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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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2023-09-01
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| Series: | Frontiers in Microbiology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1236290/full |
| _version_ | 1797676863132270592 |
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| author | Snorre Gulla Duncan J. Colquhoun 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 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 |
| collection | DOAJ |
| 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 phocoena), and their relatively distant relationship with other members of the genus Pasteurella, suggests that both P. skyensis and “P. atlantica” should be moved to the genus Phocoenobacter. |
| first_indexed | 2024-03-11T22:36:35Z |
| format | Article |
| id | doaj.art-1963a81781fb421e9d8d73966d45d0a3 |
| institution | Directory Open Access Journal |
| issn | 1664-302X |
| language | English |
| last_indexed | 2024-03-11T22:36:35Z |
| publishDate | 2023-09-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Microbiology |
| spelling | doaj.art-1963a81781fb421e9d8d73966d45d0a32023-09-22T13:07:39ZengFrontiers Media S.A.Frontiers in Microbiology1664-302X2023-09-011410.3389/fmicb.2023.12362901236290Phylogeography and host specificity of Pasteurellaceae pathogenic to sea-farmed fish in the north-east AtlanticSnorre Gulla0Duncan J. Colquhoun1Duncan J. Colquhoun2Anne Berit Olsen3Bjørn Spilsberg4Karin Lagesen5Caroline P. Åkesson6Sverri Strøm7Farah Manji8Thomas H. Birkbeck9Hanne K. Nilsen10Norwegian Veterinary Institute, Ås, NorwayNorwegian Veterinary Institute, Ås, NorwayDepartment of Biological Sciences, University of Bergen, Bergen, NorwayNorwegian Veterinary Institute, Bergen, NorwayNorwegian Veterinary Institute, Ås, NorwayNorwegian Veterinary Institute, Ås, NorwayPharmaq Analytiq, Oslo, NorwayFoMAS – Fiskehelse og Miljø AS, Karmsund, NorwayMowi Norway AS, Bergen, NorwayDivision of Infection and Immunity, University of Glasgow, Glasgow, Scotland, United KingdomNorwegian Veterinary Institute, Bergen, NorwayThe 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 phocoena), and their relatively distant relationship with other members of the genus Pasteurella, suggests that both P. skyensis and “P. atlantica” should be moved to the genus Phocoenobacter.https://www.frontiersin.org/articles/10.3389/fmicb.2023.1236290/fullAtlantic salmon (Salmo salar)lumpfish (Cyclopterus lumpus)pasteurellosisPasteurellaceaePasteurella skyensis“Pasteurella atlantica” |
| spellingShingle | Snorre Gulla Duncan J. Colquhoun 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 Frontiers in Microbiology Atlantic salmon (Salmo salar) lumpfish (Cyclopterus lumpus) pasteurellosis Pasteurellaceae Pasteurella skyensis “Pasteurella atlantica” |
| title | 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_short | 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 |
| topic | Atlantic salmon (Salmo salar) lumpfish (Cyclopterus lumpus) pasteurellosis Pasteurellaceae Pasteurella skyensis “Pasteurella atlantica” |
| url | https://www.frontiersin.org/articles/10.3389/fmicb.2023.1236290/full |
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