A Persisting Nontropical Focus of <named-content content-type="genus-species">Burkholderia pseudomallei</named-content> with Limited Genome Evolution over Five Decades

ABSTRACT Burkholderia pseudomallei is the causative agent of the high-mortality disease melioidosis. Although melioidosis is classified as a tropical disease, rare autochthonous cases have been reported from temperate climatic regions, with uncertainty as to whether B. pseudomallei is persistent in...

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Autores principales: Jessica R. Webb, Nicky Buller, Audrey Rachlin, Clayton Golledge, Derek S. Sarovich, Erin P. Price, Mark Mayo, Bart J. Currie
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Publicado: American Society for Microbiology 2020
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spelling oai:doaj.org-article:da89167fe3f84fe7ba0985dcbdbc2e862021-12-02T19:47:36ZA Persisting Nontropical Focus of <named-content content-type="genus-species">Burkholderia pseudomallei</named-content> with Limited Genome Evolution over Five Decades10.1128/mSystems.00726-202379-5077https://doaj.org/article/da89167fe3f84fe7ba0985dcbdbc2e862020-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.00726-20https://doaj.org/toc/2379-5077ABSTRACT Burkholderia pseudomallei is the causative agent of the high-mortality disease melioidosis. Although melioidosis is classified as a tropical disease, rare autochthonous cases have been reported from temperate climatic regions, with uncertainty as to whether B. pseudomallei is persistent in the local environment and whether specific genetic mechanisms facilitate the survival of B. pseudomallei outside the tropics. Sporadic cases of melioidosis occurred in a valley region (latitude 31.6°S) in southwest Western Australia, Australia, between 1966 and 1992. We report a new melioidosis cluster in the same region following high rainfall in January 2017. More than 20 animals died, and B. pseudomallei was isolated from four alpacas, a parrot, and three environmental samples taken from the farm where the alpacas resided. Epidemiological data and genomics revealed that two locations on the farm were the probable sources of the alpaca infections. We determined that B. pseudomallei isolates from the 2017 cluster belonged to sequence type 284 (ST-284), as did all isolates recovered from 1966 to 1992. Genomic analysis confirmed that the ST-284 isolates were clonal and contained conserved genomic islands and limited evidence of recombination. We identified protein-coding regions unique to these isolates that might influence the persistence of B. pseudomallei in this temperate region. We demonstrate the environmental persistence of B. pseudomallei in a temperate region for over 50 years, with limited genetic changes suggesting a latent state and with activation, potential aerosolization, and local dispersal following unusually high rainfall. IMPORTANCE Burkholderia pseudomallei is predominantly a tropical pathogen uncommonly found in the environment of temperate climatic regions. It is unclear if introduction into temperate regions is sporadic and temporary or if B. pseudomallei can persist in such environments. B. pseudomallei was identified in the environment of southwest Western Australia with melioidosis cases between 1966 and 1991. We report a new cluster with 23 animal fatalities in the same region from 2017, with B. pseudomallei again being recovered from the environment. Comparison of the isolates from the first and second clusters using genomics revealed a single sequence type, high clonality, and limited recombination, even though the time of recovery of the isolates spanned 51 years. This is a major contrast to the extensive genomic diversity seen in the tropics. Our data support the suggestion that B. pseudomallei has the ability to persist in nontropical environments, potentially in a latent state, and has the ability to activate following favorable conditions (rainfall) and then infect animals and humans.Jessica R. WebbNicky BullerAudrey RachlinClayton GolledgeDerek S. SarovichErin P. PriceMark MayoBart J. CurrieAmerican Society for MicrobiologyarticleBurkholderia pseudomalleiclonalitymelioidosisphylogeneticstemperate climateMicrobiologyQR1-502ENmSystems, Vol 5, Iss 6 (2020)
institution DOAJ
collection DOAJ
language EN
topic Burkholderia pseudomallei
clonality
melioidosis
phylogenetics
temperate climate
Microbiology
QR1-502
spellingShingle Burkholderia pseudomallei
clonality
melioidosis
phylogenetics
temperate climate
Microbiology
QR1-502
Jessica R. Webb
Nicky Buller
Audrey Rachlin
Clayton Golledge
Derek S. Sarovich
Erin P. Price
Mark Mayo
Bart J. Currie
A Persisting Nontropical Focus of <named-content content-type="genus-species">Burkholderia pseudomallei</named-content> with Limited Genome Evolution over Five Decades
description ABSTRACT Burkholderia pseudomallei is the causative agent of the high-mortality disease melioidosis. Although melioidosis is classified as a tropical disease, rare autochthonous cases have been reported from temperate climatic regions, with uncertainty as to whether B. pseudomallei is persistent in the local environment and whether specific genetic mechanisms facilitate the survival of B. pseudomallei outside the tropics. Sporadic cases of melioidosis occurred in a valley region (latitude 31.6°S) in southwest Western Australia, Australia, between 1966 and 1992. We report a new melioidosis cluster in the same region following high rainfall in January 2017. More than 20 animals died, and B. pseudomallei was isolated from four alpacas, a parrot, and three environmental samples taken from the farm where the alpacas resided. Epidemiological data and genomics revealed that two locations on the farm were the probable sources of the alpaca infections. We determined that B. pseudomallei isolates from the 2017 cluster belonged to sequence type 284 (ST-284), as did all isolates recovered from 1966 to 1992. Genomic analysis confirmed that the ST-284 isolates were clonal and contained conserved genomic islands and limited evidence of recombination. We identified protein-coding regions unique to these isolates that might influence the persistence of B. pseudomallei in this temperate region. We demonstrate the environmental persistence of B. pseudomallei in a temperate region for over 50 years, with limited genetic changes suggesting a latent state and with activation, potential aerosolization, and local dispersal following unusually high rainfall. IMPORTANCE Burkholderia pseudomallei is predominantly a tropical pathogen uncommonly found in the environment of temperate climatic regions. It is unclear if introduction into temperate regions is sporadic and temporary or if B. pseudomallei can persist in such environments. B. pseudomallei was identified in the environment of southwest Western Australia with melioidosis cases between 1966 and 1991. We report a new cluster with 23 animal fatalities in the same region from 2017, with B. pseudomallei again being recovered from the environment. Comparison of the isolates from the first and second clusters using genomics revealed a single sequence type, high clonality, and limited recombination, even though the time of recovery of the isolates spanned 51 years. This is a major contrast to the extensive genomic diversity seen in the tropics. Our data support the suggestion that B. pseudomallei has the ability to persist in nontropical environments, potentially in a latent state, and has the ability to activate following favorable conditions (rainfall) and then infect animals and humans.
format article
author Jessica R. Webb
Nicky Buller
Audrey Rachlin
Clayton Golledge
Derek S. Sarovich
Erin P. Price
Mark Mayo
Bart J. Currie
author_facet Jessica R. Webb
Nicky Buller
Audrey Rachlin
Clayton Golledge
Derek S. Sarovich
Erin P. Price
Mark Mayo
Bart J. Currie
author_sort Jessica R. Webb
title A Persisting Nontropical Focus of <named-content content-type="genus-species">Burkholderia pseudomallei</named-content> with Limited Genome Evolution over Five Decades
title_short A Persisting Nontropical Focus of <named-content content-type="genus-species">Burkholderia pseudomallei</named-content> with Limited Genome Evolution over Five Decades
title_full A Persisting Nontropical Focus of <named-content content-type="genus-species">Burkholderia pseudomallei</named-content> with Limited Genome Evolution over Five Decades
title_fullStr A Persisting Nontropical Focus of <named-content content-type="genus-species">Burkholderia pseudomallei</named-content> with Limited Genome Evolution over Five Decades
title_full_unstemmed A Persisting Nontropical Focus of <named-content content-type="genus-species">Burkholderia pseudomallei</named-content> with Limited Genome Evolution over Five Decades
title_sort persisting nontropical focus of <named-content content-type="genus-species">burkholderia pseudomallei</named-content> with limited genome evolution over five decades
publisher American Society for Microbiology
publishDate 2020
url https://doaj.org/article/da89167fe3f84fe7ba0985dcbdbc2e86
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