Ongoing diversification of the global fish pathogen Piscirickettsia salmonis through genetic isolation and transposition bursts.


Journal

The ISME journal
ISSN: 1751-7370
Titre abrégé: ISME J
Pays: England
ID NLM: 101301086

Informations de publication

Date de publication:
Dec 2023
Historique:
received: 12 04 2023
accepted: 02 10 2023
revised: 28 09 2023
medline: 4 12 2023
pubmed: 19 10 2023
entrez: 18 10 2023
Statut: ppublish

Résumé

The management of bacterial pathogens remains a key challenge of aquaculture. The marine gammaproteobacterium Piscirickettsia salmonis is the etiological agent of piscirickettsiosis and causes multi-systemic infections in different salmon species, resulting in considerable mortality and substantial commercial losses. Here, we elucidate its global diversity, evolution, and selection during human interventions. Our comprehensive analysis of 73 closed, high quality genome sequences covered strains from major outbreaks and was supplemented by an analysis of all P. salmonis 16S rRNA gene sequences and metagenomic reads available in public databases. Genome comparison showed that Piscirickettsia comprises at least three distinct, genetically isolated species of which two showed evidence for continuing speciation. However, at least twice the number of species exist in marine fish or seawater. A hallmark of Piscirickettsia diversification is the unprecedented amount and diversity of transposases which are particularly active in subgroups undergoing rapid speciation and are key to the acquisition of novel genes and to pseudogenization. Several group-specific genes are involved in surface antigen synthesis and may explain the differences in virulence between strains. However, the frequent failure of antibiotic treatment of piscirickettsiosis outbreaks cannot be explained by horizontal acquisition of resistance genes which so far occurred only very rarely. Besides revealing a dynamic diversification of an important pathogen, our study also provides the data for improving its surveillance, predicting the emergence of novel lineages, and adapting aquaculture management, and thereby contributes towards the sustainability of salmon farming.

Identifiants

pubmed: 37853183
doi: 10.1038/s41396-023-01531-9
pii: 10.1038/s41396-023-01531-9
pmc: PMC10689435
doi:

Substances chimiques

RNA, Ribosomal, 16S 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

2247-2258

Informations de copyright

© 2023. The Author(s).

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Auteurs

Isabel Schober (I)

Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany.

Boyke Bunk (B)

Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany.

Gabriela Carril (G)

Laboratorio de Genética e Inmunología Molecular, Instituto de Biología, Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile.

Heike M Freese (HM)

Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany.

Nicolás Ojeda (N)

Laboratorio de Genética e Inmunología Molecular, Instituto de Biología, Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile.

Thomas Riedel (T)

Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany.
German Center for Infection Research (DZIF), Partner Site Braunschweig-Hannover, Braunschweig, Germany.

Jan P Meier-Kolthoff (JP)

Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany.

Markus Göker (M)

Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany.

Cathrin Spröer (C)

Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany.

Patricio A Flores-Herrera (PA)

Laboratorio de Genética e Inmunología Molecular, Instituto de Biología, Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile.

Guillermo Nourdin-Galindo (G)

Instituto de Bioquímica y Microbiología, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile.

Fernando Gómez (F)

Laboratorio de Genética e Inmunología Molecular, Instituto de Biología, Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile.

Constanza Cárdenas (C)

Laboratorio de Genética e Inmunología Molecular, Instituto de Biología, Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile.
Núcleo Biotecnología Curauma, Pontificia Universidad Católica de Valparaíso, Campus Curauma, Valparaíso, Chile.

Felipe Vásquez-Ponce (F)

Laboratorio de Genética e Inmunología Molecular, Instituto de Biología, Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile.

Alvaro Labra (A)

Laboratorio de Patógenos Acuícolas, Instituto de Biología, Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile.

Jaime Figueroa (J)

Instituto de Bioquímica y Microbiología, Facultad de Ciencias, Universidad Austral de Chile, Valdivia, Chile.

Jorge Olivares-Pacheco (J)

Laboratorio de Genética e Inmunología Molecular, Instituto de Biología, Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile.
Núcleo Milenio para la Investigación Colaborativa en Resistencia Antimicrobiana (MICROB-R), Santiago, Chile.

Ulrich Nübel (U)

Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany.
German Center for Infection Research (DZIF), Partner Site Braunschweig-Hannover, Braunschweig, Germany.
Institute of Microbiology, Technische Universität Braunschweig, Braunschweig, Germany.

Johannes Sikorski (J)

Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany.

Sergio H Marshall (SH)

Laboratorio de Genética e Inmunología Molecular, Instituto de Biología, Pontificia Universidad Católica de Valparaíso, Valparaíso, Chile.
Núcleo Biotecnología Curauma, Pontificia Universidad Católica de Valparaíso, Campus Curauma, Valparaíso, Chile.

Jörg Overmann (J)

Leibniz Institute DSMZ-German Collection of Microorganisms and Cell Cultures, Braunschweig, Germany. joerg.overmann@dsmz.de.
German Center for Infection Research (DZIF), Partner Site Braunschweig-Hannover, Braunschweig, Germany. joerg.overmann@dsmz.de.
Institute of Microbiology, Technische Universität Braunschweig, Braunschweig, Germany. joerg.overmann@dsmz.de.

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