Application of suppressive subtractive hybridization to the identification of genetic differences between two lactococcus garvieae strains showing distinct differences in virulence for rainbow trout and mouse

Microbiology

Volumn 157, Issue 7, 2011, Pages 2106-2119

  Reimundo, Pilar ^a   Rivas, Amable J ^b   Osorio, Carlos R ^b   Ménndez, Jéssica ^a   Pérez Pascual, David ^a   Navais, Roberto ^a   Gómez, Esther ^a   Sotelo, Miguel ^c   Lemos, Manuel L ^b   Guijarro, José A ^a  

^a DEPARTAMENTO DE BIOQUÍMICA Y BIOLOGÍA MOLECULAR   (Spain)

^b Santiago de Compostela Spain   (Spain)

^c BioMar Group   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL DNA; BINDING PROTEIN; MEMBRANE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; DNA SEQUENCE; DOT HYBRIDIZATION; GENE SEQUENCE; GENETIC DIFFERENCE; GENETIC HETEROGENEITY; LACTOCOCCUS; LACTOCOCCUS GARVIEAE 074; LACTOCOCCUS GARVIEAE HF; LD 50; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENICITY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RAINBOW TROUT; SUPPRESSION SUBTRACTIVE HYBRIDIZATION;

ANIMALS; BACTERIAL PROTEINS; BASE SEQUENCE; DNA, BACTERIAL; FISH DISEASES; GENETIC VARIATION; GRAM-POSITIVE BACTERIAL INFECTIONS; HUMANS; LACTOCOCCUS; MEMBRANE PROTEINS; MICE; MOLECULAR SEQUENCE DATA; NUCLEIC ACID HYBRIDIZATION; ONCORHYNCHUS MYKISS; OPEN READING FRAMES; POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA; VIRULENCE FACTORS;

BACTERIA (MICROORGANISMS); LACTOCOCCUS GARVIEAE; MUS; ONCORHYNCHUS MYKISS;

EID: 79959977615     PISSN: 13500872     EISSN: None     Source Type: Journal    
DOI: 10.1099/mic.0.047969-0     Document Type: Article

References (83)

1. Alegría, A., Alvarez-Martín, P., Sacristán, N., Fernández, E., Delgado, S. & Mayo, B. (2009). Diversity and evolution of the microbial populations during manufacture and ripening of casi{dotless} ́n, a traditional Spanish, starterfree cheese made from cow's milk. Int J Food Microbiol 136, 44-51.
2. Ammor, S., Yaakoubi, K., Chevallier, I. & Dufour, E. (2004). Identification by fluorescence spectroscopy of lactic acid bacteria isolated from a small-scale facility producing traditional dry sausages. J Microbiol Methods 59, 271-281.
3. Aubin, G. G., Bémer, P., Guillouzouic, A., Crémet, L., Touchais, S., Fraquet, N., Boutoille, D., Reynaud, A., Lepelletier, D. & Corvec, S. (2011). First report of a hip prosthetic and joint infection caused by Lactococcus garvieae in a woman fishmonger. J Clin Microbiol 49, 2074-2076.
4. Austin, B. & Austin, D. A. (2007). Bacterial Fish Pathogens, Disease of Farmed and Wild Fish, 4th edn. Godalming: Springer Praxis.
5. Barakat, R. K., Griffiths, M. W. & Harris, L. J. (2000). Isolation and characterization of Carnobacterium, Lactococcus, and Enterococcus spp. from cooked, modified atmosphere packaged, refrigerated, poultry meat. Int J Food Microbiol 62, 83-94.
6. Boekhorst, J., Helmer, Q., Kleerebezem, M. & Siezen, R. J. (2006). Comparative analysis of proteins with a mucus-binding domain found exclusively in lactic acid bacteria. Microbiology 152, 273-280.
7. Bohnsack, J. F., Takahashi, S., Detrick, S. R., Pelinka, L. R., Hammitt, L. L., Aly, A. A., Whiting, A. A. & Adderson, E. E. (2001). Phylogenetic classification of serotype III group B streptococci on the basis of hylB gene analysis and DNA sequences specific to restriction digest pattern type III-3. J Infect Dis 183, 1694-1697.
8. Boyd, E. F. & Brüssow, H. (2002). Common themes among bacteriophage-encoded virulence factors and diversity among the bacteriophages involved. Trends Microbiol 10, 521-529.
9. Carvalho, M. G., Vianni, M. C., Elliott, J. A., Reeves, M., Facklam, R. R. & Teixeira, L. M. (1997). Molecular analysis of Lactococcus garvieae and Enterococcus gallinarum isolated from water buffalos with subclinical mastitis. Adv Exp Med Biol 418, 401-404.
10. Chan, J. F., Woo, P. C., Teng, J. L., Lau, S. K., Leung, S. S., Tam, F. C. & Yuen, K. Y. (2011). Primary infective spondylodiscitis caused by Lactococcus garvieae and a review of human L. garvieae infections. Infection. (Epub ahead of print). doi:10.1007/s15010-011-0094-8.
11. Chen, Z., Luong, T. T. & Lee, C. Y. (2007). The sbcDC locus mediates repression of type 5 capsule production as part of the SOS response in Staphylococcus aureus. J Bacteriol 189, 7343-7350.
12. CLSI (2006). Methods for Broth Dilution Susceptibility Testing of Bacteria Isolated from Aquatic Animals. Waune, PA, USA: Clinical and Laboratory Standards Institute.
13. Davila, E., Zamora, L. M., Pla, M., Carretero, C. & Parés, D. (2006). Identification and antagonistic activity of lactic acid bacteria occurring in porcine blood from industrial slaughterhouses - a preliminary study. Int J Food Microbiol 107, 207-211.
14. Deivanayagam, C. C., Rich, R. L., Carson, M., Owens, R. T., Danthuluri, S., Bice, T., Höök, M. & Narayana, S. V. (2000). Novel fold and assembly of the repetitive B region of the Staphylococcus aureus collagen-binding surface protein. Structure 8, 67-78.
15. Devriese, L. A., Hommez, J., Laevens, H., Pot, B., Vandamme, P. & Haesebrouck, F. (1999). Identification of aesculin-hydrolyzing streptococci, lactococci, aerococci and enterococci from subclinical intramammary infections in dairy cows. Vet Microbiol 70, 87-94.
16. el-Adhami, W. A., Stewart, P. R. & Matthaei, K. I. (1997). The isolation and cloning of chromosomal DNA specific for a clonal population of Staphylococcus aureus by subtractive hybridisation. J Med Microbiol 46, 987-997.
17. El-Baradei, G., Delacroix-Buchet, A. & Ogier, J. C. (2007). Biodiversity of bacterial ecosystems in traditional Egyptian Domiati cheese. Appl Environ Microbiol 73, 1248-1255.
18. Eldar, A., Ghittino, C., Asanta, L., Bozzetta, E., Goria, M., Prearo, M. & Bercovier, H. (1996). Enterococcus seriolicida is a junior synonym of Lactococcus garvieae, a causative agent of septicemia and meningoencephalitis in fish. Curr Microbiol 32, 85-88.
19. Eldar, A., Goria, M., Ghittino, C., Zlotkin, A. & Bercovier, H. (1999). Biodiversity of Lactococcus garvieae strains isolated from fish in Europe, Asia, and Australia. Appl Environ Microbiol 65, 1005-1008.
20. Elliott, J. A., Collins, M. D., Pigott, N. E. & Facklam, R. R. (1991). Differentiation of Lactococcus lactis and Lactococcus garvieae from humans by comparison of whole-cell protein patterns. J Clin Microbiol 29, 2731-2734.
21. Eyngor, M., Zlotkin, A., Ghittino, C., Prearo, M., Douet, D. G., Chilmonczyk, S. & Eldar, A. (2004). Clonality and diversity of the fish pathogen Lactococcus garvieae in Mediterranean countries. Appl Environ Microbiol 70, 5132-5137.
22. Fefer, J. J., Ratzan, K. R., Sharp, S. E. & Saiz, E. (1998). Lactococcus garvieae endocarditis: report of a case and review of the literature. Diagn Microbiol Infect Dis 32, 127-130.
23. Fihman, V., Raskine, L., Barrou, Z., Kiffel, C., Riahi, J., Berc ̧ot, B. & Sanson-Le Pors, M. J. (2006). Lactococcus garvieae endocarditis: identification by 16S rRNA and sodA sequence analysis. J Infect 52, e3-e6.
24. Flórez, A. B. & Mayo, B. (2006). Microbial diversity and succession during the manufacture and ripening of traditional, Spanish, blueveined Cabrales cheese, as determined by PCR-DGGE. Int J Food Microbiol 110, 165-171.
25. Fortina, M. G., Ricci, G., Foschino, R., Picozzi, C., Dolci, P., Zeppa, G., Cocolin, L. & Manachini, P. L. (2007). Phenotypic typing, technological properties and safety aspects of Lactococcus garvieae strains from dairy environments. J Appl Microbiol 103, 445-453.
26. Foschino, R., Nucera, D., Volponi, G., Picozzi, C., Ortoffi, M. & Bottero, M. T. (2008). Comparison of Lactococcus garvieae strains isolated in northern Italy from dairy products and fishes through molecular typing. J Appl Microbiol 105, 652-662.
27. Foster, T. J. & Höök, M. (1998). Surface protein adhesins of Staphylococcus aureus. Trends Microbiol 6, 484-488.
28. Furutan, N. P., Breiman, M. A., Fischer, M. A. & Facklam, R. R. (1991). Lactococcus garvieae infection in humans: a cause of prosthetic valve endocarditis [C297]. In Proceedings of the 91st America Society of Microbiology Conference, p. 109. Dallas: American Society for Microbiology.
29. Grkovic, S., Brown, M. H. & Skurray, R. A. (2002). Regulation of bacterial drug export systems. Microbiol Mol Biol Rev 66, 671-701.
30. Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41, 95-98.
31. Hueck, C. J. (1998). Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62, 379-433.
32. James, P. R., Hardman, S. M. & Patterson, D. L. (2000). Osteomyelitis and possible endocarditis secondary to Lactococcus garvieae: a first case report. Postgrad Med J 76, 301-303.
33. Juíz-Río, S., Osorio, C. R., de Lorenzo, V. & Lemos, M. L. (2005). Subtractive hybridization reveals a high genetic diversity in the fish pathogen Photobacterium damselae subsp. piscicida: evidence of a SXT-like element. Microbiology 151, 2659-2669.
34. Kawanishi, M., Kojima, A., Ishihara, K., Esaki, H., Kijima, M., Takahashi, T., Suzuki, S. & Tamura, Y. (2005). Drug resistance and pulsed-field gel electrophoresis patterns of Lactococcus garvieae isolates from cultured Seriola (yellowtail, amberjack and kingfish) in Japan. Lett Appl Microbiol 40, 322-328.
35. Kawanishi, M., Yoshida, T., Yagashiro, S., Kijima, M., Yagyu, K., Nakai, T., Murakami, M., Morita, H. & Suzuki, S. (2006). Differences between Lactococcus garvieae isolated from the genus Seriola in Japan and those isolated from other animals (trout, terrestrial animals from Europe) with regard to pathogenicity, phage susceptibility and genetic characterization. J Appl Microbiol 101, 496-504.
36. Kawanishi, M., Yoshida, T., Kijima, M., Yagyu, K., Nakai, T., Okada, S., Endo, A., Murakami, M., Suzuki, S. & Morita, H. (2007). Characterization of Lactococcus garvieae isolated from radish and broccoli sprouts that exhibited a KG+ phenotype, lack of virulence and absence of a capsule. Lett Appl Microbiol 44, 481-487.
37. Kim, S. R., Nonaka, L. & Suzuki, S. (2004). Occurrence of tetracycline resistance genes tetM and tetS in bacteria from marine aquaculture sites. FEMS Microbiol Lett 237, 147-156.
38. Kong, J. & Josephsen, J. (2002). The ability of the plasmid-encoded restriction and modification system LlaBIII to protect Lactococcus lactis against bacteriophages. Lett Appl Microbiol 34, 249-253.
39. Kong, J., Jytte, J. & Ma, G. R. (2001). [Cloning and structure analysis of a restriction and modification system, LlaBIII from Lactococcus lactis subsp. cremoris W56]. Sheng Wu Gong Cheng Xue Bao 17, 663-668 (in Chinese).
40. Kopermsub, P. & Yunchalard, S. (2010). Identification of lactic acid bacteria associated with the production of plaa-som, a traditional fermented fish product of Thailand. Int J Food Microbiol 138, 200-204.
41. Kubota, H., Tsuji, H., Matsuda, K., Kurakawa, T., Asahara, T. & Nomoto, K. (2010). Detection of human intestinal catalase-negative, Gram-positive cocci by rRNA-targeted reverse transcription-PCR. Appl Environ Microbiol 76, 5440-5451.
42. Lai, Y. C., Yang, S. L., Peng, H. L. & Chang, H. Y. (2000). Identification of genes present specifically in a virulent strain of Klebsiella pneumoniae. Infect Immun 68, 7149-7151.
43. Llosa, M., Gomis-Rüth, F. X., Coll, M. & de la Cruz Fd, F. (2002). Bacterial conjugation: a two-step mechanism for DNA transport. Mol Microbiol 45, 1-8.
44. Martínez, J. L. & Baquero, F. (2002). Interactions among strategies associated with bacterial infection: pathogenicity, epidemicity, and antibiotic resistance. Clin Microbiol Rev 15, 647-679.
45. Michel, C., Pelletier, C., Boussaha, M., Douet, D. G., Lautraite, A. & Tailliez, P. (2007). Diversity of lactic acid bacteria associated with fish and the fish farm environment, established by amplified rRNA gene restriction analysis. Appl Environ Microbiol 73, 2947-2955.
46. Mofredj, A., Baraka, D., Kloeti, G. & Dumont, J. L. (2000). Lactococcus garvieae septicemia with liver abscess in an immunosuppressed patient. Am J Med 109, 513-514.
47. Monedero, V., Maze ́, A., Boël, G., Zu ́n ̃iga, M., Beaufils, S., Hartke, A. & Deutscher, J. (2007). The phosphotransferase system of Lactobacillus casei: regulation of carbon metabolism and connection to cold shock response. J Mol Microbiol Biotechnol 12, 20-32.
48. Mushegian, A. R., Fullner, K. J., Koonin, E. V. & Nester, E. W. (1996). A family of lysozyme-like virulence factors in bacterial pathogens of plants and animals. Proc Natl Acad Sci U S A 93, 7321-7326.
49. Neuhaus, F. C. & Baddiley, J. (2003). A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in gram-positive bacteria. Microbiol Mol Biol Rev 67, 686-723.
50. Niegowski, D. & Eshaghi, S. (2007). The CorA family: structure and function revisited. Cell Mol Life Sci 64, 2564-2574.
51. Nieto, J. M., Devesa, S., Quiroga, I. & Toranzo, A. E. (1995). Histopathology of Enterococcus sp. infection in farmed turbot (Scophthalmus maximus L.). J Fish Dis 18, 21-30.
52. Nonaka, L., Ikeno, K. & Suzuki, S. (2007). Distribution of tetracycline resistance gene, tetM, in Gram-positive and Gram-negative bacteria isolated from sediment and seawater at a coastal aquaculture site in Japan. Microbes Environ 22, 355-364.
53. O'Sullivan, D. J. & Klaenhammer, T. R. (1993). Rapid mini-prep isolation of high-quality plasmid DNA from Lactococcus and Lactobacillus spp. Appl Environ Microbiol 59, 2730-2733.
54. Olivares-Fuster, O. & Arias, C. R. (2008). Use of suppressive subtractive hybridization to identify Flavobacterium columnare DNA sequences not shared with Flavobacterium johnsoniae. Lett Appl Microbiol 46, 605-612.
55. Pallen, M. J. (2002). The ESAT-6/WXG100 superfamily - and a new Gram-positive secretion system? Trends Microbiol 10, 209-212.
56. Paludan-Müller, C., Madsen, M., Sophanodora, P., Gram, L. & Møller, P. L. (2002). Fermentation and microflora of plaa-som, a thai fermented fish product prepared with different salt concentrations. Int J Food Microbiol 73, 61-70.
57. Parsons, J. A., Bannam, T. L., Devenish, R. J. & Rood, J. I. (2007). TcpA, an FtsK/SpoIIIE homolog, is essential for transfer of the conjugative plasmid pCW3 in Clostridium perfringens. J Bacteriol 189, 7782-7790.
58. Poncet, S., Milohanic, E., Mazé, A., Nait Abdallah, J., Aké, F., Larribe, M., Deghmane, A. E., Taha, M. K., Dozot, M. & other authors (2009). Correlations between carbon metabolism and virulence in bacteria. Contrib Microbiol 16, 88-102.
59. Pot, B., Devnese, L. A., Ursi, D., Vandamme, P., Haesebrouck, F. & Kersters, K. (1996). Phenotypic identification and differentiation of Lactococcus strains isolated from animals. Syst Appl Microbiol 19, 213-222.
60. Rantsiou, K., Urso, R., Iacumin, L., Cantoni, C., Cattaneo, P., Comi, G. & Cocolin, L. (2005). Culture-dependent and -independent methods to investigate the microbial ecology of Italian fermented sausages. Appl Environ Microbiol 71, 1977-1986.
61. Ravelo, C., Magarin ̃os, B., Lo ́pez-Romalde, S., Toranzo, A. E. & Romalde, J. L. (2003). Molecular fingerprinting of fish-pathogenic Lactococcus garvieae strains by random amplified polymorphic DNA analysis. J Clin Microbiol 41, 751-756.
62. Reckseidler, S. L., DeShazer, D., Sokol, P. A. & Woods, D. E. (2001). Detection of bacterial virulence genes by subtractive hybridization: identification of capsular polysaccharide of Burkholderia pseudomallei as a major virulence determinant. Infect Immun 69, 34-44.
63. Reed, L. J. & Muench, H. (1938). A simple method of estimating fifty per cent end points. Am J Epidemiol 27, 493-497.
64. Rozen, S. & Skaletsky, H. (2000). Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132, 365-386.
65. Saier, M. H., Jr & Reizer, J. (1994). The bacterial phosphotransferase system: new frontiers 30 years later. Mol Microbiol 13, 755-764.
66. Sambrook, J. & Russell, D. W. (2001). Molecular Cloning: a Laboratory Manual, 3rd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
67. Soule, M., Cain, K., LaFrentz, S. & Call, D. R. (2005). Combining suppression subtractive hybridization and microarrays to map the intraspecies phylogeny of Flavobacterium psychrophilum. Infect Immun 73, 3799-3802.
68. Speziale, P., Raucci, G., Visai, L., Switalski, L. M., Timpl, R. & Höök, M. (1986). Binding of collagen to Staphylococcus aureus Cowan 1. J Bacteriol 167, 77-81.
69. Swoboda, J. G., Campbell, J., Meredith, T. C. & Walker, S. (2010). Wall teichoic acid function, biosynthesis, and inhibition. ChemBioChem 11, 35-45.
70. Teixeira, L. M., Merquior, V. L., Vianni, M. C., Carvalho, M. G., Fracalanzza, S. E., Steigerwalt, A. G., Brenner, D. J. & Facklam, R. R. (1996). Phenotypic and genotypic characterization of atypical Lactococcus garvieae strains isolated from water buffalos with subclinical mastitis and confirmation of L. garvieae as a senior subjective synonym of Enterococcus seriolicida. Int J Syst Bacteriol 46, 664-668.
71. Thaker, M., Spanogiannopoulos, P. & Wright, G. D. (2010). The tetracycline resistome. Cell Mol Life Sci 67, 419-431.
72. Vela, A. I., Vázquez, J., Gibello, A., Blanco, M. M., Moreno, M. A., Lie ́ bana, P., Albendea, C., Alcala ́, B., Mendez, A. & other authors (2000). Phenotypic and genetic characterization of Lactococcus garvieae isolated in Spain from lactococcosis outbreaks and comparison with isolates of other countries and sources. J Clin Microbiol 38, 3791-3795.
73. Vendrell, D., Balca ́zar, J. L., Ruiz-Zarzuela, I., de Blas, I., Girone ́s, O. and Mu ́zquiz, J. L. (2006). Lactococcus garvieae in fish: a review. Comp Immunol Microbiol Infect Dis 29, 177-198.
74. Villani, F., Aponte, M., Blaiotta, G., Mauriello, G., Pepe, O. & Moschetti, G. (2001). Detection and characterization of a bacteriocin, garviecin L1-5, produced by Lactococcus garvieae isolated from raw cow's milk. J Appl Microbiol 90, 430-439.
75. Vinh, D. C., Nichol, K. A., Rand, F. & Embil, J. M. (2006). Native-valve bacterial endocarditis caused by Lactococcus garvieae. Diagn Microbiol Infect Dis 56, 91-94.
76. Wang, C. Y., Shie, H. S., Chen, S. C., Huang, J. P., Hsieh, I. C., Wen, M. S., Lin, F. C. & Wu, D. (2007). Lactococcus garvieae infections in humans: possible association with aquaculture outbreaks. Int J Clin Pract 61, 68-73.
77. Wang, Y., Xu, Z., Jia, A., Chen, J., Mo, Z. & Zhang, X. (2009). Genetic diversity between two Vibrio anguillarum strains exhibiting different virulence by suppression subtractive hybridization. Wei Sheng Wu Xue Bao 49, 363-371.
78. Wilbring, M., Alexiou, K., Reichenspurner, H., Matschke, K. &Tugtekin, S. M. (2011). Lactococcus garvieae causing zoonotic prosthetic valve endocarditis. Clin Res Cardiol. (Epub ahead of print).
79. Winstanley, C. (2002). Spot the difference: applications of subtractivehybridisation to the study of bacterial pathogens. J Med Microbiol 51, 459-467.
80. Zechner, E. L., de la Cruz, F., Eisenbrandt, R., Grahn, A. M., Koraimann, G. & Lanka, E. & al., e. (2000). Conjugative DNA transfer processes. In The Horizontal Gene Pool: Bacterial Plasmids and Gene Spread, pp. 87-174. Edited by C. M. Thomas. Amsterdam: H. A. Publishers.
81. Zhang, Y. L., Ong, C. T. & Leung, K. Y. (2000). Molecular analysis of genetic differences between virulent and avirulent strains of Aeromonas hydrophila isolated from diseased fish. Microbiology 146, 999-1009.
82. Zlotkin, A., Eldar, A., Ghittino, C. & Bercovier, H. (1998). Identification of Lactococcus garvieae by PCR. J Clin Microbiol 36, 983-985.
83. Zuily, S., Mami, Z. & Meune, C. (2011). Lactococcus garvieae endocarditis. Arch Cardiovasc Dis 104, 138-139.