Emergence and clonal expansion of Vibrio aestuarianus lineages pathogenic for oysters in Europe.
adaptation
bacteria
clonal expansion
molecular evolution
Journal
Molecular ecology
ISSN: 1365-294X
Titre abrégé: Mol Ecol
Pays: England
ID NLM: 9214478
Informations de publication
Date de publication:
06 2023
06 2023
Historique:
revised:
07
01
2023
received:
24
09
2022
accepted:
20
02
2023
medline:
23
5
2023
pubmed:
2
3
2023
entrez:
1
3
2023
Statut:
ppublish
Résumé
Crassostrea gigas oysters represent a significant global food source with 4.7 million tons harvested per year. In 2001, the bacterium Vibrio aestuarianus subsp. francensis emerged as a pathogen that causes adult oyster mortality in France and Ireland. Its impact on oyster aquaculture has increased in Europe since its re-emergence in 2012. To better understand the evolutionary mechanisms leading to the emergence and persistence over time of this pathogen, we conducted a survey of mollusc diseases through national reference laboratories across Europe. We analysed 54 new genomes of Vibrio aestuarianus (Va) isolated from multiple environmental compartments since 2001, in areas with and without bivalve mortalities. We used a combination of comparative genomics and population genetics approaches and show that Va has a classical epidemic population structure from which the pathogenic Va francensis subspecies emerged and clonally expanded. Furthermore, we identified a specific cus-cop-containing island conferring copper resistance to Va francensis whose acquisition may have favoured the emergence of pathogenic lineages adapted and specialized to oysters.
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2869-2883Informations de copyright
© 2023 Crown copyright. Molecular Ecology © 2023 John Wiley & Sons Ltd. This article is published with the permission of the Controller of HMSO and the King's Printer for Scotland.
Références
Anderson, P. K., Cunningham, A. A., Patel, N. G., Morales, F. J., Epstein, P. R., & Daszak, P. (2004). Emerging infectious diseases of plants: Pathogen pollution, climate change and agrotechnology drivers. Trends in Ecology & Evolution, 19, 535-544.
Anderson, R. M., Spratt, B. G., & Maiden, M. C. J. (1999). Bacterial population genetics, evolution and epidemiology. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences, 354, 701-710.
Argüello, J. M., Raimunda, D., & Padilla-Benavides, T. (2013). Mechanisms of copper homeostasis in bacteria. Frontiers in Cellular and Infection Microbiology, 3, 73.
Baele, G., Lemey, P., Bedford, T., Rambaut, A., Suchard, M. A., & Alekseyenko, A. V. (2012). Improving the accuracy of demographic and molecular clock model comparison while accommodating phylogenetic uncertainty. Molecular Biology and Evolution, 29, 2157-2167.
Baele, G., Li, W. L. S., Drummond, A. J., Suchard, M. A., & Lemey, P. (2012). Accurate model selection of relaxed molecular clocks in Bayesian Phylogenetics. Molecular Biology and Evolution, 30, 239-243.
Bankevich, A., Nurk, S., Antipov, D., Gurevich, A. A., Dvorkin, M., Kulikov, A. S., Lesin, V. M., Nikolenko, S. I., Pham, S., Prjibelski, A. D., Pyshkin, A. V., Sirotkin, A. V., Vyahhi, N., Tesler, G., Alekseyev, M. A., & Pevzner, P. A. (2012). SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology, 19, 455-477.
Bäumler, A., & Fang, F. C. (2013). Host specificity of bacterial pathogens. Cold Spring Harbor Perspectives in Medicine, 3, a010041.
Bergstrom, C. T., McElhany, P., & Real, L. A. (1999). Transmission bottlenecks as determinants of virulence in rapidly evolving pathogens. Proceedings of the National Academy of Sciences, 96, 5095-5100.
Bhuiyan, N. A., Ansaruzzaman, M., Kamruzzaman, M., Alam, K., Chowdhury, N. R., Nishibuchi, M., Faruque, S. M., Sack, D. A., Takeda, Y., & Nair, G. B. (2002). Prevalence of the pandemic genotype of Vibrio parahaemolyticus in Dhaka, Bangladesh, and significance of its distribution across different serotypes. Journal of Clinical Microbiology, 40, 284-286.
Bondarczuk, K., & Piotrowska-Seget, Z. (2013). Molecular basis of active copper resistance mechanisms in gram-negative bacteria. Cell Biology and Toxicology, 29, 397-405.
Bruto, M., James, A., Petton, B., Labreuche, Y., Chenivesse, S., Alunno-Bruscia, M., Polz, M. F., & Le Roux, F. (2017). Vibrio crassostreae, a benign oyster colonizer turned into a pathogen after plasmid acquisition. The ISME Journal, 11, 1043-1052.
Bush, S. J. (2020). Read trimming has minimal effect on bacterial SNP-calling accuracy. Microbial Genomics, 6, mgen000434.
Cantalapiedra, C. P., Hernández-Plaza, A., Letunic, I., Bork, P., & Huerta-Cepas, J. (2021). eggNOG-mapper v2: Functional annotation, Orthology assignments, and domain prediction at the metagenomic scale. Molecular Biology and Evolution, 38, 5825-5829.
Charlesworth, D., & Charlesworth, B. (1995). Quantitative genetics in plants: The effect of the breeding system on genetic variability. Evolution, 49, 911-920.
Charlesworth, D., Charlesworth, B., & Morgan, M. T. (1995). The pattern of neutral molecular variation under the background selection model. Genetics, 141, 1619-1632.
Claisse, D., & Alzieu, C. (1993). Copper contamination as a result of antifouling paint regulations? Marine Pollution Bulletin, 26, 395-397.
Cohan, F. M. (2002). Sexual isolation and speciation in bacteria. Genetics of Mate Choice: From Sexual Selection to Sexual Isolation, 116, 359-370.
Darling, A. E., Mau, B., & Perna, N. T. (2010). progressiveMauve: Multiple genome alignment with gene gain, loss and rearrangement. PLOS One, 5, e11147.
Davis, B. M., & Waldor, M. K. (2003). Filamentous phages linked to virulence of vibrio cholerae. Current Opinion in Microbiology, 6, 35-42.
Dégremont, L., Azéma, P., Maurouard, E., & Travers, M.-A. (2020). Enhancing resistance to vibrio aestuarianus in Crassostrea gigas by selection. Aquaculture, 526, 735429.
Destoumieux-Garzón, D., Canesi, L., Oyanedel, D., Travers, M.-A., Charrière, G. M., Pruzzo, C., & Vezzulli, L. (2020). Vibrio-bivalve interactions in health and disease. Environmental Microbiology, 22, 4323-4341.
Didelot, X., Bowden, R., Street, T., Golubchik, T., Spencer, C., McVean, G., Sangal, V., Anjum, M. F., Achtman, M., Falush, D., & Donnelly, P. (2011). Recombination and population structure in salmonella enterica. PLoS Genetics, 7, e1002191.
Didelot, X., Pang, B., Zhou, Z., McCann, A., Ni, P., Li, D., Achtman, M., & Kan, B. (2015). The role of China in the global spread of the current cholera pandemic. PLoS Genetics, 11, e1005072.
Didelot, X., & Wilson, D. J. (2015). ClonalFrameML: Efficient inference of recombination in whole bacterial genomes. PLOS Computational Biology, 11, e1004041.
Drummond, A. J., Nicholls, G. K., Rodrigo, A. G., & Solomon, W. (2002). Estimating mutation parameters, population history and genealogy simultaneously from temporally spaced sequence data. Genetics, 161, 1307-1320.
Falush, D., Stephens, M., & Pritchard, J. K. (2003). Inference of population structure using multilocus genotype data: Linked loci and correlated allele frequencies. Genetics, 164, 1567-1587.
Floriano, A. M., Castelli, M., Krenek, S., Berendonk, T. U., Bazzocchi, C., Petroni, G., & Sassera, D. (2018). The genome sequence of "Candidatus Fokinia solitaria": Insights on reductive evolution in Rickettsiales. Genome Biology and Evolution, 10, 1120-1126.
FranceAgriMer. (2021). https://www.franceagrimer.fr/
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.
Garnier, M., Labreuche, Y., & Nicolas, J. L. (2008). Molecular and phenotypic characterization of vibrio aestuarianus subsp. francensis subsp. nov., a pathogen of the oyster Crassostrea gigas. Systematic and Applied Microbiology, 31, 358-365.
González-Escalona, N., Martinez-Urtaza, J., Romero, J., Espejo, R. T., Jaykus, L.-A., & DePaola, A. (2008). Determination of molecular phylogenetics of Vibrio parahaemolyticus strains by multilocus sequence typing. Journal of Bacteriology, 190, 2831-2840.
Goris, J., Konstantinidis, K. T., Klappenbach, J. A., Coenye, T., Vandamme, P., & Tiedje, J. M. (2007). DNA-DNA hybridization values and their relationship to whole-genome sequence similarities. International Journal of Systematic and Evolutionary Microbiology, 57, 81-91.
Goudenège, D., Travers, M. A., Lemire, A., Petton, B., Haffner, P., Labreuche, Y., Tourbiez, D., Mangenot, S., Calteau, A., Mazel, D., Nicolas, J. L., Jacq, A., & Le Roux, F. (2015). A single regulatory gene is sufficient to alter vibrio aestuarianus pathogenicity in oysters. Environmental Microbiology, 17, 4189-4199.
Gurevich, A., Saveliev, V., Vyahhi, N., & Tesler, G. (2013). QUAST: Quality assessment tool for genome assemblies. Bioinformatics, 29, 1072-1075.
Hall, L. W., & Anderson, R. D. (1999). A deterministic ecological risk assessment for copper in European saltwater environments. Marine Pollution Bulletin, 38, 207-218.
Hauck, S., & Maiden, M. C. J. (2018). Clonally evolving pathogenic bacteria. In P. H. Rampelotto (Ed.), Molecular mechanisms of microbial evolution (pp. 307-325). Springer International Publishing. https://doi.org/10.1007/978-3-319-69078-0_12
Huerta-Cepas, J., Szklarczyk, D., Heller, D., Hernández-Plaza, A., Forslund, S. K., Cook, H., Mende, D. R., Letunic, I., Rattei, T., Jensen Lars, J., von Mering, C., & Bork, P. (2018). eggNOG 5.0: A hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Research, 47, D309-D314.
Kolmogorov, M., Yuan, J., Lin, Y., & Pevzner, P. A. (2019). Assembly of long, error-prone reads using repeat graphs. Nature Biotechnology, 37, 540-546.
Lafferty, K. D., Harvell, C. D., Conrad, J. M., Friedman, C. S., Kent, M. L., Kuris, A. M., Powell, E. N., Rondeau, D., & Saksida, S. M. (2015). Infectious diseases affect marine fisheries and aquaculture economics. Annual Review of Marine Science, 7, 471-496.
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.
Levin, B. R. (1981). Periodic selection, infectious gene exchange and the genetic strucutre of E. coli populations. Genetics, 99, 1-23.
Mandas, D., Salati, F., Polinas, M., Sanna, M. A., Zobba, R., Burrai, G. P., Alberti, A., & Antuofermo, E. (2020). Histopathological and molecular study of Pacific oyster tissues provides insights into V. aestuarianus infection related to oyster mortality. Pathogens, 9, 492.
Martínez, J. L. (2013). Bacterial pathogens: From natural ecosystems to human hosts. Environmental Microbiology, 15, 325-333.
Martinez-Urtaza, J., Rv, A., Abanto, M., Haendiges, J., Myers, R. A., Trinanes, J., Baker-Austin, C., & Gonzalez-Escalona, N. (2017). Genomic variation and evolution of Vibrio parahaemolyticus ST36 over the course of a transcontinental epidemic expansion. mBio, 8, e01425-17.
Minin, V. N., Bloomquist, E. W., & Suchard, M. A. (2008). Smooth Skyride through a rough skyline: Bayesian coalescent-based inference of population dynamics. Molecular Biology and Evolution, 25, 1459-1471.
Moore, S., Thomson, N., Mutreja, A., & Piarroux, R. (2014). Widespread epidemic cholera caused by a restricted subset of vibrio cholerae clones. Clinical Microbiology and Infection, 20, 373-379.
Moran, N. A. (2002). Microbial minimalism: Genome reduction in bacterial pathogens. Cell, 108, 583-586.
Murray, A. G., & Peeler, E. J. (2005). A framework for understanding the potential for emerging diseases in aquaculture. Preventive Veterinary Medicine, 67, 223-235.
Namouchi, A., Didelot, X., Schöck, U., Gicquel, B., & Rocha, E. P. C. (2012). After the bottleneck: Genome-wide diversification of the mycobacterium tuberculosis complex by mutation, recombination, and natural selection. Genome Research, 22, 721-734.
Page, A. J., Cummins, C. A., Hunt, M., Wong, V. K., Reuter, S., Holden, M. T. G., Fookes, M., Falush, D., Keane, J. A., & Parkhill, J. (2015). Roary: Rapid large-scale prokaryote pan genome analysis. Bioinformatics, 31, 3691-3693.
Paradis, E. (2010). Pegas: An R package for population genetics with an integrated-modular approach. Bioinformatics, 26, 419-420.
Parizadeh, L., Tourbiez, D., Garcia, C., Haffner, P., Dégremont, L., Le Roux, F., & Travers, M.-A. (2018). Ecologically realistic model of infection for exploring the host damage caused by vibrio aestuarianus. Environmental Microbiology, 20, 4343-4355.
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.
Polz, M. F., Alm, E. J., & Hanage, W. P. (2013). Horizontal gene transfer and the evolution of bacterial and archaeal population structure. Trends in Genetics, 29, 170-175.
Rambaut, A., Drummond, A. J., Xie, D., Baele, G., & Suchard, M. A. (2018). Posterior summarization in Bayesian Phylogenetics using tracer 1.7. Systematic Biology, 67, 901-904.
Rambaut, A., Lam, T. T., Max Carvalho, L., & Pybus, O. G. (2016). Exploring the temporal structure of heterochronous sequences using TempEst (formerly path-O-gen). Virus Evolution, 2, vew007.
Rossi, N., & Jamet, J.-L. (2008). In situ heavy metals (copper, lead and cadmium) in different plankton compartments and suspended particulate matter in two coupled Mediterranean coastal ecosystems (Toulon Bay, France). Marine Pollution Bulletin, 56, 1862-1870.
Salim, A., Lan, R., & Reeves, P. R. (2005). Vibrio cholerae pathogenic clones. Emerging Infectious Diseases, 11, 1758-1760.
Saulnier, D., De Decker, S., & Haffner, P. (2009). Real-time PCR assay for rapid detection and quantification of vibrio aestuarianus in oyster and seawater: A useful tool for epidemiologic studies. Journal of Microbiological Methods, 77, 191-197.
Seemann, T. (2014). Prokka: Rapid prokaryotic genome annotation. Bioinformatics, 30, 2068-2069.
Sheppard, S. K., Guttman, D. S., & Fitzgerald, J. R. (2018). Population genomics of bacterial host adaptation. Nature Reviews Genetics, 19, 549-565.
Shi, B., Wang, T., Zeng, Z., Zhou, L., You, W., & Ke, C. (2019). The role of copper and zinc accumulation in defense against bacterial pathogen in the Fujian oyster (Crassostrea angulata). Fish & Shellfish Immunology, 92, 72-82.
Siguier, P., Gourbeyre, E., & Chandler, M. (2014). Bacterial insertion sequences: Their genomic impact and diversity. FEMS Microbiology Reviews, 38, 865-891.
Simão, F. A., Waterhouse, R. M., Ioannidis, P., Kriventseva, E. V., & Zdobnov, E. M. (2015). BUSCO: Assessing genome assembly and annotation completeness with single-copy orthologs. Bioinformatics, 31, 3210-3212.
Smith, J. M., Feil, E. J., & Smith, N. H. (2000). Population structure and evolutionary dynamics of pathogenic bacteria. BioEssays, 22, 1115-1122.
Smith, J. M., & Haigh, J. (2009). The hitch-hiking effect of a favourable gene. Genetical Research, 23, 23-35.
Subramanian, S. (2016). The effects of sample size on population genomic analyses - Implications for the tests of neutrality. BMC Genomics, 17, 123.
Syberg-Olsen, M. J., Garber, A. I., Keeling, P. J., McCutcheon, J. P., & Husnik, F. (2022). Pseudofinder: Detection of pseudogenes in prokaryotic genomes. Molecular Biology and Evolution, 39, msac153.
Tajima, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics, 123, 585-595.
Tettelin, H., Riley, D., Cattuto, C., & Medini, D. (2008). Comparative genomics: The bacterial pan-genome. Current Opinion in Microbiology, 11, 472-477.
Tibayrenc, M., & Ayala, F. J. (2012). Reproductive clonality of pathogens: A perspective on pathogenic viruses, bacteria, fungi, and parasitic protozoa. Proceedings of the National Academy of Sciences, 109, E3305-E3313.
Tison, D. L., & Seidler, R. J. (1983). Vibrio aestuarianus: A new species from estuarine waters and shellfish†. International Journal of Systematic and Evolutionary Microbiology, 33, 699-702.
Touchon, M., & Rocha, E. P. C. (2007). Causes of insertion sequences abundance in prokaryotic genomes. Molecular Biology and Evolution, 24, 969-981.
Travers, M. A., Tourbiez, D., Parizadeh, L., Haffner, P., Kozic-Djellouli, A., Aboubaker, M., Koken, M., Degremont, L., & Lupo, C. (2017). Several strains, one disease: Experimental investigation of vibrio aestuarianus infection parameters in the Pacific oyster, Crassostrea gigas. Veterinary Research, 48, 32.
Vanhove, A. S., Duperthuy, M., Charriere, G. M., Le Roux, F., Goudenege, D., Gourbal, B., Kieffer-Jaquinod, S., Coute, Y., Wai, S. N., & Destoumieux-Garzon, D. (2015). Outer membrane vesicles are vehicles for the delivery of Vibrio tasmaniensis virulence factors to oyster immune cells. Environmental Microbiology, 17, 1152-1165.
Vaser, R., Sovic, I., Nagarajan, N., & Sikic, M. (2017). Fast and accurate de novo genome assembly from long uncorrected reads. Genome Research, 27, 737-746. https://doi.org/10.1101/gr.214270.116
Weng, N., & Wang, W.-X. (2014). Variations of trace metals in two estuarine environments with contrasting pollution histories. Science of the Total Environment, 485-486, 604-614.
Wingett, S. W., & Andrews, S. (2018). FastQ screen: A tool for multi-genome mapping and quality control. F1000Research, 7, 1338.
Xie, Z., & Tang, H. (2017). ISEScan: Automated identification of insertion sequence elements in prokaryotic genomes. Bioinformatics, 33, 3340-3347.
Yeh, S.-T., Liu, C.-H., & Chen, J.-C. (2004). Effect of copper sulfate on the immune response and susceptibility to vibrio alginolyticus in the white shrimp Litopenaeus vannamei. Fish & Shellfish Immunology, 17, 437-446.