The diversity, evolution and ecology of Salmonella in venomous snakes.


Journal

PLoS neglected tropical diseases
ISSN: 1935-2735
Titre abrégé: PLoS Negl Trop Dis
Pays: United States
ID NLM: 101291488

Informations de publication

Date de publication:
06 2019
Historique:
received: 17 01 2019
accepted: 08 05 2019
entrez: 5 6 2019
pubmed: 5 6 2019
medline: 28 11 2019
Statut: epublish

Résumé

Reptile-associated Salmonella bacteria are a major, but often neglected cause of both gastrointestinal and bloodstream infection in humans globally. The diversity of Salmonella enterica has not yet been determined in venomous snakes, however other ectothermic animals have been reported to carry a broad range of Salmonella bacteria. We investigated the prevalence and diversity of Salmonella in a collection of venomous snakes and non-venomous reptiles. We used a combination of selective enrichment techniques to establish a unique dataset of reptilian isolates to study Salmonella enterica species-level evolution and ecology and used whole-genome sequencing to investigate the relatedness of phylogenetic groups. We observed that 91% of venomous snakes carried Salmonella, and found that a diverse range of serovars (n = 58) were carried by reptiles. The Salmonella serovars belonged to four of the six Salmonella enterica subspecies: diarizonae, enterica, houtanae and salamae. Subspecies enterica isolates were distributed among two distinct phylogenetic clusters, previously described as clade A (52%) and clade B (48%). We identified metabolic differences between S. diarizonae, S. enterica clade A and clade B involving growth on lactose, tartaric acid, dulcitol, myo-inositol and allantoin. We present the first whole genome-based comparative study of the Salmonella bacteria that colonise venomous and non-venomous reptiles and shed new light on Salmonella evolution. Venomous snakes examined in this study carried a broad range of Salmonella, including serovars which have been associated with disease in humans such as S. Enteritidis. The findings raise the possibility that venomous snakes could be a reservoir for Salmonella serovars associated with human salmonellosis.

Sections du résumé

BACKGROUND
Reptile-associated Salmonella bacteria are a major, but often neglected cause of both gastrointestinal and bloodstream infection in humans globally. The diversity of Salmonella enterica has not yet been determined in venomous snakes, however other ectothermic animals have been reported to carry a broad range of Salmonella bacteria. We investigated the prevalence and diversity of Salmonella in a collection of venomous snakes and non-venomous reptiles.
METHODOLOGY/PRINCIPLE FINDINGS
We used a combination of selective enrichment techniques to establish a unique dataset of reptilian isolates to study Salmonella enterica species-level evolution and ecology and used whole-genome sequencing to investigate the relatedness of phylogenetic groups. We observed that 91% of venomous snakes carried Salmonella, and found that a diverse range of serovars (n = 58) were carried by reptiles. The Salmonella serovars belonged to four of the six Salmonella enterica subspecies: diarizonae, enterica, houtanae and salamae. Subspecies enterica isolates were distributed among two distinct phylogenetic clusters, previously described as clade A (52%) and clade B (48%). We identified metabolic differences between S. diarizonae, S. enterica clade A and clade B involving growth on lactose, tartaric acid, dulcitol, myo-inositol and allantoin.
SIGNIFICANCE
We present the first whole genome-based comparative study of the Salmonella bacteria that colonise venomous and non-venomous reptiles and shed new light on Salmonella evolution. Venomous snakes examined in this study carried a broad range of Salmonella, including serovars which have been associated with disease in humans such as S. Enteritidis. The findings raise the possibility that venomous snakes could be a reservoir for Salmonella serovars associated with human salmonellosis.

Identifiants

pubmed: 31163033
doi: 10.1371/journal.pntd.0007169
pii: PNTD-D-19-00040
pmc: PMC6548357
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e0007169

Subventions

Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/CSP17270/1
Pays : United Kingdom
Organisme : Biotechnology and Biological Sciences Research Council
ID : BB/L024209/1
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 106690/A/14/Z
Pays : United Kingdom
Organisme : Wellcome Trust
ID : 106914/Z/15/Z
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/L01839X/1
Pays : United Kingdom
Organisme : Wellcome Trust
Pays : United Kingdom

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

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Auteurs

Caisey V Pulford (CV)

Department of Functional and Comparative Genomics, Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom.

Nicolas Wenner (N)

Department of Functional and Comparative Genomics, Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom.

Martha L Redway (ML)

Department of Functional and Comparative Genomics, Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom.

Ella V Rodwell (EV)

Department of Functional and Comparative Genomics, Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom.

Hermione J Webster (HJ)

Department of Functional and Comparative Genomics, Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom.

Roberta Escudero (R)

Department of Functional and Comparative Genomics, Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom.

Carsten Kröger (C)

Department of Functional and Comparative Genomics, Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom.

Rocío Canals (R)

Department of Functional and Comparative Genomics, Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom.

Will Rowe (W)

Department of Functional and Comparative Genomics, Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom.

Javier Lopez (J)

Animal Health Department, Chester Zoo, Cheshire, United Kingdom.

Neil Hall (N)

Earlham Institute, Norwich Research Park, Norwich, United Kingdom.
School of Biological Sciences, University of East Anglia, Norwich, United Kingdom.

Paul D Rowley (PD)

Centre for Snakebite Research and Interventions, Liverpool School of Tropical Medicine, Liverpool, United Kingdom.

Dorina Timofte (D)

Institute of Veterinary Science, University of Liverpool, Leahurst Campus, Cheshire, United Kingdom.
Institute of Infection and Global Health, University of Liverpool, Liverpool, United Kingdom.

Robert A Harrison (RA)

Centre for Snakebite Research and Interventions, Liverpool School of Tropical Medicine, Liverpool, United Kingdom.

Kate S Baker (KS)

Department of Functional and Comparative Genomics, Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom.

Jay C D Hinton (JCD)

Department of Functional and Comparative Genomics, Institute of Integrative Biology, University of Liverpool, Liverpool, United Kingdom.

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