Phylogeography and host specificity of Pasteurellaceae pathogenic to sea-farmed fish in the north-east Atlantic

The present study was undertaken to address the recent spate of pasteurellosis outbreaks among sea-farmed Atlantic salmon (Salmo salar) in Norway and Scotland, coinciding with sporadic disease episodes in lumpfish (Cyclopterus lumpus) used for delousing purposes in salmon farms. Genome assemblies fr...

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Published in:Frontiers in Microbiology
Main Authors: Snorre Gulla, Duncan J. Colquhoun, Anne Berit Olsen, Bjørn Spilsberg, Karin Lagesen, Caroline P. Åkesson, Sverri Strøm, Farah Manji, Thomas H. Birkbeck, Hanne K. Nilsen
Format: Article in Journal/Newspaper
Language:English
Published: Frontiers Media S.A. 2023
Subjects:
Online Access:https://doi.org/10.3389/fmicb.2023.1236290
https://doaj.org/article/1963a81781fb421e9d8d73966d45d0a3
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spelling ftdoajarticles:oai:doaj.org/article:1963a81781fb421e9d8d73966d45d0a3 2023-10-09T21:49:57+02:00 Phylogeography and host specificity of Pasteurellaceae pathogenic to sea-farmed fish in the north-east Atlantic Snorre Gulla Duncan J. Colquhoun Anne Berit Olsen Bjørn Spilsberg Karin Lagesen Caroline P. Åkesson Sverri Strøm Farah Manji Thomas H. Birkbeck Hanne K. Nilsen 2023-09-01T00:00:00Z https://doi.org/10.3389/fmicb.2023.1236290 https://doaj.org/article/1963a81781fb421e9d8d73966d45d0a3 EN eng Frontiers Media S.A. https://www.frontiersin.org/articles/10.3389/fmicb.2023.1236290/full https://doaj.org/toc/1664-302X 1664-302X doi:10.3389/fmicb.2023.1236290 https://doaj.org/article/1963a81781fb421e9d8d73966d45d0a3 Frontiers in Microbiology, Vol 14 (2023) Atlantic salmon (Salmo salar) lumpfish (Cyclopterus lumpus) pasteurellosis Pasteurellaceae Pasteurella skyensis “Pasteurella atlantica” Microbiology QR1-502 article 2023 ftdoajarticles https://doi.org/10.3389/fmicb.2023.1236290 2023-09-24T00:34:50Z The present study was undertaken to address the recent spate of pasteurellosis outbreaks among sea-farmed Atlantic salmon (Salmo salar) in Norway and Scotland, coinciding with sporadic disease episodes in lumpfish (Cyclopterus lumpus) used for delousing purposes in salmon farms. Genome assemblies from 86 bacterial isolates cultured from diseased salmon or lumpfish confirmed them all as bona fide members of the Pasteurellaceae family, with phylogenetic reconstruction dividing them into two distinct branches sharing <88% average nucleotide identity. These branches therefore constitute two separate species, namely Pasteurella skyensis and the as-yet invalidly named “Pasteurella atlantica”. Both species further stratify into multiple discrete genomovars (gv.) and/or lineages, each being nearly or fully exclusive to a particular host, geographic region, and/or time period. Pasteurellosis in lumpfish is, irrespective of spatiotemporal origin, linked almost exclusively to the highly conserved “P. atlantica gv. cyclopteri” (Pac). In contrast, pasteurellosis in Norwegian sea-farmed salmon, dominated since the late-1980s by “P. atlantica gv. salmonicida” (Pas), first saw three specific lineages (Pas-1, -2, and -3) causing separate, geographically restricted, and short-lived outbreaks, before a fourth (Pas-4) emerged recently and became more widely disseminated. A similar situation involving P. skyensis (Ps) has apparently been unfolding in Scottish salmon farming since the mid-1990s, where two historic (Ps-1 and -2) and one contemporary (Ps-3) lineages have been recorded. While the epidemiology underlying all these outbreaks/epizootics remains unclear, repeated detection of 16S rRNA gene amplicons very closely related to P. skyensis and “P. atlantica” from at least five cetacean species worldwide raises the question as to whether marine mammals may play a part, possibly as reservoirs. In fact, the close relationship between the studied isolates and Phocoenobacter uteri associated with harbor porpoise (Phocoena ... Article in Journal/Newspaper Atlantic salmon North East Atlantic Norwegian Sea Salmo salar Directory of Open Access Journals: DOAJ Articles Norway Norwegian Sea Spate ENVELOPE(76.102,76.102,-69.418,-69.418) Frontiers in Microbiology 14
institution Open Polar
collection Directory of Open Access Journals: DOAJ Articles
op_collection_id ftdoajarticles
language English
topic Atlantic salmon (Salmo salar)
lumpfish (Cyclopterus lumpus)
pasteurellosis
Pasteurellaceae
Pasteurella skyensis
“Pasteurella atlantica”
Microbiology
QR1-502
spellingShingle Atlantic salmon (Salmo salar)
lumpfish (Cyclopterus lumpus)
pasteurellosis
Pasteurellaceae
Pasteurella skyensis
“Pasteurella atlantica”
Microbiology
QR1-502
Snorre Gulla
Duncan J. Colquhoun
Anne Berit Olsen
Bjørn Spilsberg
Karin Lagesen
Caroline P. Åkesson
Sverri Strøm
Farah Manji
Thomas H. Birkbeck
Hanne K. Nilsen
Phylogeography and host specificity of Pasteurellaceae pathogenic to sea-farmed fish in the north-east Atlantic
topic_facet Atlantic salmon (Salmo salar)
lumpfish (Cyclopterus lumpus)
pasteurellosis
Pasteurellaceae
Pasteurella skyensis
“Pasteurella atlantica”
Microbiology
QR1-502
description The present study was undertaken to address the recent spate of pasteurellosis outbreaks among sea-farmed Atlantic salmon (Salmo salar) in Norway and Scotland, coinciding with sporadic disease episodes in lumpfish (Cyclopterus lumpus) used for delousing purposes in salmon farms. Genome assemblies from 86 bacterial isolates cultured from diseased salmon or lumpfish confirmed them all as bona fide members of the Pasteurellaceae family, with phylogenetic reconstruction dividing them into two distinct branches sharing <88% average nucleotide identity. These branches therefore constitute two separate species, namely Pasteurella skyensis and the as-yet invalidly named “Pasteurella atlantica”. Both species further stratify into multiple discrete genomovars (gv.) and/or lineages, each being nearly or fully exclusive to a particular host, geographic region, and/or time period. Pasteurellosis in lumpfish is, irrespective of spatiotemporal origin, linked almost exclusively to the highly conserved “P. atlantica gv. cyclopteri” (Pac). In contrast, pasteurellosis in Norwegian sea-farmed salmon, dominated since the late-1980s by “P. atlantica gv. salmonicida” (Pas), first saw three specific lineages (Pas-1, -2, and -3) causing separate, geographically restricted, and short-lived outbreaks, before a fourth (Pas-4) emerged recently and became more widely disseminated. A similar situation involving P. skyensis (Ps) has apparently been unfolding in Scottish salmon farming since the mid-1990s, where two historic (Ps-1 and -2) and one contemporary (Ps-3) lineages have been recorded. While the epidemiology underlying all these outbreaks/epizootics remains unclear, repeated detection of 16S rRNA gene amplicons very closely related to P. skyensis and “P. atlantica” from at least five cetacean species worldwide raises the question as to whether marine mammals may play a part, possibly as reservoirs. In fact, the close relationship between the studied isolates and Phocoenobacter uteri associated with harbor porpoise (Phocoena ...
format Article in Journal/Newspaper
author Snorre Gulla
Duncan J. Colquhoun
Anne Berit Olsen
Bjørn Spilsberg
Karin Lagesen
Caroline P. Åkesson
Sverri Strøm
Farah Manji
Thomas H. Birkbeck
Hanne K. Nilsen
author_facet Snorre Gulla
Duncan J. Colquhoun
Anne Berit Olsen
Bjørn Spilsberg
Karin Lagesen
Caroline P. Åkesson
Sverri Strøm
Farah Manji
Thomas H. Birkbeck
Hanne K. Nilsen
author_sort Snorre Gulla
title Phylogeography and host specificity of Pasteurellaceae pathogenic to sea-farmed fish in the north-east Atlantic
title_short Phylogeography and host specificity of Pasteurellaceae pathogenic to sea-farmed fish in the north-east Atlantic
title_full Phylogeography and host specificity of Pasteurellaceae pathogenic to sea-farmed fish in the north-east Atlantic
title_fullStr Phylogeography and host specificity of Pasteurellaceae pathogenic to sea-farmed fish in the north-east Atlantic
title_full_unstemmed Phylogeography and host specificity of Pasteurellaceae pathogenic to sea-farmed fish in the north-east Atlantic
title_sort phylogeography and host specificity of pasteurellaceae pathogenic to sea-farmed fish in the north-east atlantic
publisher Frontiers Media S.A.
publishDate 2023
url https://doi.org/10.3389/fmicb.2023.1236290
https://doaj.org/article/1963a81781fb421e9d8d73966d45d0a3
long_lat ENVELOPE(76.102,76.102,-69.418,-69.418)
geographic Norway
Norwegian Sea
Spate
geographic_facet Norway
Norwegian Sea
Spate
genre Atlantic salmon
North East Atlantic
Norwegian Sea
Salmo salar
genre_facet Atlantic salmon
North East Atlantic
Norwegian Sea
Salmo salar
op_source Frontiers in Microbiology, Vol 14 (2023)
op_relation https://www.frontiersin.org/articles/10.3389/fmicb.2023.1236290/full
https://doaj.org/toc/1664-302X
1664-302X
doi:10.3389/fmicb.2023.1236290
https://doaj.org/article/1963a81781fb421e9d8d73966d45d0a3
op_doi https://doi.org/10.3389/fmicb.2023.1236290
container_title Frontiers in Microbiology
container_volume 14
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