Exposure of the Opportunistic Marine Pathogen Photobacterium damselae subsp. damselae to Human Body Temperature Is a Stressful Condition That Shapes the Transcriptome, Viability, Cell Morphology, and Virulence

Photobacterium damselae subsp. damselae (Pdd), an important pathogen for marine animals, is also an opportunistic human pathogen that can cause fatal necrotizing fasciitis. The regulatory changes triggered by the temperature shift experienced by this marine pathogen upon entering the human body, are...

Descripción completa

Detalles Bibliográficos
Autores: Matanza Fente, José Manuel, Rodríguez Osorio, Carlos
Tipo de recurso: artículo
Fecha de publicación:2020
País:España
Institución:Universidad de Santiago de Compostela (USC)
Repositorio:Minerva. Repositorio Institucional de la Universidad de Santiago de Compostela
Idioma:inglés
OAI Identifier:oai:minerva.usc.gal:10347/23459
Acceso en línea:http://hdl.handle.net/10347/23459
Access Level:acceso abierto
id ES_97afbe358f21779bc4d2c8fcf3c8f2b0
oai_identifier_str oai:minerva.usc.gal:10347/23459
network_acronym_str ES
network_name_str España
repository_id_str
spelling Exposure of the Opportunistic Marine Pathogen Photobacterium damselae subsp. damselae to Human Body Temperature Is a Stressful Condition That Shapes the Transcriptome, Viability, Cell Morphology, and VirulenceMatanza Fente, José ManuelRodríguez Osorio, CarlosPhotobacterium damselae subsp. damselae (Pdd), an important pathogen for marine animals, is also an opportunistic human pathogen that can cause fatal necrotizing fasciitis. The regulatory changes triggered by the temperature shift experienced by this marine pathogen upon entering the human body, are completely unknown. Here we report an RNA-seq approach combined with phenotypical assays to study the response of Pdd to cultivation at 37°C in comparison to 25°C. We found that cultivation of a Pdd highly virulent strain for fish and mice, RM-71, at 37°C, initially enhanced bacterial growth in comparison to 25°C as evidenced by the increase in optical density. However, cells were found to undergo a progressive loss of viability after 6 h cultivation at 37°C, and no viable cells could be detected from 30 h cultures at 37°C. In contrast, at 25°C, viable cell counts achieved the highest values at 30 h cultivation. Cells grown at 25°C showed normal rod morphology by scanning electron microscopy analysis whereas cells grown at 37°C exhibited chain-like structures and aberrant long shapes suggesting a defect in daughter cell separation and in septum formation. Cells grown at 37°C also exhibited reduced tolerance to benzylpenicillin. Using a RNA-seq approach we discovered that growth at 37°C triggered a heat-shock response, whereas genes involved in motility and virulence were repressed including iron acquisition systems, the type two secretion system, and damselysin toxin, a major virulence factor of Pdd. Human isolates did not exhibit advantage growing at 37°C compared to fish isolates, and comparative genomics did not reveal gene markers specific of human isolates, suggesting that any Pdd genotype existing in the marine environment might potentially cause disease in humans. Altogether, these data indicate that the potential of Pdd to cause disease in humans is an accidental condition rather than a selected trait, and that human body temperature constitutes a stressful condition for Pdd. This study provides the first transcriptome profile of Pdd exposed at human body temperature, and unveils a number of candidate molecular targets for prevention and control of human infections caused by this pathogenFrontiersUniversidade de Santiago de Compostela. Departamento de Microbioloxía e ParasitoloxíaUniversidade de Santiago de Compostela. Instituto de Acuicultura20202020-01-0120202020-01-01journal articlehttp://purl.org/coar/resource_type/c_6501VoRhttp://purl.org/coar/version/c_970fb48d4fbd8a85info:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10347/23459reponame:Minerva. Repositorio Institucional de la Universidad de Santiago de Compostelainstname:Universidad de Santiago de Compostela (USC)Inglésengopen accesshttp://purl.org/coar/access_right/c_abf2Copyright © 2020 Matanza and Osorio. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these termshttp://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:minerva.usc.gal:10347/234592026-06-15T12:47:27Z
dc.title.none.fl_str_mv Exposure of the Opportunistic Marine Pathogen Photobacterium damselae subsp. damselae to Human Body Temperature Is a Stressful Condition That Shapes the Transcriptome, Viability, Cell Morphology, and Virulence
title Exposure of the Opportunistic Marine Pathogen Photobacterium damselae subsp. damselae to Human Body Temperature Is a Stressful Condition That Shapes the Transcriptome, Viability, Cell Morphology, and Virulence
spellingShingle Exposure of the Opportunistic Marine Pathogen Photobacterium damselae subsp. damselae to Human Body Temperature Is a Stressful Condition That Shapes the Transcriptome, Viability, Cell Morphology, and Virulence
Matanza Fente, José Manuel
title_short Exposure of the Opportunistic Marine Pathogen Photobacterium damselae subsp. damselae to Human Body Temperature Is a Stressful Condition That Shapes the Transcriptome, Viability, Cell Morphology, and Virulence
title_full Exposure of the Opportunistic Marine Pathogen Photobacterium damselae subsp. damselae to Human Body Temperature Is a Stressful Condition That Shapes the Transcriptome, Viability, Cell Morphology, and Virulence
title_fullStr Exposure of the Opportunistic Marine Pathogen Photobacterium damselae subsp. damselae to Human Body Temperature Is a Stressful Condition That Shapes the Transcriptome, Viability, Cell Morphology, and Virulence
title_full_unstemmed Exposure of the Opportunistic Marine Pathogen Photobacterium damselae subsp. damselae to Human Body Temperature Is a Stressful Condition That Shapes the Transcriptome, Viability, Cell Morphology, and Virulence
title_sort Exposure of the Opportunistic Marine Pathogen Photobacterium damselae subsp. damselae to Human Body Temperature Is a Stressful Condition That Shapes the Transcriptome, Viability, Cell Morphology, and Virulence
dc.creator.none.fl_str_mv Matanza Fente, José Manuel
Rodríguez Osorio, Carlos
author Matanza Fente, José Manuel
author_facet Matanza Fente, José Manuel
Rodríguez Osorio, Carlos
author_role author
author2 Rodríguez Osorio, Carlos
author2_role author
dc.contributor.none.fl_str_mv Universidade de Santiago de Compostela. Departamento de Microbioloxía e Parasitoloxía
Universidade de Santiago de Compostela. Instituto de Acuicultura
description Photobacterium damselae subsp. damselae (Pdd), an important pathogen for marine animals, is also an opportunistic human pathogen that can cause fatal necrotizing fasciitis. The regulatory changes triggered by the temperature shift experienced by this marine pathogen upon entering the human body, are completely unknown. Here we report an RNA-seq approach combined with phenotypical assays to study the response of Pdd to cultivation at 37°C in comparison to 25°C. We found that cultivation of a Pdd highly virulent strain for fish and mice, RM-71, at 37°C, initially enhanced bacterial growth in comparison to 25°C as evidenced by the increase in optical density. However, cells were found to undergo a progressive loss of viability after 6 h cultivation at 37°C, and no viable cells could be detected from 30 h cultures at 37°C. In contrast, at 25°C, viable cell counts achieved the highest values at 30 h cultivation. Cells grown at 25°C showed normal rod morphology by scanning electron microscopy analysis whereas cells grown at 37°C exhibited chain-like structures and aberrant long shapes suggesting a defect in daughter cell separation and in septum formation. Cells grown at 37°C also exhibited reduced tolerance to benzylpenicillin. Using a RNA-seq approach we discovered that growth at 37°C triggered a heat-shock response, whereas genes involved in motility and virulence were repressed including iron acquisition systems, the type two secretion system, and damselysin toxin, a major virulence factor of Pdd. Human isolates did not exhibit advantage growing at 37°C compared to fish isolates, and comparative genomics did not reveal gene markers specific of human isolates, suggesting that any Pdd genotype existing in the marine environment might potentially cause disease in humans. Altogether, these data indicate that the potential of Pdd to cause disease in humans is an accidental condition rather than a selected trait, and that human body temperature constitutes a stressful condition for Pdd. This study provides the first transcriptome profile of Pdd exposed at human body temperature, and unveils a number of candidate molecular targets for prevention and control of human infections caused by this pathogen
publishDate 2020
dc.date.none.fl_str_mv 2020
2020-01-01
2020
2020-01-01
dc.type.none.fl_str_mv journal article
http://purl.org/coar/resource_type/c_6501
VoR
http://purl.org/coar/version/c_970fb48d4fbd8a85
dc.type.openaire.fl_str_mv info:eu-repo/semantics/article
format article
dc.identifier.none.fl_str_mv http://hdl.handle.net/10347/23459
url http://hdl.handle.net/10347/23459
dc.language.none.fl_str_mv Inglés
eng
language_invalid_str_mv Inglés
language eng
dc.rights.none.fl_str_mv open access
http://purl.org/coar/access_right/c_abf2
http://creativecommons.org/licenses/by/4.0/
dc.rights.openaire.fl_str_mv info:eu-repo/semantics/openAccess
rights_invalid_str_mv open access
http://purl.org/coar/access_right/c_abf2
http://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv Frontiers
publisher.none.fl_str_mv Frontiers
dc.source.none.fl_str_mv reponame:Minerva. Repositorio Institucional de la Universidad de Santiago de Compostela
instname:Universidad de Santiago de Compostela (USC)
instname_str Universidad de Santiago de Compostela (USC)
reponame_str Minerva. Repositorio Institucional de la Universidad de Santiago de Compostela
collection Minerva. Repositorio Institucional de la Universidad de Santiago de Compostela
repository.name.fl_str_mv
repository.mail.fl_str_mv
_version_ 1869414099940540416
score 15,811543

Similares en LA Referencia