Molecular Epidemiology of Subsp. Outbreaks in Marine Rainbow Trout Farms Reveals Extensive Horizontal Gene Transfer and High Genetic Diversity

Overview

Journal Front Microbiol

Specialty Microbiology

Date 2018 Oct 5

PMID 30283411

Citations 11

Authors

Mateus S Terceti

Ana Vences

Xose M Matanza

Inger Dalsgaard

Karl Pedersen

Carlos R Osorio

Affiliations

Soon will be listed here.

Abstract

The marine bacterium subsp. is a pathogen for a variety of marine animals, as well as for humans, and is nowadays considered an emerging pathogen for fish of importance in marine aquaculture. Recent studies have suggested that outbreaks in fish farms are caused by multiclonal populations of this subspecies that exist in the environment. Here, we report the study of a collection of 31 strains isolated during the course of disease outbreaks in marine rainbow trout farms in Denmark in 1994, 1995, and 2006, respectively. A phylogenetic analysis based on the gene sequence, and the screening of virulence-related genes uncovered a high genetic heterogeneity, even among strains isolated from the same fish farm at the same time. Moreover, comparative analysis of the whole genome sequences of four selected strains revealed a large number of differentially occurring genes, which included virulence genes, pPHDD1 plasmid, polysaccharide synthesis gene clusters, CRISPR-Cas systems and putative new mobile genetic elements. This study provides sound evidence that subsp. outbreaks in Danish rainbow trout farms were caused by multiclonal populations and that horizontal gene transfer constitutes a strong driving force in the generation of intraspecific diversity in this pathogen.

Citing Articles

Clustered Regularly Interspaced Short Palindromic Repeat/CRISPR-Associated Protein and Its Utility All at Sea: Status, Challenges, and Prospects.

Li J, Wu S, Zhang K, Sun X, Lin W, Wang C Microorganisms. 2024; 12(1).

PMID: 38257946 PMC: 10820777. DOI: 10.3390/microorganisms12010118.

Low salinity activates a virulence program in the generalist marine pathogen subsp. .

Barca A, Vences A, Terceti M, do Vale A, Osorio C mSystems. 2023; 8(3):e0125322.

PMID: 37288979 PMC: 10308900. DOI: 10.1128/msystems.01253-22.

The Evolution of a Specialized, Highly Virulent Fish Pathogen through Gene Loss and Acquisition of Host-Specific Survival Mechanisms.

Baseggio L, Rudenko O, Engelstadter J, Barnes A Appl Environ Microbiol. 2022; 88(14):e0022222.

PMID: 35862683 PMC: 9317898. DOI: 10.1128/aem.00222-22.

Systematic review of the status of veterinary epidemiological research in two species regarding the FAIR guiding principles.

Meyer A, Faverjon C, Hostens M, Stegeman A, Cameron A BMC Vet Res. 2021; 17(1):270.

PMID: 34380468 PMC: 8355576. DOI: 10.1186/s12917-021-02971-1.

ML1206 Isolated from Wild Oysters Enhances the Survival of against .

Li Y, Wang N, Zhou Y, Lin C, Wu J, Chen X Mar Drugs. 2021; 19(3).

PMID: 33809116 PMC: 7999227. DOI: 10.3390/md19030150.

References

Tamura K, Nei M, Kumar S . Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A. 2004; 101(30):11030-5. PMC: 491989. DOI: 10.1073/pnas.0404206101. View

Balado M, Puentes B, Couceiro L, Fuentes-Monteverde J, Rodriguez J, Osorio C . Secreted Citrate Serves as Iron Carrier for the Marine Pathogen subsp . Front Cell Infect Microbiol. 2017; 7:361. PMC: 5550697. DOI: 10.3389/fcimb.2017.00361. View

Machado H, Gram L . Comparative Genomics Reveals High Genomic Diversity in the Genus . Front Microbiol. 2017; 8:1204. PMC: 5489566. DOI: 10.3389/fmicb.2017.01204. View

Sharma S, Pradeep M, Sadu N, Dube P, Vijayan K . First report of isolation and characterization of Photobacterium damselae subsp. damselae from cage-farmed cobia (Rachycentron canadum). J Fish Dis. 2016; 40(7):953-958. DOI: 10.1111/jfd.12557. View

Whitfield C . Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem. 2006; 75:39-68. DOI: 10.1146/annurev.biochem.75.103004.142545. View

Pedersen K, Dalsgaard I, Larsen J . Vibrio damsela associated with diseased fish in Denmark. Appl Environ Microbiol. 1997; 63(9):3711-5. PMC: 168678. DOI: 10.1128/aem.63.9.3711-3715.1997. View

Pedersen K, Skall H, Lassen-Nielsen A, Bjerrum L, Olesen N . Photobacterium damselae subsp. damselae, an emerging pathogen in Danish rainbow trout, Oncorhynchus mykiss (Walbaum), mariculture. J Fish Dis. 2009; 32(5):465-72. DOI: 10.1111/j.1365-2761.2009.01041.x. View

Makarova K, Wolf Y, Alkhnbashi O, Costa F, Shah S, Saunders S . An updated evolutionary classification of CRISPR-Cas systems. Nat Rev Microbiol. 2015; 13(11):722-36. PMC: 5426118. DOI: 10.1038/nrmicro3569. View

Thomas C, Nielsen K . Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nat Rev Microbiol. 2005; 3(9):711-21. DOI: 10.1038/nrmicro1234. View

10.

Schmidt H, Hensel M . Pathogenicity islands in bacterial pathogenesis. Clin Microbiol Rev. 2004; 17(1):14-56. PMC: 321463. DOI: 10.1128/CMR.17.1.14-56.2004. View

11.

Ma K, Cao Q, Luo S, Wang Z, Liu G, Lu C . Enhances Bacterial Virulence by Repressing the Transcriptional Regulator in Streptococcus agalactiae. Infect Immun. 2017; 86(3). PMC: 5820942. DOI: 10.1128/IAI.00552-17. View

12.

Rivas A, Vences A, Husmann M, Lemos M, Osorio C . Photobacterium damselae subsp. damselae major virulence factors Dly, plasmid-encoded HlyA, and chromosome-encoded HlyA are secreted via the type II secretion system. Infect Immun. 2015; 83(4):1246-56. PMC: 4363413. DOI: 10.1128/IAI.02608-14. View

13.

Rivas A, Balado M, Lemos M, Osorio C . Synergistic and additive effects of chromosomal and plasmid-encoded hemolysins contribute to hemolysis and virulence in Photobacterium damselae subsp. damselae. Infect Immun. 2013; 81(9):3287-99. PMC: 3754223. DOI: 10.1128/IAI.00155-13. View

14.

Labella A, Vida M, Alonso M, Infante C, Cardenas S, Lopez-Romalde S . First isolation of Photobacterium damselae ssp. damselae from cultured redbanded seabream, Pagrus auriga Valenciennes, in Spain. J Fish Dis. 2006; 29(3):175-9. DOI: 10.1111/j.1365-2761.2006.00697.x. View

15.

Osorio C, Vences A, Matanza X, Terceti M . subsp. , a generalist pathogen with unique virulence factors and high genetic diversity. J Bacteriol. 2018; 200(15):e00002-18. PMC: 6040198. DOI: 10.1128/JB.00002-18. View

16.

Terceti M, Ogut H, Osorio C . Photobacterium damselae subsp. damselae, an Emerging Fish Pathogen in the Black Sea: Evidence of a Multiclonal Origin. Appl Environ Microbiol. 2016; 82(13):3736-3745. PMC: 4907178. DOI: 10.1128/AEM.00781-16. View

17.

Carraro R, Rovere G, Ferraresso S, Carraro L, Franch R, Toffan A . Development of a real-time PCR assay for rapid detection and quantification of Photobacterium damselae subsp. piscicida in fish tissues. J Fish Dis. 2017; 41(2):247-254. DOI: 10.1111/jfd.12703. View

18.

Spencer-Smith R, Roberts S, Gurung N, Snyder L . DNA uptake sequences in as intrinsic transcriptional terminators and markers of horizontal gene transfer. Microb Genom. 2017; 2(8):e000069. PMC: 5320588. DOI: 10.1099/mgen.0.000069. View

19.

Ambur O, Frye S, Tonjum T . New functional identity for the DNA uptake sequence in transformation and its presence in transcriptional terminators. J Bacteriol. 2006; 189(5):2077-85. PMC: 1855724. DOI: 10.1128/JB.01408-06. View

20.

Terceti M, Rivas A, Alvarez L, Noia M, Cava F, Osorio C . Regulates Expression of the subsp. Major Virulence Factors Damselysin, Phobalysin P and Phobalysin C. Front Microbiol. 2017; 8:582. PMC: 5385354. DOI: 10.3389/fmicb.2017.00582. View