Host-microbiota interactions shed light on mortality events in the striped venus clam Chamelea gallina.
bivalve
host-microbiota interactions
mass mortality
molluscs
pollutant-pathogen interactions
transcriptomics
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
10 2019
10 2019
Historique:
received:
29
10
2018
revised:
19
07
2019
accepted:
05
08
2019
pubmed:
5
9
2019
medline:
17
6
2020
entrez:
5
9
2019
Statut:
ppublish
Résumé
Mass mortalities due to disease outbreaks have recently affected a number of major taxa in marine ecosystems. Climate- and pollution-induced stress may compromise host immune defenses, increasing the risk of opportunistic diseases. Despite growing evidence that mass mortality events affecting marine species worldwide are strongly influenced by the interplay of numerous environmental factors, the reductionist approaches most frequently used to investigate these factors hindered the interpretation of these multifactorial pathologies. In this study, we propose a broader approach based on the combination of RNA-sequencing and 16S microbiota analyses to decipher the factors underlying mass mortality in the striped venus clam, Chamelea gallina, along the Adriatic coast. On one hand, gene expression profiling and functional analyses of microbial communities showed the over-expression of several genes and molecular pathways involved in xenobiotic metabolism, suggesting potential chemical contamination in mortality sites. On the other hand, the down-regulation of several genes involved in immune and stress response, and the over-representation of opportunistic pathogens such as Vibrio and Photobacterium spp. indicates that these microbial species may take advantage of compromised host immune pathways and defense mechanisms that are potentially affected by chemical exposure, resulting in periodic mortality events. We propose the application of our approach to interpret and anticipate the risks inherent in the combined effects of pollutants and microbes on marine animals in today's rapidly changing environment.
Substances chimiques
Water Pollutants
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
4486-4499Informations de copyright
© 2019 John Wiley & Sons Ltd.
Références
Austin, B., Austin, D., Sutherland, R., Thompson, F., & Swings, J. (2005). Pathogenicity of vibrios to rainbow trout (Oncorhynchus mykiss, Walbaum) and Artemia nauplii. Environmental Microbiology, 7(9), 1488-1495. https://doi.org/10.1111/j.1462-2920.2005.00847.x
Avio, C. G., Gorbi, S., Milan, M., Benedetti, M., Fattorini, D., d'Errico, G., … Regoli, F. (2015). Pollutants bioavailability and toxicological risk from microplastics to marine mussels. Environmental Pollution, 198, 211-222. https://doi.org/10.1016/j.envpol.2014.12.021
Benard, E. L., Racz, P. I., Rougeot, J., Nezhinsky, A. E., Verbeek, F. J., Spaink, H. P., & Meijer, A. H. (2015). Macrophage-expressed perforins Mpeg1 and Mpeg1.2 have an anti-bacterial function in zebrafish. Journal of Innate Immunity, 7(2), 136-152. https://doi.org/10.1159/000366103
Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., … Knight, R. (2010). QIIME allows analysis of high-throughput community sequencing data. Nature Methods, 7, 335-336. https://doi.org/10.1038/nmeth.f.303
Cheng, W., Hsiao, I. S., & Chen, J. C. (2004a). Effect of ammonia on the immune response of Taiwan abalone Haliotis diversicolor supertexta and its susceptibility to Vibrio parahaemolyticus. Fish and Shellfish Immunology, 17(3), 193-202. https://doi.org/10.1016/j.fsi.2004.03.004
Cheng, W., Hsiao, I. S., & Chen, J. C. (2004b). Effect of nitrite on immune response of Taiwan abalone Haliotis diversicolor supertexta and its susceptibility to Vibrio parahaemolyticus. Diseases of Aquatic Organisms, 60(2), 157-164. https://doi.org/10.3354/dao060157
Choy, R. K. M., Kemner, J. M., & Thomas, J. H. (2006). Fluoxetine-resistance genes in Caenorhabditis elegans function in the intestine and may act in drug transport. Genetics, 172(2), 885-892. https://doi.org/10.1534/genetics.103.024869
Choy, R. K. M., & Thomas, J. H. (1999). Fluoxetine-resistant mutants in C. elegans define a novel family of transmembrane proteins. Molecular Cell, 4(2), 143-152. https://doi.org/10.1016/S1097-2765(00)80362-7
Cleary, D. F. R., Becking, L. E., Polónia, A. R. M., Freitas, R. M., & Gomes, N. C. M. (2015). Composition and predicted functional ecology of mussel-associated bacteria in Indonesian marine lakes. Antonie Van Leeuwenhoek, 107(3), 821-834. https://doi.org/10.1007/s10482-014-0375-1
Cossu, C., Doyotte, A., Jacquin, M. C., Babut, M., Exinger, A., & Vasseur, P. (1997). Glutathione reductase, selenium - dependent glutathione peroxidase, glutathione levels, and lipid peroxidation in freshwater bivalves, Unio tumidus, as biomarkers of aquatic contamination in field studies. Ecotoxicology and Environmental Safety, 38(2), 122-131. https://doi.org/10.1006/eesa.1997.1582
Davenport, M., Poles, J., Leung, J. M., Wolff, M. J., Abidi, W. M., Ullman, T., … Loke, P. (2014). Metabolic alterations to the mucosal microbiota in inflammatory bowel disease. Inflammatory Bowel Diseases, 20(4), 723-731. https://doi.org/10.1097/MIB.0000000000000011
de Lorgeril, J., Lucasson, A., Petton, B., Toulza, E., Montagnani, C., Clerissi, C., … Mitta, G. (2018). Immune-suppression by OsHV-1 viral infection causes fatal bacteraemia in Pacific oysters. Nature Communication, 9(1), 4215. https://doi.org/10.1038/s41467-018-06659-3
Del Piero, D., Fornaroli, D., & Balzo, M. (1998). Situazione dello stock di Chamelea gallina (L.) nel golfo di Trieste dal 1984 al 1995. Biologia Marina Mediterranea, 5(2), 382-392.
Dennis, G., Sherman, B. T., Hosack, D. A., Yang, J., Gao, W., Lane, H., & Lempicki, R. A. (2003). david: Database for annotation, visualization, and integrated discovery. Genome Biology, 4(9), R60. https://doi.org/10.1186/gb-2003-4-9-r60
Di Francesco, N. (2010). Minacce da alterazione di habitat e da inquinamento per l'erpetofauna in Abruzzo. In Atti. VIII Congresso Nazionale Societas Herpetologica Italica (Chieti, 22-26 settembre 2010) (pp. 487-491). Pescara: Ianieri Edizioni.
Ding, J., Dou, Y., Wang, Y., & Chang, Y. (2014). Draft genome sequence of Vibrio fortis Dalian14 isolated from diseased sea Urchin (Strongylocentrotus intermedius). Genome Announcements, 2(4), e00409-14. https://doi.org/10.1128/genomeA.00409-14
Eiston, R. A., Hasegawa, H., Humphrey, K. L., Polyak, I. K., & Hase, C. C. (2008). Re-emergence of Vibrio tubiashii in bivalve shellfish aquaculture: Severity, environmental drivers, geographic extent and management. Diseases of Aquatic Organisms, 82(2), 119-134. https://doi.org/10.3354/dao01982
Ezgeta-Balić, D., Rinaldi, A., Peharda, M., Prusina, I., Montalto, V., Niceta, N., & Sarà, G. (2011). An energy budget for the subtidal bivalve Modiolus barbatus (Mollusca) at different temperatures. Marine Environmental Research, 71(1), 79-85. https://doi.org/10.1016/j.marenvres.2010.10.005
Fornace, A. J., Jackman, J., Hollander, M., Hoffman-Liebermann, B., & Liebermann, D. (1992). Genotoxic-stress-response genes and growth-arrest genes: gadd, MyD, and other genes induced by treatments eliciting growth arrest. Annals of the New York Academy of Sciences, 663(1), 139-153. https://doi.org/10.1111/j.1749-6632.1992.tb38657.x
Froglia, C. (2000). Il contributo della ricerca scientifica alla gestione della pesca dei molluschi bivalvi con draghe idrauliche. Biologia Marina Mediterranea, 7(4), 71-82.
Fujii, N., Minetti, C. A. S. A., Nakhasi, H. L., Chen, S. W., Barbehenn, E., Nunes, P. H., & Nguyen, N. Y. (1992). Isolation, cDNA cloning, and characterization of an 18-kDa hemagglutinin and amebocyte aggregation factor from Limulus polyphemus. Journal of Biological Chemistry, 267(31), 22452-22459. https://doi.org/10.1007/s002390010230
Gagnaire, B., Gay, M., Huvet, A., Daniel, J.-Y., Saulnier, D., & Renault, T. (2007). Combination of a pesticide exposure and a bacterial challenge: In vivo effects on immune response of Pacific oyster, Crassostrea gigas (Thunberg). Aquatic Toxicology, 84(1), 92-102. https://doi.org/10.1016/j.aquatox.2007.06.002
Galloway, T. S., & Depledge, M. H. (2001). Immunotoxicity in invertebrates: Measurement and ecotoxicological relevance. Ecotoxicology, 10(1), 5-23.
Green, T. J., & Barnes, A. C. (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. https://doi.org/10.1111/j.1365-2672.2010.04687.x.
Green, T. J., Siboni, N., King, W. L., Labbate, M., Seymore, J. R., & Raftos, D. (2018). 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(3), 736-747. https://doi.org/10.1007/s00248-018-1242-9
Hanlon, R. T., Forsythe, J. W., Cooper, K. M., Dinuzzo, A. R., Folse, D. S., & Kelly, M. T. (1984). Fatal penetrating skin ulcers in laboratory-reared octopuses. Journal of Invertebrate Pathology, 44(1), 67-83. https://doi.org/10.1016/0022-2011(84)90047-8
Hazen, T. H., Pan, L., Gu, J. D., & Sobecky, P. A. (2010). The contribution of mobile genetic elements to the evolution and ecology of Vibrios. FEMS Microbiology Ecology, 74(3), 485-499. https://doi.org/10.1111/j.1574-6941.2010.00937.x
Huang, D. D. W., Sherman, B. T. B., & Lempicki, R. A. R. (2009). Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nature Protocols, 4(1), 44-57. https://doi.org/10.1038/nprot.2008.211
Ishimaru, K., Akagawa, M. M., & Muroga, K. (1996). Vibrio ichthyoenteri sp. nov., a pathogens of Japanese flounder (Paralichthys olivaceus) larvae. International Journal of Systematic Bacteriology, 46, 155-159.
King, W. L., Jenkins, C., Go, J., Siboni, N., Seymour, J. R., & Labbate, M. (2019). Characterisation of the pacific oyster microbiome during a summer mortality event. Microbial Ecology, 77(2), 502-512. https://doi.org/10.1007/s00248-018-1226-9.
King, G. M., Judd, C., Kuske, C. R., & Smith, C. (2012). Analysis of stomach and gut microbiomes of the Eastern Oyster (Crassostrea virginica) from Coastal Louisiana, USA. PLoS ONE, 7(12), e51475. https://doi.org/10.1371/journal.pone.0051475
Labella, A., Manchado, M., Alonso, M. C., Castro, D., Romalde, J. L., & Borrego, J. J. (2010). Molecular intraspecific characterization of Photobacterium damselae ssp. damselae strains affecting cultured marine fish. Journal of Applied Microbiology, 108(6), 2122-2132. https://doi.org/10.1111/j.1365-2672.2009.04614.x
Labella, A., Sanchez-Montes, N., Berber, C., Aparicio, M., Castro, D., Manchado, M., & Borrego, J. J. (2010). Toxicity of Photobacterium damselae subsp. damselae strains isolated from new cultured marine fish. Diseases of Aquatic Organisms, 92(1), 31-40. https://doi.org/10.3354/dao02275
Labella, A., Vida, M., Alonso, M. C., Infante, C., Cardenas, S., Lopez-Romalde, S., … Borrego, J. J. (2006). First isolation of Photobacterium damselae ssp. damselae from cultured redbanded seabream, Pagrus auriga Valenciennes, in Spain. Journal of Fish Diseases, 29(3), 175-179. https://doi.org/10.1111/j.1365-2761.2006.00697.x
Langille, M. G. I., Zaneveld, J., Caporaso, J. G., McDonald, D., Knights, D., Reyes, J. A., … Huttenhower, C. (2013). Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nature Biotechnology, 31(9), 814-821. https://doi.org/10.1038/nbt.2676
Le Roux, F., Wegner, K. M., & Polz, M. F. (2016). Oysters and Vibrios as a model for disease dynamics in wild animals. Trends in Microbiology, 24(7), 568-580. https://doi.org/10.1016/j.tim.2016.03.006
Livingstone, D., Kirchin, M., & Wiseman, A. (1989). Cytochrome P-450 and oxidative metabolism in molluscs. Xenobiotica, 19(10), 1041-1062. https://doi.org/10.3109/00498258909043161
Lokmer, A., Goedknegt, M. A., Thieltges, D. W., Fiorentino, D., Kuenzel, S., Baines, J. F., & Mathias Wegner, K. (2016). Spatial and temporal dynamics of pacific oyster hemolymph microbiota across multiple scales. Frontiers in Microbiology, 7, 1367. https://doi.org/10.3389/fmicb.2016.01367
Lokmer, A., & Mathias Wegner, K. (2015). Hemolymph microbiome of Pacific oysters in response to temperature, temperature stress and infection. ISME Journal, 9(3), 670-682. https://doi.org/10.1038/ismej.2014.160
Lozano-León, A., Osorio, C. R., Nuñez, S., Martínez-Urtaza, J., & Magariños, B. (2003). Occurrence of Photobacterium damselae subsp. damselae in bivavlve molluscs from Northwest Spain. Bulletin of the European Association of Fish Pathologists, 23(1), 40-44.
Matozzo, V., Chinellato, A., Munari, M., Finos, L., Bressan, M., & Marin, M. G. (2012). First evidence of immunomodulation in bivalves under seawater acidification and increased temperature. PLoS ONE, 7(3), e33820. https://doi.org/10.1371/journal.pone.0033820
Mezzelani, M., Gorbi, S., Fattorini, D., d'Errico, G., Benedetti, M., Milan, M., … Regoli, F. (2016). Transcriptional and cellular effects of Non-Steroidal Anti-Inflammatory Drugs (NSAIDs) in experimentally exposed mussels, Mytilus galloprovincialis. Aquatic Toxicology, 180, 306-319. https://doi.org/10.1016/j.aquatox.2016.10.006
Milan, M., Carraro, L., Fariselli, P., Martino, M. E., Cavalieri, D., Vitali, F., … Cardazzo, B. (2018). Microbiota and environmental stress: How pollution affects microbial communities in Manila clams. Aquatic Toxicology, 194, 195-207. https://doi.org/10.1016/j.aquatox.2017.11.019
Milan, M., Ferraresso, S., Ciofi, C., Chelazzi, G., Carrer, C., Ferrari, G., … Bargelloni, L. (2013). Exploring the effects of seasonality and chemical pollution on the hepatopancreas transcriptome of the Manila clam. Molecular Ecology, 22(8), 2157-2172. https://doi.org/10.1111/mec.12257
Milan, M., Matozzo, V., Pauletto, M., Di Camillo, B., Giacomazzo, M., Boffo, L., … Bargelloni, L. (2016). Can ecological history influence response to pollutants? Transcriptomomic analysis of Manila clam collected in different Venice lagoon areas and exposed to heavy metal. Aquatic Toxicology, 174, 123-133. https://doi.org/10.1016/j.aquatox.2016.02.024
Milan, M., Palazzo, F., Papetti, C., Grotta, L., Marchetti, S., Patarnello, T., … Martino, G. (2016). Transcriptomic profiling of Chamelea gallina from sites along the Abruzzo coast (Italy), subject to periodic localized mortality events. Marine Biology, 163(9), 163-196. https://doi.org/10.1007/s00227-016-2971-2
Milan, M., Pauletto, M., Patarnello, T., Bargelloni, L., Marin, M. G., & Matozzo, V. (2013). Gene transcription and biomarker responses in the clam Ruditapes philippinarum after exposure to ibuprofen. Aquatic Toxicology, 126, 17-29. https://doi.org/10.1016/j.aquatox.2012.10.007.
Milan, M., Pauletto, M., Boffo, L., Carrer, C., Sorrentino, F., Ferrari, G., … Bargelloni, L. (2015). Transcriptomic resources for environmental risk assessment: A case study in the Venice lagoon. Environmental Pollution, 197, 90-98. https://doi.org/10.1016/j.envpol.2014.12.005
Mohanty, B., Mohanty, S., Sahoo, J., & Sharma, A. (2010). Climate change: Impacts on fisheries and aquaculture. In S. Simard (Ed.), Climate change and variability (pp. 1-486). Croatia: IntechOpen. https://doi.org/10.5772/9805
Monari, M., Foschi, J., Rosmini, R., Marin, M. G., & Serrazanetti, G. P. (2011). Heat shock protein 70 response to physical and chemical stress in Chamelea gallina. Journal of Experimental Marine Biology and Ecology, 397(2), 71-78. https://doi.org/10.1016/j.jembe.2010.11.016
Moreira, R., Balseiro, P., Planas, J. V., Fuste, B., Beltran, S., Novoa, B., & Figueras, A. (2012). Transcriptomics of in vitro immune-stimulated hemocytes from the manila clam Ruditapes philippinarum using high-throughput sequencing. PLoS ONE, 7(4), e35009. https://doi.org/10.1371/journal.pone.0035009
Morello, E. B., Froglia, C., Atkinson, R. J. A., & Moore, P. G. (2005). Hydraulic dredge discards of the clam (Chamelea gallina) fishery in the western Adriatic Sea, Italy. Fisheries Research, 76(3), 430-444. https://doi.org/10.1016/j.fishres.2005.07.002
Morley, N. J. (2009). Environmental risk and toxicology of human and veterinary waste pharmaceutical exposure to wild aquatic host-parasite relationships. Environmental Toxicology and Pharmacology, 27(2), 161-175. https://doi.org/10.1016/j.etap.2008.11.004
Morley, N. J. (2010). Interactive effects of infectious diseases and pollution in aquatic molluscs. Aquatic Toxicology, 96(1), 27-36. https://doi.org/10.1016/j.aquatox.2009.09.017
Moschino, V., Deppieri, M., & Marin, M. G. (2003). Evaluation of shell damage to the clam Chamelea gallina captured by hydraulic dredging in the Northern Adriatic Sea. ICES Journal of Marine Science, 60(2), 393-401. https://doi.org/10.1016/S1054-3139(03)00014-6
Moschino, V., & Marin, M. G. (2006). Seasonal changes in physiological responses and evaluation of “well-being” in the Venus clam Chamelea gallina from the Northern Adriatic Sea. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology, 145(4), 433-440. https://doi.org/10.1016/j.cbpa.2006.07.021
Nadkarni, M. A., Martin, F. E., Jacques, N. A., & Hunter, N. (2002). Determination of bacterial load by real-time PCR using a broad-range (universal) probe and primers set. Microbiology, 148(Pt 1), 257-266. https://doi.org/10.1099/00221287-148-1-257
Olicard, C., Renault, T., Torhy, C., Benmansour, A., & Bourgougnon, N. (2005). Putative antiviral activity in hemolymph from adult Pacific oysters, Crassostrea gigas. Antiviral Research, 66, 147-152. https://doi.org/10.1016/j.antiviral.2005.03.003
Orban, E., Di Lena, G., Nevigato, T., Casini, I., Caproni, R., Santaroni, G., & Giulini, G. (2006). Nutritional and commercial quality of the striped venus clam, Chamelea gallina, from the Adriatic sea. Food Chemistry, 101(3), 1063-1070. https://doi.org/10.1016/j.foodchem.2006.03.005
Park, H., Ahn, I. Y., Kim, H., Lee, J., & Shin, S. C. (2009). Glutathione S-transferase as a biomarker in the Antarctic bivalve Laternula elliptica after exposure to the polychlorinated biphenyl mixture Aroclor 1254. Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology, 150(4), 528-536. https://doi.org/10.1016/j.cbpc.2009.07.008
Parry, H. E., & Pipe, R. K. (2004). Interactive effects of temperature and copper on immunocompetence and disease susceptibility in mussels (Mytilus edulis). Aquatic Toxicology, 69, 311-325. https://doi.org/10.1016/j.aquatox.2004.06.003
Pauletto, M., Segarra, A., Montagnani, C., Quillien, V., Faury, N., Le Grand, J., & Huvet, A. (2017). Long dsRNAs promote an anti-viral response in Pacific oyster hampering ostreid herpesvirus 1 replication. The Journal of Experimental Biology, 220(Pt 20), 3671-3685. https://doi.org/10.1242/jeb.156299
Paulson, J. N., Colin Stine, O., Bravo, H. C., & Pop, M. (2013). Robust methods for differential abundance analysis in marker gene surveys. Nature Methods, 10(12), 1200-1202. https://doi.org/10.1038/nmeth.2658.
Pedersen, K., Skall, H. F., Lassen-Nielsen, A. M., Bjerrum, L., & Olesen, N. J. (2009). Photobacterium damselae subsp. damselae, an emerging pathogen in Danish rainbow trout, Oncorhynchus mykiss (Walbaum), mariculture. Journal of Fish Diseases, 32(5), 465-472. https://doi.org/10.1111/j.1365-2761.2009.01041.x
Pessatti, T. B., Lüchmann, K. H., Flores-Nunes, F., Mattos, J. J., Sasaki, S. T., Taniguchi, S., … Dias Bainy, A. C. (2016). Upregulation of biotransformation genes in gills of oyster Crassostrea brasiliana exposed in situ to urban effluents, Florianópolis Bay, Southern Brazil. Ecotoxicology and Environmental Safety, 131, 172-180. https://doi.org/10.1016/j.ecoenv.2016.04.003
Petton, B., Bruto, M., James, A., Labreuche, Y., Alunno-Bruscia, M., & Le Roux, F. (2015). Crassostrea gigas mortality in France: The usual suspect, a herpes virus, may not be the killer in this polymicrobial opportunistic disease. Frontiers in Microbiology, 6, 686. https://doi.org/10.3389/fmicb.2015.00686
Piccoli, F., Dragani, L. K., Verri, C., Celli, N., Calabrese, R., Marchetti, R., … Pagliani, T. (2010). Genotoxicity and bioconcentration of polycyclic aromatic hydrocarbons and heavy: Metals in Leuciscus cephalus from Pescara River (Abruzzo, Italy): An integrated approach. Environmental Quality/Qualité de l'Environnement/Qualità Ambientale, 3, 41-48. https://doi.org/10.6092/issn.2281-4485/3791
Pipe, R. K., & Coles, J. A. (1995). Environmental contaminants influencing immune function in marine bivalve molluscs. Fish & Shellfish Immunology, 5, 581-595. https://doi.org/10.1016/S1050-4648(95)80043-3
Ramon, M., & Richardson, C. A. (1992). Age determination and shell growth of Chamelea gallina (Bivalvia: Veneridae) in the western Mediterranean. Marine Ecology Progress Series, 89(1), 15-23. https://doi.org/10.3354/meps089015
Reen, F. J., Almagro-Moreno, S., Ussery, D., & Boyd, E. F. (2006). The genomic code: Inferring Vibrionaceae niche specialization. Nature Reviews Microbiology, 4(9), 697-704. https://doi.org/10.1038/nrmicro1476
Renault, T., Faury, N., Barbosa-Solomieu, V., & Moreau, K. (2011). Suppression substractive hybridisation (SSH) and real time PCR reveal differential gene expression in the Pacific cupped oyster, Crassostrea gigas, challenged with Ostreid herpesvirus 1. Developmental and Comparative Immunology, 35, 725-735. https://doi.org/10.1016/j.dci.2011.02.004
Richards, G. P., Watson, M. A., Crane, E. J., Burt, I. G., & Bushek, D. (2008). Shewanella and Photobacterium spp. in oysters and seawater from the Delaware bay. Applied and Environmental Microbiology, 74(11), 3323-3327. https://doi.org/10.1128/AEM.00060-08
Rittschof, D., & McClellan-Green, P. (2005). Molluscs as multidisciplinary models in environment toxicology. Marine Pollution Bulletin, 50(4), 369-373. https://doi.org/10.1016/j.marpolbul.2005.02.008
Rizzi, J., Torresan, S., Critto, A., Zabeo, A., Brigolin, D., Carniel, S., … Marcomini, A. (2016). Climate change impacts on marine water quality: The case study of the Northern Adriatic sea. Marine Pollution Bulletin, 102(2), 271-282. https://doi.org/10.1016/j.marpolbul.2015.06.037
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010). edger: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics, 26(1), 139-140. https://doi.org/10.1093/bioinformatics/btp616
Romalde, J. L., Diguez, A. L., Lasa, A., & Balboa, S. (2014). New Vibrio species associated to molluscan microbiota: A review. Frontiers in Microbiology, 4, 413. https://doi.org/10.3389/fmicb.2013.00413
Romanelli, M., Cordisco, C. A., & Giovanardi, O. (2009). The long-term decline of the Chamelea gallina L. (Bivalvia: Veneridae) clam fishery in the Adriatic Sea: Is a synthesis possible? Acta Adriatica: International journal of Marine Sciences, 50(2), 171-205.
Rosenberg, E., Kushmaro, A., Kramarsky-Winter, E., Banin, E., & Yossi, L. (2009). The role of microorganisms in coral bleaching. The ISME Journal, 3(2), 139-146. https://doi.org/10.1038/ismej.2008.104
Segarra, A., Mauduit, F., Faury, N., Trancart, S., Dégremont, L., Tourbiez, D., … Renault, T. (2014). Dual transcriptomics of virus-host interactions: Comparing two Pacific oyster families presenting contrasted susceptibility to ostreid herpesvirus 1. BMC Genomics, 15(1), 580. https://doi.org/10.1186/1471-2164-15-580
Siboni, N., Balaraju, V., Carney, R., Labbate, M., & Seymour, J. R. (2016). Spatiotemporal dynamics of Vibrio spp. within the Sydney Harbour Estuary. Frontiers in Microbiology, 7, 460. https://doi.org/10.3389/fmicb.2016.00460
Sobral, P., & Widdows, J. (1997). Effects of elevated temperatures on the scope for growth and resistance to air exposure of the clam Ruditapes decussatus (L.), from southern Portugal. Scientia Marina, 61(1), 163-171. https://doi.org/10.1016/S0025-326X(97)00116-1
Stegeman, J. J. (1985). Benzo(a)pyrene oxidation and microsomal enzyme activity in the musseel (Mytilus edulis) and other bivalve mollusc species from the western North Atlantic. Marine Biology, 89(1), 21-30.
Sugumar, G., Nakai, T., Hirata, Y., Matsubara, D., & Muroga, K. (1998). Vibrio splendidus biovar II as the causative agent of bacillary necrosis of Japanese oyster Crassostrea gigas larvae. Diseases of Aquatic Organisms, 33(2), 111-118. https://doi.org/10.3354/dao033111
Tabanelli, G., Montanari, C., Gardini, A., Maffei, M., Prioli, C., & Gardini, F. (2017). Environmental factors affecting Escherichia coli concentrations in striped Venus clam (Chamelea gallina L.) harvested in the North Adriatic Sea. Journal of Food Protection, 80(9), 1429-1435. https://doi.org/10.4315/0362-028X.JFP-17-058
Takekawa, M., & Saito, H. (1998). A family of stress-inducible GADD45-like proteins mediate activation of the stress-responsive MTK1/MEKK4 MAPKKK. Cell, 95(4), 521-530. https://doi.org/10.1016/S0092-8674(00)81619-0
Torresi, M., Acciari, V. A., Piano, A., Serratore, P., Prencipe, V., & Migliorati, G. (2011). Detection of vibrio splendidus and related species in Chamelea gallina sampled in the Adriatic along the Abruzzi coastline. Veterinaria Italiana, 47(3), 371-378.
Trabal Fernanndez, N., Mazon-Suastegui, J., Vazquez-Juarez, R., Ascencio-Valle, F., & Romero, J. (2014). Changes in the composition and diversity of the bacterial microbiota associated with oysters (Crassostrea corteziensis, Crassostrea gigas and Crassostrea sikamea) during commercial production. FEMS Microbiology Ecology, 88(1), 69-83. https://doi.org/10.1111/1574-6941.12270
Trabal, N., Mazon-Suastegui, J. M., Vazquez-Juarez, R., Asencio-Valle, F., Morales-Bojorquez, 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(2), 555-569. https://doi.org/10.1007/s00248-0
Visciano, P., Scortichini, G., Suzzi, G., Diletti, G., Schirone, M., & Martino, G. (2015). Concentrations of contaminants with regulatory limits in samples of clam (Chamelea gallina) collected along the Abruzzi Region Coast in Central Italy. Journal of Food Protection, 78(9), 1719-1728. https://doi.org/10.4315/0362-028X.JFP-15-082
Wang, X., Zhang, Y., Qin, G., Luo, W., & Lin, Q. (2016). A novel pathogenic bacteria (Vibrio fortis) causing enteritis in cultured seahorses, Hippocampus erectus Perry, 1810. Journal of Fish Diseases, 39(6), 765-769. https://doi.org/10.1111/jfd.12411
Xu, C., Pan, L., Liu, N., Wang, L., & Miao, J. (2010). Cloning, characterization and tissue distribution of a pi-class glutathione S-transferase from clam (Venerupis philippinarum): Response to benzo[α]pyrene exposure. Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology, 152(2), 160-166. https://doi.org/10.1016/j.cbpc.2010.03.011
Zakrzewski, M., Proietti, C., Ellis, J. J., Hasan, S., Brion, M. J., Berger, B., & Krause, L. (2017). Calypso: A user-friendly web-server for mining and visualizing microbiome-environment interactions. Bioinformatics, 33(5), 782-783. https://doi.org/10.1093/bioinformatics/btw725
Zanette, J., Goldstone, J. V., Bainy, A. C. D., & Stegeman, J. J. (2010). Identification of CYP genes in Mytilus (mussel) and Crassostrea (oyster) species: First approach to the full complement of cytochrome P450 genes in bivalves. Marine Environmental Research, 69(Suppl. 1), S1-S3. https://doi.org/10.1016/j.marenvres.2009.10.013