The taxonomic composition, characteristics, and neurotoxic activities of ribbon worm-associated bacteria from the Sea of Japan
Tóm tắt
The taxonomic composition of bacteria associated with two species of tetrodotoxin-bearing (TTX-bearing) (Hubrechtella juliae and Lineus alborostratus) and two species of non-TTX-bearing (Quasitetrastemma stimpsoni and Malacobdella grossa) ribbon worms collected from the Peter the Great Bay of Sea of Japan was studied. Bacterial isolates were identified using 16S rRNA gene sequencing and phenotypic characteristics. Thirty-eight strains of heterotrophic bacteria from the eight genera: Pseudoalteromonas, Shewanella, Ruegeria, Pseudomonas, Defluviicoccus, Vibrio, Alteromonas, and Bacillus, were isolated and characterized. γ-Proteobacteria dominated among the associated microflora of nemerteans (76.3% of the total number of isolates). Sensitivity analysis of 38 strains to antibiotics of various classes revealed multiple resistance to three or more antibiotics in all of the studied isolates. The 15 bacterial strains isolated in the study exhibited antimicrobial activities against at least one of five indicator microorganisms, most of which corresponded to the Pseudoalteromonas genus. Screening of the TTX-producing bacteria was performed using confocal laserscanning microscopy and polyclonal antibodies. A TTX-producing strain, Pseudoalteromonas sp., was found in the nemertean H. juliae. A correlation between the presence of TTX-positive microflora and the toxicity of nemerteans was determined.
Tài liệu tham khảo
Asakawa, M., Toyoshima, T., Shida, Y., et al., Paralytic toxins in a ribbon worm Cephalothrix species (Nemertean) adherent to cultured oysters in Hiroshima Bay, Hiroshima Prefecture, Japan, Toxicon, 2000, vol. 38, pp. 763–773.
Asakawa, M., Ito, K., and Kajihara, H., Highly toxic ribbon worm Cephalothrix simula containing tetrodotoxin in Hiroshima Bay, Hiroshima Prefecture, Japan, Toxins, 2013, vol. 5, pp. 376–395.
Baquero, F., Martínez, J.L., and Cantón, R., Antibiotics and antibiotic resistance in water environments, Curr. Opin. Biotechnol., 2008, vol. 19, pp. 260–265.
Beleneva, I.A., Kukhlevsky, A.D., and Kharchenko, U.V., Antimicrobial activity of heterotrophic bacterial strains of marine origin, Jundishapur J. Microbiol., 2013, vol. 6, pp. 166–175.
Beleneva, I.A., Magarlamov, T.Yu., and Kukhlevsky, A.D., Characterization, identification, and screening for tetrodotoxin production by bacteria associated with the ribbon worm (Nemertea) Cephalotrix simula (Ivata, 1952), Microbiology, 2014, vol. 83, pp. 220–226.
Carroll, S., McEvoy, E.G., and Gibson, R., The production of tetrodotoxin-like substances by nemertean worms in conjunction with bacteria, J. Exp. Mar. Biol. Ecol., 2003. vol. 288, pp. 51–63.
Chau, R., Kalaitzis, J.A., and Neilan, B.A., On the origins and biosynthesis of tetrodotoxin, Aquat. Toxicol., 2011, vol. 104, pp. 61–72.
Dubrovina, A.S., Manyakhin, A.Y., Zhuravlev, Y.N., et al., Resveratrol content and expression of phenylalanine ammonia-lyase and stilbene synthase genes in rolC transgenic cell cultures of Vitis amurensis, Appl. Microbiol. Biotechnol., 2010, vol. 88, pp. 727–736.
Giovannoni, S. and Rappe, M., Evolution, diversity, and molecular ecology of marine prokaryotes, in Microbial Ecology of the Oceans, New York: Wiley, 2000, pp. 47–84.
Haefner, B., Drugs from the deep: marine natural products as drug candidates, Drug Discovery Today, 2003, vol. 8, pp. 536–544.
Ivanova, E.P., Vysotskii, M.V., Svetashev, V.I., et al., Characterization of Bacillus strains of marine origin, Int. Microbiol., 1999, vol. 2, pp. 267–271.
Ivanova, E.P., Romanenko, L.A., Matté, M.H., et al., Retrieval of the species Alteromonas tetraodonis Simidu et al. 1990 as Pseudoalteromonas tetraodonis comb. nov. and emendation of description, Int. J. Syst. Evol. Microbiol., 2001, vol. 51, pp. 1071–1078.
Kem, W.R., Structure and action of nemertine toxins, Am. Zool., 1985, vol. 25, pp. 99–111.
Kiselev, K.V., Ageenko, N.V., and Kurilenko, V.V., Involvement of the cell-specific pigment genes pks and sult in the bacteria defense response of the sea urchin Strongylocentrotus intermedius, Dis. Aquat. Organ., 2013, vol. 103, pp. 121–132.
Lane, D.J., 16S/23S rRNA sequencing, in Nucleic Acid Techniques in Bacterial Systematics, Chichester: Wiley, 1991, pp. 115–175.
Lee, K., Choo, Y.J., Giovannoni, S.J., et al., Ruegeria pelagia sp. nov., isolated from the Sargasso Sea, Atlantic Ocean, Int. J. Syst. Evol. Microbiol., 2007, vol. 57, pp. 1815–1818.
Long, R. and Azam, F., Antagonistic interactions among marine pelagic bacteria, Appl. Environ. Microbiol., 2001, vol. 67, pp. 4975–4983.
Magarlamov, T.Yu., Shokur, O.A., and Chernyshev, A.V., Distribution of tetrodotoxin in the ribbon worm Lineus alborostratus (Takakura, 1898) (Nemertea): Immunoelectron and immunofluorescence studies, Toxicon, 2016, vol. 112, pp. 29–34.
Maszenan, A.M., Seviour, R.J., Patel, B.K., et al., Defluvicoccus vanus gen. nov., sp. nov., a novel Gramnegative coccus/coccoBacillus in the “Alphaproteobacteria” from activated sludge, Int. J. Syst. Evol. Microbiol., 2005, vol. 55, pp. 2105–2111.
McEvoy, E.G., Rogers, A., and Gibson, R., Preliminary investigation of Vibrio alginolyticus-like bacteria associated with marine nemerteans, Hydrobiologia, 1998, vol. 365, pp. 287–290.
Mikhailov, V.V., Romanenko, L.A., and Ivanova, E.P., The genus Alteromonas and related Proteobacteria, in The Prokaryotes, New York: Springer, 2002, vol. 6, pp. 597–645.
Mosher, H.S. and Furhman, F.A., Occurrence and origin of tetrodotoxin, in Seafood Toxins, Washington, DC: Am. Chem. Soc., 1984, pp. 333–344.
Pratheepa, V. and Vasconcelos, V., Microbial diversity associated with tetrodotoxin production in marine organisms, Environ. Toxicol. Pharmacol., 2013, vol. 36, pp. 1046–1054.
Romanenko, L.A., Uchinob, M., Kalinovskaya, N.I., et al., Isolation, phylogenetic analysis and screening of marine mollusc-associated bacteria for antimicrobial, hemolytic and surface activities, Microbiol. Res., 2008, vol. 163, pp. 663–644.
Saitou, N. and Nei, M., The neighbor-joining method: a new method for reconstructing phylogenetic trees, Mol. Biol. Evol., 1987, vol. 4, pp. 406–425.
Shokur, O.A., Magarlamov, T.Yu., Melnikova, D.I., et al., Life cycle of tetrodotoxin-producing Bacillus sp. on solid and liquid medium: Light and electron microscopy studies, Russ. J. Mar. Biol., 2016, vol. 42, pp. 252–257.
Sinimol, S., Sarika, A.R., and Jayakumaran, N.A., Diversity and antagonistic potential of marine microbes collected from south-west coast of India, 3 Biotech, 2016, vol. 6, p.7.
Smibert, R.M. and Krieg, N.R., Phenotypic characterization, in Methods for General and Molecular Bacteriology, Washington, DC: Am. Soc. Microbiol., 1994, pp. 607–655.
Suleria, H.A.R., Gobe, G., Masci, P., et al., Marine bioactive compounds and health promoting perspectives; innovation pathways for drug discovery, Trends Food Sci. Technol., 2016, vol. 50, pp. 44–55.
Tamura, K., Stecher, G., Peterson, D., et al., MEGA6: Molecular Evolutionary Genetics Analysis version 6.0, Mol. Biol. Evol., 2013, vol. 30, pp. 2725–2729.
Thompson, J.D., Gibson, T.J., Plewniak, F., et al., The Clustal X windows interface: Flexible strategies for multiple sequence alignment aided by quality analysis tools, Nucl. Acids Res., 1997. vol. 25, pp. 4876–4882.
Thompson, F.L., Iida, T., and Swings, J., Biodiversity of vibrios, Microbiol. Mol. Biol. Rev., 2004, vol. 68, pp. 403–431.
Venkateswaran, K., Moser, D.P., Dollhopf, M.E., et al., Polyphasic taxonomy of the genus Shewanella and description of Shewanella oneidensis sp. nov., Int. J. Syst. Bacteriol., 1999, vol. 49, pp. 705–724.
von Wintersdorff, C.J.H., Penders, J., van Niekerk, J.M., et al., Dissemination of antimicrobial resistance in microbial ecosystems through horizontal gene transfer, Front. Microbiol., 2016, vol. 9, p.173.
Zaslavskaya, N.I., Akhmatova, A.F., and Chernyshev, A.V., Allozyme comparison of the species and colour morphs of the nemertean genus Quasitetrastemma Chernyshev, 2004 (Hoplonemertea: Tetrastemmatidae) from the Sea of Japan, J. Nat. Hist., 2010, vol. 44, pp. 2303–2320.
Zhang, Y.B., Li, Y., and Sun, X.L., Antibiotic resistance of bacteria isolated from shrimp hatcheries and cultural ponds on Donghai Island, China, Mar. Pollut. Bull., 2011, vol. 62, pp. 2299–2307.
