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Increased abundance of potentially pathogenic Vibrio and a marine heatwave co-occur with a Pacific Oyster summer mortality event

Increased abundance of potentially pathogenic Vibrio and a marine heatwave co-occur with a Pacific Oyster summer mortality event
Increased abundance of potentially pathogenic Vibrio and a marine heatwave co-occur with a Pacific Oyster summer mortality event

The Pacific Oyster (Crassostrea gigas) is an important aquaculture species, that has been globally affected by “summer mortality” outbreaks. The causes of summer mortality are often unclear, but several contributing factors have been implicated. To better understand the factors contributing to C. gigas summer mortality, we performed a 24 week experiment in tanks filled by a continuous flow of unfiltered surface seawater during a summer mortality high-risk period. Throughout this period, we measured a suite of environmental parameters, with weekly sampling to characterise the bacterial community composition, the abundance and diversity of the Vibrio genus, and the expression of oyster immune response genes. We observed three clear phases of oyster mortality: Phase 1 (day 0 to 75) was characterised by sporadic and low levels (mean < 1% per week) of oyster mortality; Phase 2 (day 82 to 119) involved constant levels of ongoing mortality (mean < 10% per week); and Phase 3 (day 125 to 161) involved a sharp increase in mortality (mean > 10% per week) reaching up to weekly mortality of 51%. The shift between phase 2 and 3 coincided with heavy rainfall and a marine heatwave (MHW) event at our study site, which lasted 13 days, when the average water temperature was elevated by 0.8 °C when compared to the weeks prior and following the MHW, and a maximum water temperature of 27.7 °C was reached. Oyster mortality was positively correlated with the occurrence of the MHW as well as bacterial and Vibrio abundance, and negatively correlated with seawater salinity that decreased from a salinity of 34.6 to 31.4 psu following rainfall events. In addition, the relative abundance of several Vibrio species, including V. campbellii, V. rotiferianus and V. owensii displayed positive correlations to oyster mortality. Shifts in the oyster-associated bacterial community and oyster immunity gene expression profiles occurred in parallel to increased mortality levels, with genes involved in the regulation of antimicrobial peptides (IkB1 and NF-kB p105) significantly over-expressed during high mortality. Overall, we observed a C. gigas mortality event that coincided with a marine heatwave, rainfall event and a shift in bacterial community composition. Our analyses provides further evidence for the putative role of Vibrio in summer mortality events.

Crassostrea gigas, Nanostring, Pacific Oyster, qPCR, Spirochaeata, Summer mortality, Vibrio
0044-8486
Siboni, Nachshon
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King, William L.
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Williams, Nathan L.R.
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Scanes, Elliot
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Giardina, Marco
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Green, Timothy J.
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Ostrowski, Martin
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O'Connor, Wayne
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Dove, Michael
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Labbate, Maurizio
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Seymour, Justin R.
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Siboni, Nachshon
cd5ba51e-896e-4b3f-be74-ab136fd96675
King, William L.
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Williams, Nathan L.R.
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Scanes, Elliot
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Giardina, Marco
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Green, Timothy J.
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Ostrowski, Martin
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O'Connor, Wayne
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Dove, Michael
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Labbate, Maurizio
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Seymour, Justin R.
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Siboni, Nachshon, King, William L., Williams, Nathan L.R., Scanes, Elliot, Giardina, Marco, Green, Timothy J., Ostrowski, Martin, O'Connor, Wayne, Dove, Michael, Labbate, Maurizio and Seymour, Justin R. (2024) Increased abundance of potentially pathogenic Vibrio and a marine heatwave co-occur with a Pacific Oyster summer mortality event. Aquaculture, 583, [740618]. (doi:10.1016/j.aquaculture.2024.740618).

Record type: Article

Abstract

The Pacific Oyster (Crassostrea gigas) is an important aquaculture species, that has been globally affected by “summer mortality” outbreaks. The causes of summer mortality are often unclear, but several contributing factors have been implicated. To better understand the factors contributing to C. gigas summer mortality, we performed a 24 week experiment in tanks filled by a continuous flow of unfiltered surface seawater during a summer mortality high-risk period. Throughout this period, we measured a suite of environmental parameters, with weekly sampling to characterise the bacterial community composition, the abundance and diversity of the Vibrio genus, and the expression of oyster immune response genes. We observed three clear phases of oyster mortality: Phase 1 (day 0 to 75) was characterised by sporadic and low levels (mean < 1% per week) of oyster mortality; Phase 2 (day 82 to 119) involved constant levels of ongoing mortality (mean < 10% per week); and Phase 3 (day 125 to 161) involved a sharp increase in mortality (mean > 10% per week) reaching up to weekly mortality of 51%. The shift between phase 2 and 3 coincided with heavy rainfall and a marine heatwave (MHW) event at our study site, which lasted 13 days, when the average water temperature was elevated by 0.8 °C when compared to the weeks prior and following the MHW, and a maximum water temperature of 27.7 °C was reached. Oyster mortality was positively correlated with the occurrence of the MHW as well as bacterial and Vibrio abundance, and negatively correlated with seawater salinity that decreased from a salinity of 34.6 to 31.4 psu following rainfall events. In addition, the relative abundance of several Vibrio species, including V. campbellii, V. rotiferianus and V. owensii displayed positive correlations to oyster mortality. Shifts in the oyster-associated bacterial community and oyster immunity gene expression profiles occurred in parallel to increased mortality levels, with genes involved in the regulation of antimicrobial peptides (IkB1 and NF-kB p105) significantly over-expressed during high mortality. Overall, we observed a C. gigas mortality event that coincided with a marine heatwave, rainfall event and a shift in bacterial community composition. Our analyses provides further evidence for the putative role of Vibrio in summer mortality events.

Text
AQUACULTURE-D-23-02137_R2 - Jan2024[2] - Accepted Manuscript
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SIMS oyster experiment_2024_final[1] - Other
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More information

Accepted/In Press date: 22 January 2024
e-pub ahead of print date: 24 January 2024
Published date: 29 January 2024
Additional Information: Funding Information: This research was supported by Australian Research Council Linkage Project ( LP160101795 ) and Discovery Project ( DP210101610 ) grants to JS and ML; a Cooperative Research Centre Project ( CRC-P 2016-805 ; Future Oysters), led by the Australian Seafood Industry Pty Ltd. in partnership with a number of Australian Research Organisations; and Ausgem, a research partnership initiated between the University of Technology Sydney and the New South Wales Department of Primary Industries.
Keywords: Crassostrea gigas, Nanostring, Pacific Oyster, qPCR, Spirochaeata, Summer mortality, Vibrio

Identifiers

Local EPrints ID: 487763
URI: http://eprints.soton.ac.uk/id/eprint/487763
ISSN: 0044-8486
PURE UUID: af10af4c-226e-4059-8ddb-7b1837f20cd5
ORCID for William L. King: ORCID iD orcid.org/0000-0001-7272-8242

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Date deposited: 04 Mar 2024 18:05
Last modified: 18 Mar 2024 04:18

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Contributors

Author: Nachshon Siboni
Author: William L. King ORCID iD
Author: Nathan L.R. Williams
Author: Elliot Scanes
Author: Marco Giardina
Author: Timothy J. Green
Author: Martin Ostrowski
Author: Wayne O'Connor
Author: Michael Dove
Author: Maurizio Labbate
Author: Justin R. Seymour

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