Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE (Open Access)

Impact of seawater temperature on the Pacific oyster (Crassostrea gigas) microbiome and susceptibility to disease associated with Ostreid herpesvirus-1 (OsHV-1)

Erandi Pathirana https://orcid.org/0000-0002-1795-5423 A B , Richard J. Whittington A and Paul M. Hick A C *
+ Author Affiliations
- Author Affiliations

A Sydney School of Veterinary Science, Faculty of Science, The University of Sydney, Camden, NSW 2570, Australia.

B Present address: Department of Aquatic Bioresources, Faculty of Urban and Aquatic Bioresources, The University of Sri Jayewardenepura, Gangodawila, Nugegoda 10250, Sri Lanka.

C Present address: Elizabeth Macarthur Agricultural Institute, NSW Department of Primary Industries, Woodbridge Road, Menangle, NSW 2568, Australia.

* Correspondence to: paul.hick@dpi.nsw.gov.au

Handling Editor: Lucy Watt

Animal Production Science - https://doi.org/10.1071/AN21505
Submitted: 30 September 2021  Accepted: 9 March 2022   Published online: 26 May 2022

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context: Intertidal estuarine environments expose oysters to wide temperature variations. This can shift their microbiome composition towards pathogen-dominated communities. Understanding the impact of temperature on the microbiome will facilitate oyster health management.

Aims: The present study was conducted to (1) assess the Pacific oyster microbiome at different temperatures (21°C, 22°C, 26°C and diurnal fluctuation between 22°C and 26°C) and (2) investigate microbiome changes in response to exposure to the pathogen Ostreid herpesvirus-1 (OsHV-1) at different temperatures.

Methods: Pacific oysters (15 months of age; n = 480) were acclimated to different temperatures in laboratory aquaria. Samples were obtained before and after acclimation and after OsHV-1 exposure for quantification of OsHV-1, total bacteria and Vibrio, by quantitative PCR. Bacterial 16S rRNA gene (V1–V3) sequences were used to characterise the gill bacterial community.

Key results: The alpha diversity (number of observed amplicon sequence variants) and total number of bacteria associated with the gills of oysters did not change with acclimation to different water temperature profiles, but there was variation in beta diversity. The highest mortality after OsHV-1 exposure occurred at 26°C and these, together with oysters at 22/26°C, had a higher concentration of OsHV-1 DNA compared with to the ones at the lower constant temperatures (P < 0.05). The total bacterial quantity increased after the OsHV-1 challenge in oysters at 22/26°C. The alpha diversity of microbiota increased after the OsHV-1 challenge in oysters at 21°C and 22/26°C. The beta diversity changed both after acclimation and OsHV-1 challenge. The highest abundance of Vibrio and higher OsHV-1 loads were seen in OsHV-1-challenged oysters at 26°C (P < 0.05).

Conclusions: The gill microbiome altered with seawater temperature and OsHV-1 challenge. Higher mortality following OsHV-1 exposure was associated with a higher water temperature and greater abundance of Vibrio spp. arising from the microbiome.

Implications: Higher seawater temperature can be considered a key risk factor influencing oyster health by altering the microbiome, increasing susceptibility to OsHV-1 and increasing the Vibrio fraction in the oyster microbiome.

Keywords: Crassostrea gigas, estuarine, intertidal, microbiome, OsHV-1, Ostreid herpesvirus-1, Pacific oyster, temperature.


References

Adair KL, Douglas AE (2017) Making a microbiome: the many determinants of host-associated microbial community composition. Current Opinion in Microbiology 35, 23–29.
Making a microbiome: the many determinants of host-associated microbial community composition.Crossref | GoogleScholarGoogle Scholar | 27907842PubMed |

Aigle A, Prosser JI, Gubry-Rangin C (2019) The application of high-throughput sequencing technology to analysis of amoA phylogeny and environmental niche specialisation of terrestrial bacterial ammonia-oxidisers. Environmental Microbiome 14, 1–10.
The application of high-throughput sequencing technology to analysis of amoA phylogeny and environmental niche specialisation of terrestrial bacterial ammonia-oxidisers.Crossref | GoogleScholarGoogle Scholar |

Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. Available at http://www.bioinformatics.babraham.ac.uk/projects/fastqc/. [Accessed 17 August]

Azevedo C (1993) Occurrence of an unusual branchial mycoplasma-like infection in cockle Cerastoderma edule (Mollusca, Bivalvia). Diseases of Aquatic Organisms 16, 55–59.
Occurrence of an unusual branchial mycoplasma-like infection in cockle Cerastoderma edule (Mollusca, Bivalvia).Crossref | GoogleScholarGoogle Scholar |

Bokulich NA, Dillon MR, Bolyen E, Kaehler BD, Huttley GA, Caporaso JG (2018) q2-sample-classifier: machine-learning tools for microbiome classification and regression. Journal of Open Research Software 3, 934
q2-sample-classifier: machine-learning tools for microbiome classification and regression.Crossref | GoogleScholarGoogle Scholar | 31552137PubMed |

Bourlès Y, Alunno-Bruscia M, Pouvreau S, Tollu G, Leguay D, Arnaud C, Goulletquer P, Kooijman SALM (2009) Modelling growth and reproduction of the Pacific oyster Crassostrea gigas: advances in the oyster-DEB model through application to a coastal pond. Journal of Sea Research 62, 62–71.
Modelling growth and reproduction of the Pacific oyster Crassostrea gigas: advances in the oyster-DEB model through application to a coastal pond.Crossref | GoogleScholarGoogle Scholar |

Boutin S, Bernatchez L, Audet C, Derôme N (2013) Network analysis highlights complex interactions between pathogen, host and commensal microbiota. PLoS ONE 8, e84772
Network analysis highlights complex interactions between pathogen, host and commensal microbiota.Crossref | GoogleScholarGoogle Scholar | 24376845PubMed |

Burge CA, Mark Eakin C, Friedman CS, Froelich B, Hershberger PK, Hofmann EE, Petes LE, Prager KC, Weil E, Willis BL, Ford SE, Harvell CD (2014) Climate change influences on marine infectious diseases: implications for management and society. Annual Review of Marine Science 6, 249–277.
Climate change influences on marine infectious diseases: implications for management and society.Crossref | GoogleScholarGoogle Scholar | 23808894PubMed |

Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nature Methods 13, 581–583.
DADA2: high-resolution sample inference from Illumina amplicon data.Crossref | GoogleScholarGoogle Scholar | 27214047PubMed |

Cebrian E, Uriz MJ, Garrabou J, Ballesteros E (2011) Sponge mass mortalities in a warming Mediterranean Sea: are cyanobacteria-harboring species worse off? PLoS ONE 6, e20211
Sponge mass mortalities in a warming Mediterranean Sea: are cyanobacteria-harboring species worse off?Crossref | GoogleScholarGoogle Scholar | 21673798PubMed |

Clegg TA, Morrissey T, Geoghegan F, Martin SW, Lyons K, Ashe S, More SJ (2014) Risk factors associated with increased mortality of farmed Pacific oysters in Ireland during 2011. Preventive Veterinary Medicine 113, 257–267.
Risk factors associated with increased mortality of farmed Pacific oysters in Ireland during 2011.Crossref | GoogleScholarGoogle Scholar | 24290496PubMed |

Dacey DP, Chain FJJ (2021) Concatenation of paired-end reads improves taxonomic classification of amplicons for profiling microbial communities. BMC Bioinformatics 22, 1–25.
Concatenation of paired-end reads improves taxonomic classification of amplicons for profiling microbial communities.Crossref | GoogleScholarGoogle Scholar |

de Kantzow M, Hick P, Becker JA, Whittington RJ (2016) Effect of water temperature on mortality of Pacific oysters Crassostrea gigas associated with microvariant Ostreid herpesvirus 1 (OsHV-1 μVar). Aquaculture Environment Interactions 8, 419–428.
Effect of water temperature on mortality of Pacific oysters Crassostrea gigas associated with microvariant Ostreid herpesvirus 1 (OsHV-1 μVar).Crossref | GoogleScholarGoogle Scholar |

de Kantzow MC, Hick PM, Dhand NK, Whittington RJ (2017) Risk factors for mortality during the first occurrence of Pacific Oyster Mortality Syndrome due to Ostreid herpesvirus-1 in Tasmania, 2016. Aquaculture 468, 328–336.
Risk factors for mortality during the first occurrence of Pacific Oyster Mortality Syndrome due to Ostreid herpesvirus-1 in Tasmania, 2016.Crossref | GoogleScholarGoogle Scholar |

de Lorgeril J, Lucasson A, Petton B, et al. (2018) Immune-suppression by OsHV-1 viral infection causes fatal bacteraemia in Pacific oysters. Nature Communications 9, 4215
Immune-suppression by OsHV-1 viral infection causes fatal bacteraemia in Pacific oysters.Crossref | GoogleScholarGoogle Scholar | 30310074PubMed |

Delisle L, Petton B, Burguin JF, Morga B, Corporeau C, Pernet F (2018) Temperature modulate disease susceptibility of the Pacific oyster Crassostrea gigas and virulence of the Ostreid herpesvirus type 1. Fish & Shellfish Immunology 80, 71–79.
Temperature modulate disease susceptibility of the Pacific oyster Crassostrea gigas and virulence of the Ostreid herpesvirus type 1.Crossref | GoogleScholarGoogle Scholar |

Erwin PM, Pita L, López-Legentil S, Turon X (2012) Stability of sponge-associated bacteria over large seasonal shifts in temperature and irradiance. Applied and Environmental Microbiology 78, 7358–7368.
Stability of sponge-associated bacteria over large seasonal shifts in temperature and irradiance.Crossref | GoogleScholarGoogle Scholar | 22885741PubMed |

Evans O, Hick P, Dhand N, Whittington RJ (2015) Transmission of Ostreid herpesvirus-1 in Crassostrea gigas by cohabitation: effects of food and number of infected donor oysters. Aquaculture Environment Interactions 7, 281–295.
Transmission of Ostreid herpesvirus-1 in Crassostrea gigas by cohabitation: effects of food and number of infected donor oysters.Crossref | GoogleScholarGoogle Scholar |

Evans O, Kan JZF, Pathirana E, Whittington RJ, Dhand N, Hick P (2019) Effect of emersion on the mortality of Pacific oysters (Crassostrea gigas) infected with Ostreid herpesvirus-1 (OsHV-1). Aquaculture 505, 157–166.
Effect of emersion on the mortality of Pacific oysters (Crassostrea gigas) infected with Ostreid herpesvirus-1 (OsHV-1).Crossref | GoogleScholarGoogle Scholar |

Fernandez-Piquer J, Bowman JP, Ross T, Tamplin ML (2012) Molecular analysis of the bacterial communities in the live Pacific oyster (Crassostrea gigas) and the influence of postharvest temperature on its structure. Journal of Applied Microbiology 112, 1134–1143.
Molecular analysis of the bacterial communities in the live Pacific oyster (Crassostrea gigas) and the influence of postharvest temperature on its structure.Crossref | GoogleScholarGoogle Scholar | 22429335PubMed |

Flores-Higuera FA, Luis-Villaseñor IE, Rochin-Arenas JA, Gómez-Gil B, Mazón-Suástegui JM, Voltolina D, Medina-Hernández D (2019) Effect of pH on the bacterial community present in larvae and spat of Crassostrea gigas. Latin American Journal of Aquatic Research 47, 513–523.

Garcia C, Thébault A, Dégremont L, Arzul I, Miossec L, Robert M, Chollet B, François C, Joly J-P, Ferrand S, Kerdudou N, Renault T (2011) Ostreid herpesvirus 1 detection and relationship with Crassostrea gigas spat mortality in France between 1998 and 2006. Veterinary Research 42, 73
Ostreid herpesvirus 1 detection and relationship with Crassostrea gigas spat mortality in France between 1998 and 2006.Crossref | GoogleScholarGoogle Scholar | 21635731PubMed |

Garnier M, Labreuche Y, Garcia C, Robert M, Nicolas J-L (2007) Evidence for the involvement of pathogenic bacteria in summer mortalities of the Pacific oyster Crassostrea gigas. Microbial Ecology 53, 187–196.
Evidence for the involvement of pathogenic bacteria in summer mortalities of the Pacific oyster Crassostrea gigas.Crossref | GoogleScholarGoogle Scholar | 17245611PubMed |

Go J, Deutscher AT, Spiers ZB, Dahle K, Kirkland PD, Jenkins C (2017) Mass mortalities of unknown aetiology in Pacific oysters Crassostrea gigas in Port Stephens, New South Wales, Australia. Diseases of Aquatic Organisms 125, 227–242.
Mass mortalities of unknown aetiology in Pacific oysters Crassostrea gigas in Port Stephens, New South Wales, Australia.Crossref | GoogleScholarGoogle Scholar | 28792421PubMed |

Green TJ, Barnes AC (2010) Bacterial diversity of the digestive gland of Sydney rock oysters, Saccostrea glomerata infected with the paramyxean parasite, Marteilia sydneyi. Journal of Applied Microbiology 109, 613–622.
Bacterial diversity of the digestive gland of Sydney rock oysters, Saccostrea glomerata infected with the paramyxean parasite, Marteilia sydneyi.Crossref | GoogleScholarGoogle Scholar | 20202017PubMed |

Green TJ, Montagnani C, Benkendorff K, Robinson N, Speck P (2014) Ontogeny and water temperature influences the antiviral response of the Pacific oyster, Crassostrea gigas. Fish & Shellfish Immunology 36, 151–157.
Ontogeny and water temperature influences the antiviral response of the Pacific oyster, Crassostrea gigas.Crossref | GoogleScholarGoogle Scholar |

Green TJ, Siboni N, King WL, Labbate M, Seymour JR, Raftos D (2019) Simulated marine heat wave alters abundance and structure of Vibrio populations associated with the Pacific oyster resulting in a mass mortality event. Microbial Ecology 77, 736–747.
Simulated marine heat wave alters abundance and structure of Vibrio populations associated with the Pacific oyster resulting in a mass mortality event.Crossref | GoogleScholarGoogle Scholar | 30097682PubMed |

Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296, 2158–2162.
Climate warming and disease risks for terrestrial and marine biota.Crossref | GoogleScholarGoogle Scholar | 12077394PubMed |

Hernandez-Zarate G, Olmos-Soto J (2006) Identification of bacterial diversity in the oyster Crassostrea gigas by fluorescent in situ hybridization and polymerase chain reaction. Journal of Applied Microbiology 100, 664–672.
Identification of bacterial diversity in the oyster Crassostrea gigas by fluorescent in situ hybridization and polymerase chain reaction.Crossref | GoogleScholarGoogle Scholar | 16553721PubMed |

King GM, Judd C, Kuske CR, Smith C (2012) Analysis of stomach and gut microbiomes of the eastern oyster (Crassostrea virginica) from coastal Louisiana, USA. PLoS ONE 7, e51475
Analysis of stomach and gut microbiomes of the eastern oyster (Crassostrea virginica) from coastal Louisiana, USA.Crossref | GoogleScholarGoogle Scholar | 23251548PubMed |

King WL, Jenkins C, Go J, Siboni N, Seymour JR, Labbate M (2019a) Characterisation of the Pacific oyster microbiome during a summer mortality event. Microbial Ecology 77, 502–512.
Characterisation of the Pacific oyster microbiome during a summer mortality event.Crossref | GoogleScholarGoogle Scholar | 29987529PubMed |

King WL, Jenkins C, Seymour JR, Labbate M (2019b) Oyster disease in a changing environment: decrypting the link between pathogen, microbiome and environment. Marine Environmental Research 143, 124–140.
Oyster disease in a changing environment: decrypting the link between pathogen, microbiome and environment.Crossref | GoogleScholarGoogle Scholar | 30482397PubMed |

Kirchhoff H, Beyene P, Fischer M, Flossdorf J, Heitmann J, Khattab B, Lopatta D, Rosengarten R, Seidel G, Yousef C (1987) Mycoplasma mobile sp. nov., a new species from fish. International Journal of Systematic and Evolutionary Microbiology 37, 192–197.
Mycoplasma mobile sp. nov., a new species from fish.Crossref | GoogleScholarGoogle Scholar |

Krol RM, Hawkins WE, Overstreet RM (1991) Rickettsial and mollicute infections in hepatopancreatic cells of cultured Pacific white shrimp (Penaeus vannamei). Journal of Invertebrate Pathology 57, 362–370.
Rickettsial and mollicute infections in hepatopancreatic cells of cultured Pacific white shrimp (Penaeus vannamei).Crossref | GoogleScholarGoogle Scholar | 2066576PubMed |

Lane DJ (1991) 16S/23S rRNA sequencing. In ‘Nucleic acid techniques in bacterial systematics’. (Eds E Stackebrandt, M Goodfellow) pp. 115–175. (John Wiley and Sons: New York, NY, USA)

Lasa A, di Cesare A, Tassistro G, Borello A, Gualdi S, Furones D, Carrasco N, Cheslett D, Brechon A, Paillard C, Bidault A, Pernet F, Canesi L, Edomi P, Pallavicini A, Pruzzo C, Vezzulli L (2019) Dynamics of the Pacific oyster pathobiota during mortality episodes in Europe assessed by 16S rRNA gene profiling and a new target enrichment next-generation sequencing strategy. Environmental Microbiology 21, 4548–4562.
Dynamics of the Pacific oyster pathobiota during mortality episodes in Europe assessed by 16S rRNA gene profiling and a new target enrichment next-generation sequencing strategy.Crossref | GoogleScholarGoogle Scholar | 31325353PubMed |

Le Roux F, Wegner KM, Polz MF (2016) Oysters and vibrios as a model for disease dynamics in wild animals. Trends in Microbiology 24, 568–580.
Oysters and vibrios as a model for disease dynamics in wild animals.Crossref | GoogleScholarGoogle Scholar | 27038736PubMed |

Ley RE, Lozupone CA, Hamady M, Knight R, Gordon JI (2008) Worlds within worlds: evolution of the vertebrate gut microbiota. Nature Reviews Microbiology 6, 776–788.
Worlds within worlds: evolution of the vertebrate gut microbiota.Crossref | GoogleScholarGoogle Scholar | 18794915PubMed |

Lokmer A, Wegner KM (2015) Hemolymph microbiome of Pacific oysters in response to temperature, temperature stress and infection. The ISME Journal 9, 670–682.
Hemolymph microbiome of Pacific oysters in response to temperature, temperature stress and infection.Crossref | GoogleScholarGoogle Scholar | 25180968PubMed |

Lokmer A, Kuenzel S, Baines JF, Wegner KM (2016a) The role of tissue-specific microbiota in initial establishment success of Pacific oysters. Environmental Microbiology 18, 970–987.
The role of tissue-specific microbiota in initial establishment success of Pacific oysters.Crossref | GoogleScholarGoogle Scholar | 26695476PubMed |

Lokmer A, Goedknegt MA, Thieltges DW, Fiorentino D, Kuenzel S, Baines JF, Wegner KM (2016b) Spatial and temporal dynamics of Pacific oyster hemolymph microbiota across multiple scales. Frontiers in Microbiology 7, 1367
Spatial and temporal dynamics of Pacific oyster hemolymph microbiota across multiple scales.Crossref | GoogleScholarGoogle Scholar | 27630625PubMed |

Maldonado M, Sánchez-Tocino L, Navarro C (2010) Recurrent disease outbreaks in corneous demosponges of the genus Ircinia: epidemic incidence and defense mechanisms. Marine Biology 157, 1577–1590.
Recurrent disease outbreaks in corneous demosponges of the genus Ircinia: epidemic incidence and defense mechanisms.Crossref | GoogleScholarGoogle Scholar |

Mancuso FP, D’Hondt S, Willems A, Airoldi L, De Clerck O (2016) Diversity and temporal dynamics of the epiphytic bacterial communities associated with the canopy-forming seaweed Cystoseira compressa (Esper) Gerloff and Nizamuddin. Frontiers in Microbiology 7, 476
Diversity and temporal dynamics of the epiphytic bacterial communities associated with the canopy-forming seaweed Cystoseira compressa (Esper) Gerloff and Nizamuddin.Crossref | GoogleScholarGoogle Scholar | 27092130PubMed |

Martenot C, Oden E, Travaillé E, Malas JP, Houssin M (2010) Comparison of two real-time PCR methods for detection of ostreid herpesvirus 1 in the Pacific oyster Crassostrea gigas. Journal of Virological Methods 170, 86–89.

McDonald D, Price MN, Goodrich J, Nawrocki EP, DeSantis TZ, Probst A, Andersen GL, Knight R, Hugenholtz P (2012) An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea. The ISME Journal 6, 610–618.
An improved Greengenes taxonomy with explicit ranks for ecological and evolutionary analyses of bacteria and archaea.Crossref | GoogleScholarGoogle Scholar | 22134646PubMed |

Meyer JL, Gunasekera SP, Scott RM, Paul VJ, Teplitski M (2016) Microbiome shifts and the inhibition of quorum sensing by Black Band Disease cyanobacteria. The ISME Journal 10, 1204–1216.
Microbiome shifts and the inhibition of quorum sensing by Black Band Disease cyanobacteria.Crossref | GoogleScholarGoogle Scholar | 26495995PubMed |

Nadkarni MA, Martin FE, Jacques NA, Hunter N (2002) Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology 148, 257–266.
Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set.Crossref | GoogleScholarGoogle Scholar | 11782518PubMed |

Paillard C, Le Roux F, Borrego JJ (2004) Bacterial disease in marine bivalves, a review of recent studies: trends and evolution. Aquatic Living Resources 17, 477–498.
Bacterial disease in marine bivalves, a review of recent studies: trends and evolution.Crossref | GoogleScholarGoogle Scholar |

Pathirana E, McPherson A, Whittington R, Hick P (2019a) The role of tissue type, sampling and nucleic acid purification methodology on the inferred composition of Pacific oyster (Crassostrea gigas) Microbiome. Journal of Applied Microbiology 127, 429–444.
The role of tissue type, sampling and nucleic acid purification methodology on the inferred composition of Pacific oyster (Crassostrea gigas) Microbiome.Crossref | GoogleScholarGoogle Scholar | 31102430PubMed |

Pathirana E, Fuhrmann M, Whittington R, Hick P (2019b) Influence of environment on the pathogenesis of Ostreid herpesvirus-1 (OsHV-1) infections in Pacific oysters (Crassostrea gigas) through differential microbiome responses. Heliyon 5, e02101
Influence of environment on the pathogenesis of Ostreid herpesvirus-1 (OsHV-1) infections in Pacific oysters (Crassostrea gigas) through differential microbiome responses.Crossref | GoogleScholarGoogle Scholar | 31372553PubMed |

Paul-Pont I, Dhand NK, Whittington RJ (2013) Influence of husbandry practices on OsHV-1 associated mortality of Pacific oysters Crassostrea gigas. Aquaculture 412-413, 202–214.
Influence of husbandry practices on OsHV-1 associated mortality of Pacific oysters Crassostrea gigas.Crossref | GoogleScholarGoogle Scholar |

Paul-Pont I, Evans O, Dhand NK, Rubio A, Coad P, Whittington RJ (2014) Descriptive epidemiology of mass mortality due to Ostreid herpesvirus-1 (OsHV-1) in commercially farmed Pacific oysters (Crassostrea gigas) in the Hawkesbury River estuary, Australia. Aquaculture 422–423, 146–159.
Descriptive epidemiology of mass mortality due to Ostreid herpesvirus-1 (OsHV-1) in commercially farmed Pacific oysters (Crassostrea gigas) in the Hawkesbury River estuary, Australia.Crossref | GoogleScholarGoogle Scholar |

Pernet F, Barret J, Le Gall P, Corporeau C, Dégremont L, Lagarde F, Pépin J-F, Keck N (2012) Mass mortalities of Pacific oysters Crassostrea gigas reflect infectious diseases and vary with farming practices in the Mediterranean Thau lagoon, France. Aquaculture Environment Interactions 2, 215–237.
Mass mortalities of Pacific oysters Crassostrea gigas reflect infectious diseases and vary with farming practices in the Mediterranean Thau lagoon, France.Crossref | GoogleScholarGoogle Scholar |

Petton B, Pernet F, Robert R, Boudry P (2013) Temperature influence on pathogen transmission and subsequent mortalities in juvenile Pacific oysters Crassostrea gigas. Aquaculture Environment Interactions 3, 257–273.
Temperature influence on pathogen transmission and subsequent mortalities in juvenile Pacific oysters Crassostrea gigas.Crossref | GoogleScholarGoogle Scholar |

Petton B, Boudry P, Alunno-Bruscia M, Pernet F (2015) Factors influencing disease-induced mortality of Pacific oysters Crassostrea gigas. Aquaculture Environment Interactions 6, 205–222.
Factors influencing disease-induced mortality of Pacific oysters Crassostrea gigas.Crossref | GoogleScholarGoogle Scholar |

Petton B, de Lorgeril J, Mitta G, Daigle G, Pernet F, Alunno-Bruscia M (2019) Fine-scale temporal dynamics of herpes virus and vibrios in seawater during a polymicrobial infection in the Pacific oyster Crassostrea gigas. Diseases of Aquatic Organisms 135, 97–106.
Fine-scale temporal dynamics of herpes virus and vibrios in seawater during a polymicrobial infection in the Pacific oyster Crassostrea gigas.Crossref | GoogleScholarGoogle Scholar | 31342911PubMed |

Renault T, Bouquet AL, Maurice J-T, Lupo C, Blachier P (2014) Ostreid herpesvirus 1 infection among Pacific oyster (Crassostrea gigas) spat: relevance of water temperature to virus replication and circulation prior to the onset of mortality. Applied and Environmental Microbiology 80, 5419–5426.
Ostreid herpesvirus 1 infection among Pacific oyster (Crassostrea gigas) spat: relevance of water temperature to virus replication and circulation prior to the onset of mortality.Crossref | GoogleScholarGoogle Scholar | 24973071PubMed |

Rideout JR, Chase JH, Bolyen E, Ackermann G, González A, Knight R, Caporaso JG (2016) Keemei: cloud-based validation of tabular bioinformatics file formats in Google Sheets. GigaScience 5, s13742-016-0133-6
Keemei: cloud-based validation of tabular bioinformatics file formats in Google Sheets.Crossref | GoogleScholarGoogle Scholar |

Roterman YR, Benayahu Y, Reshef L, Gophna U (2015) The gill microbiota of invasive and indigenous Spondylus oysters from the Mediterranean Sea and northern Red Sea. Environmental Microbiology Reports 7, 860–867.
The gill microbiota of invasive and indigenous Spondylus oysters from the Mediterranean Sea and northern Red Sea.Crossref | GoogleScholarGoogle Scholar | 26111733PubMed |

Shade A, Gregory Caporaso J, Handelsman J, Knight R, Fierer N (2013) A meta-analysis of changes in bacterial and archaeal communities with time. The ISME Journal 7, 1493–1506.
A meta-analysis of changes in bacterial and archaeal communities with time.Crossref | GoogleScholarGoogle Scholar | 23575374PubMed |

Soletchnik P, Ropert M, Mazurié J, Gildas Fleury P, Le Coz F (2007) Relationships between oyster mortality patterns and environmental data from monitoring databases along the coasts of France. Aquaculture 271, 384–400.
Relationships between oyster mortality patterns and environmental data from monitoring databases along the coasts of France.Crossref | GoogleScholarGoogle Scholar |

Trabal N, Mazón-Suástegui JM, Vázquez-Juárez R, Asencio-Valle F, Morales-Bojórquez E, Romero J (2012) Molecular analysis of bacterial microbiota associated with oysters (Crassostrea gigas and Crassostrea corteziensis) in different growth phases at two cultivation sites. Microbial Ecology 64, 555–569.
Molecular analysis of bacterial microbiota associated with oysters (Crassostrea gigas and Crassostrea corteziensis) in different growth phases at two cultivation sites.Crossref | GoogleScholarGoogle Scholar | 22450510PubMed |

Travers M-A, Boettcher Miller K, Roque A, Friedman CS (2015) Bacterial diseases in marine bivalves. Journal of Invertebrate Pathology 131, 11–31.
Bacterial diseases in marine bivalves.Crossref | GoogleScholarGoogle Scholar | 26210496PubMed |

Vandamme P, De Ley J (1991) Proposal for a new family, Campylobacteraceae. International Journal of Systematic and Evolutionary Microbiology 41, 451–455.
Proposal for a new family, Campylobacteraceae.Crossref | GoogleScholarGoogle Scholar |

Vezzulli L, Brettar I, Pezzati E, Reid PC, Colwell RR, Höfle MG, Pruzzo C (2012) Long-term effects of ocean warming on the prokaryotic community: evidence from the vibrios. ISME Journal 6, 21–30.
Long-term effects of ocean warming on the prokaryotic community: evidence from the vibrios.Crossref | GoogleScholarGoogle Scholar | 21753799PubMed |

Vezzulli L, Pezzati E, Stauder M, Stagnaro L, Venier P, Pruzzo C (2015) Aquatic ecology of the oyster pathogens Vibrio splendidus and Vibrio aestuarianus. Environmental Microbiology 17, 1065–1080.
Aquatic ecology of the oyster pathogens Vibrio splendidus and Vibrio aestuarianus.Crossref | GoogleScholarGoogle Scholar | 24725454PubMed |

Wegner KM, Volkenborn N, Peter H, Eiler A (2013) Disturbance induced decoupling between host genetics and composition of the associated microbiome. BMC Microbiology 13, 252
Disturbance induced decoupling between host genetics and composition of the associated microbiome.Crossref | GoogleScholarGoogle Scholar | 24206899PubMed |

Whittington RJ, Dhand NK, Evans O, Paul-Pont I (2015) Further observations on the influence of husbandry practices on OsHV-1 μVar mortality in Pacific oysters Crassostrea gigas: age, cultivation structures and growing height. Aquaculture 438, 82–97.
Further observations on the influence of husbandry practices on OsHV-1 μVar mortality in Pacific oysters Crassostrea gigas: age, cultivation structures and growing height.Crossref | GoogleScholarGoogle Scholar |

Whittington RJ, Liu O, Hick PM, Dhand N, Rubio A (2019) Long-term temporal and spatial patterns of Ostreid herpesvirus 1 (OsHV-1) infection and mortality in sentinel Pacific oyster spat (Crassostrea gigas) inform farm management. Aquaculture 513, 734395
Long-term temporal and spatial patterns of Ostreid herpesvirus 1 (OsHV-1) infection and mortality in sentinel Pacific oyster spat (Crassostrea gigas) inform farm management.Crossref | GoogleScholarGoogle Scholar |

Yatsunenko T, Rey FE, Manary MJ, et al. (2012) Human gut microbiome viewed across age and geography. Nature 486, 222–227.
Human gut microbiome viewed across age and geography.Crossref | GoogleScholarGoogle Scholar | 22699611PubMed |

Zwietering MH, De Wit JC, Cuppers HGAM, Van’t Riet K (1994) Modeling of bacterial growth with shifts in temperature. Applied and Environmental Microbiology 60, 204–213.
Modeling of bacterial growth with shifts in temperature.Crossref | GoogleScholarGoogle Scholar | 16349151PubMed |