schneider
Elizabeth E. Rogers
Fernando D. Andreote
Niklaus J. Grünwald
Melodie L. Putnam
Jeff H. Chang
author_sort Edward W. Davis
title Evolution of the U.S. Biological Select Agent <named-content content-type="genus-species">Rathayibacter toxicus</named-content>
title_short Evolution of the U.S. Biological Select Agent <named-content content-type="genus-species">Rathayibacter toxicus</named-content>
title_full Evolution of the U.S. Biological Select Agent <named-content content-type="genus-species">Rathayibacter toxicus</named-content>
title_fullStr Evolution of the U.S. Biological Select Agent <named-content content-type="genus-species">Rathayibacter toxicus</named-content>
title_full_unstemmed Evolution of the U.S. Biological Select Agent <named-content content-type="genus-species">Rathayibacter toxicus</named-content>
title_sort evolution of the u.s. biological select agent <named-content content-type="genus-species">rathayibacter toxicus</named-content>
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/6a8c1015c1894d8f9d68a3cb5fc24206
work_keys_str_mv AT edwardwdavis evolutionoftheusbiologicalselectagentnamedcontentcontenttypegenusspeciesrathayibactertoxicusnamedcontent
AT javierftabima evolutionoftheusbiologicalselectagentnamedcontentcontenttypegenusspeciesrathayibactertoxicusnamedcontent
AT alexandrajweisberg evolutionoftheusbiologicalselectagentnamedcontentcontenttypegenusspeciesrathayibactertoxicusnamedcontent
AT lucasdantaslopes evolutionoftheusbiologicalselectagentnamedcontentcontenttypegenusspeciesrathayibactertoxicusnamedcontent
AT micheleswiseman evolutionoftheusbiologicalselectagentnamedcontentcontenttypegenusspeciesrathayibactertoxicusnamedcontent
AT michaelswiseman evolutionoftheusbiologicalselectagentnamedcontentcontenttypegenusspeciesrathayibactertoxicusnamedcontent
AT talpupko evolutionoftheusbiologicalselectagentnamedcontentcontenttypegenusspeciesrathayibactertoxicusnamedcontent
AT michaelsbelcher evolutionoftheusbiologicalselectagentnamedcontentcontenttypegenusspeciesrathayibactertoxicusnamedcontent
AT aaronjsechler evolutionoftheusbiologicalselectagentnamedcontentcontenttypegenusspeciesrathayibactertoxicusnamedcontent
AT mattatancos evolutionoftheusbiologicalselectagentnamedcontentcontenttypegenusspeciesrathayibactertoxicusnamedcontent
AT brendakschroeder evolutionoftheusbiologicalselectagentnamedcontentcontenttypegenusspeciesrathayibactertoxicusnamedcontent
AT timothydmurray evolutionoftheusbiologicalselectagentnamedcontentcontenttypegenusspeciesrathayibactertoxicusnamedcontent
AT douglasgluster evolutionoftheusbiologicalselectagentnamedcontentcontenttypegenusspeciesrathayibactertoxicusnamedcontent
AT williamlschneider evolutionoftheusbiologicalselectagentnamedcontentcontenttypegenusspeciesrathayibactertoxicusnamedcontent
AT elizabetherogers evolutionoftheusbiologicalselectagentnamedcontentcontenttypegenusspeciesrathayibactertoxicusnamedcontent
AT fernandodandreote evolutionoftheusbiologicalselectagentnamedcontentcontenttypegenusspeciesrathayibactertoxicusnamedcontent
AT niklausjgrunwald evolutionoftheusbiologicalselectagentnamedcontentcontenttypegenusspeciesrathayibactertoxicusnamedcontent
AT melodielputnam evolutionoftheusbiologicalselectagentnamedcontentcontenttypegenusspeciesrathayibactertoxicusnamedcontent
AT jeffhchang evolutionoftheusbiologicalselectagentnamedcontentcontenttypegenusspeciesrathayibactertoxicusnamedcontent
_version_ 1718426971609759744