Stimulated bacterioplankton growth and selection for certain bacterial taxa in the vicinity of the ctenophore Mnemiopsis leidyi

Frontiers in Microbiology

Volumn 3, Issue AUG, 2012, Pages

  Dinasquet, Julie ^a,b   Granhag, Lena ^c,d   Riemann, Lasse ^b  

^a LINNAEUS UNIVERSITY   (Sweden)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF GOTHENBURG   (Sweden)

^d CHALMERS UNIVERSITY OF TECHNOLOGY   (Sweden)

Author keywords

Bacterial community composition; Bacterioplankton; Ctenophore; Mnemiopsis leidyi

Indexed keywords

EID: 84875766119     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2012.00302     Document Type: Article

References (47)

1. Bernardet, J. F., and Nakagawa, Y. (2006). "An introduction to the family Flavobacteriaceae," in The Prokaryotes, eds M. Dworking, S. Falkow, E. Rosenber, K. H. Schleifer, and E. Stackebrandt (New York, NY: Springer), 455-480.
2. Berry, D., Ben Mahfoudh, K., Wagner, M., and Loy, A. (2011). Barcoded primers used in multiplex ampli-con pyrosequencing bias amplification. Appl. Environ. Microbiol. 77, 7846-7849.
3. Boström, K. H., Simu, K., Hagström, Å., and Riemann, L. (2004). Optimization of DNA extraction for quantitative marine bacterioplankton community analysis. Limnol. Oceanogr. Methods 2, 365-373.
4. Caporaso, J. G., Bittinger, K., Bushman, F. D., DeSantis, T. Z., Andersen, G. L., and Knight, R. (2010a). Pynast: a flexible tool for align ing sequences to a template alignment. Bioinformatics 26, 266-267.
5. Caporaso, J. G., Kuczynski, J., Stombaugh, J., Bittinger, K., Bushman, F. D., Costello, E. K., Fierer, N., Pena, A. G., Goodrich, J. K., Gordon, J. I., Huttley, G. A., Kelley, S. T., Knights, D., Koenig, J. E., Ley, R. E., Lozupone, C. A., McDonald, D., Muegge, B. D., Pirrung, M., Reeder, J., Sevinsky, J. R., Tumbaugh, P. J., Walters, W. A., Widmann, J., Yatsunenko, T., Zaneveld, J., and Knight, R. (2010b). QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7, 335-336.
6. Church, M. J. (2008). "Resource control of bacterial dynamics in the sea," in Microbial Ecology of the Oceans, ed D. L. Kirchman (New York, NY: Wiley-Liss), 335-382.
7. Colin, S. P., Costello, J. H., Hansson, L. J., Titelman, J., and Dabiri, J. O. (2010). Stealth predation and the predatory success of the invasive ctenophore Mnemiopsis leidyi. Proc. Natl. Acad. Sci. U.S.A. 107, 17223-17227.
8. Condon, R. H., Steinberg, D. K., del Giorgio, P. A., Bouvier, T. C., Bronk, D. A., Graham, W. M., and Ducklow, H. W. (2011). Jellyfish blooms result in a major microbial respiratory sink of carbon in marine systems. Proc. Natl. Acad. Sci. U.S.A. 108, 10225-10230.
9. Delannoy, C. M. J., Houghton, J. D. R., Fleming, N. E. C., and Ferguson, H. W. (2011). Mauve stingers (Pelagia noctiluca) as carriers of the bacterial fish pathogen Tenacibaculum mar-itimum. Aquaculture 311, 255-257.
10. DeSantis, T. Z., Hugenholtz, P., Larsen, N., Rojas, M., Brodie, E. L., Keller, K., Huber, T., Dalevi, D., Hu, P., and Andersen, G. L. (2006). Greengenes, a chimera-checked 16s rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol. 72, 5069-5072.
11. Dinasquet, J., Titelman, J., Friis-Møller, L., Setälä, O., Granhag, L., Andersen, T., Båmstedt, U., Haraldsson, M., Hosia, O., Katajisto, T., Kragh, T., Kuparinen, J., Schrøter, M.-L., Søndergaard, M., Tiselius, P., and Riemann, L. (2012). Cascading effects of the ctenophore Mnemiopsis leidyi on the planktonic food web in a nutrient-limited estuarine system. Mar. Ecol. Prog. Ser. 460, 49-61.
12. Ferguson, H. W., Delannoy, C. M. J., Hay, S., Nicolson, J., Sutherland, D., and Crumlish, M. (2010). Jellyfish as vectors of bacterial disease for farmed salmon (Salmo salar). J. Vet. Diagnos. Invest. 22, 376-382.
13. Finenko, G. A., Kideys, A. E., Anninsky, B. E., Shiganova, T. A., Roohi, A., Tabari, M. R., Rostami, H., and Bagheri, S. (2006). Invasive ctenophore Mnemiopsis leidyi in the Caspian Sea: feeding, respiration, reproduction and predatory impact on the zooplankton community. Mar. Ecol. Prog. Ser. 314, 171-185.
14. Gasol, J. M., and del Giorgio, P. A. (2000). Using flow cytometry for counting natural planktonic bacteria and understanding the structure of planktonic bacterial communities. Sci. Mar. 64, 197-224.
15. Graham, W M., Pagès, F., and Hamner, W M. (2001). A physical context for gelatinous zooplankton aggregations: a review. Hydrobiologia 451, 199-212.
16. Granhag, L., Friis Møller, L., and Hansson, L. J. (2011). Size-specific clearance rates of the ctenophore Mnemiopsis leidyi based on in situ gut content analyses. J. Plankton Res. 33,1043-1052.
17. Grossart, H.-P., Dziallas, C., Leunert, E, and Tang, K. W (2010). Bacteria dispersal by hichhiking on zooplankton. Proc. Natl. Acad. Sci. U.S.A. 107, 11959-11964.
18. Haas, B. J., Gevers, D., Earl, A. M., Feldgarden, M., Ward, D. V., Giannoukos, G., Ciulla, D., Tabbaa, D., Highlander, S. K., Sodergren, E., Methe, B., DeSantis, T. Z., Petrosino, J. F., Knight, R., and Birren, B. W (2011). Chimeric 16s rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. Genome Res. 21,494-504.
19. Handlinger, J., Soltani, M., and Percival, S. (1997). The pathology of Flexibacter maritimus in aquaculture species in tasmania, australia. J. Fish Dis. 20, 159-168.
20. Hansson, L. J., andNorrman, B. (1995). Release of dissolved organic carbon (DOC) by the scyphozoan jellyfish Aurelia aurita and its potential influence on the production of planktic bacteria. Mar. Biol. 121, 527-532.
21. Jacobsen, T. R., and Azam, F. (1984). Role of bacteria in copepod fecal pellet decomposition: colonization, growth rates and mineralization. Bull. Mar. Sci. 35, 495-502.
22. Kiørboe, T., Tang, K., Grossart, H.-P., and Ploug, H. (2003). Dynamics of microbial communities on marine snow aggregates: colonization, growth, detachment, and grazing mortality of attached bacteria. Appl. Environ. Microbiol. 69, 3036-3047.
23. Kirchman, D. L. (2002). The ecology of Cytophaga-Flavobacteria in aquatic environments. FEMS Microbiol. Ecol. 39,91-100.
24. Kremer, P. (1977). Respiration and excretion by the ctenophore Mnemiopsis leidyi. Mar. Biol. 44, 43-50.
25. Kremer, P. (1982). Effect of food avali-ability on the metabolism of the ctenophore Mnemiopsis mccradyi. Mar. Biol. 71, 149-156.
26. Kremer, P. (1994). Patterns of abundance for Mnemiopsis in U.S. coastal waters - a comparative overview. ICES I Mar. Sci. 51, 347-354.
27. Kremer, P., and Reeve, M. R. (1989). Growth dynamics of a ctenophore (Mnemiopsis) in relation to variable food supply. II. Carbon budgets and growth model. J. Plankton Res. 11, 553-574.
28. Kremer, P., Reeve, M. R., and Syms, M. A. (1986). The nutritional ecology of the ctenophore Bolinopsis vitrea: comparison with Mnemiopsis mccradyi from the same region. J. Plankton Res. 8, 1197-1208.
29. Møller, E. F., Riemann, L., and Søndergaard, M. (2007). Bacteria associated with copepods: abundance, activity and community composition. Aquat. Microb. Ecol. 47, 99-106.
30. Nemazie, D. A., Purcell, J. E., and Glibert, P. M. (1993). Ammonium excretion by gelatinous zooplank-ton and their contribution to the ammonium requirements of microplankton in Chesapeake Bay. Mar. Biol. 116,451-458.
31. Pilloni, G., Granitsiotis, M. S., Engel, M., and Lueders, T. (2012). Testing the limits of 454 pyrotag sequencing: reproducibility, quantitative assessment and comparison to t-RFLP fingerprinting of aquifer microbes. PLoS ONE 7:e40467. doi: 10.1371/journal.pone.0040467
32. Pinhassi, J., Winding, A., Binnerup, S. J., Zweifel, U. L., Riemann, B., and Hagström, A. (2003). Spatial variability in bacterioplankton community composition at the Skagerrak-Kattegat front. Mar. Ecol. Prog. Ser. 255, 1-13.
33. Pitt, K. A., Welsh, D. T., and Condon, R. H. (2009). Influence of jellyfish blooms on carbon, nitrogen and phosphorus cycling and plankton production. Hydrobiologia 616, 133-149.
34. Reeder, J., and Knight, R. (2010). Rapidly denoising pyrosequenc-ing amplicon reads by exploiting rank-abundance distributions. Nat. Methods 7, 668-669.
35. Riemann, L., Steward, G. F., and Azam, E (2000). Dynamics of bacterial community composition and activity during a mesocosm diatom bloom. Appl. Environ. Microbiol. 66, 578-587.
36. Schneider, G. (1990). A comparison of carbon based ammonia excretion rates between gelatinous and non-gelatinous zooplankton: implications and consequences. Mar. Biol. 106,219-225.
37. Shiganova, T. A., Mirzoyan, Z. A., Studenikina, E. A., Volovik, S. P., Siokou-Frangou, I., Zervoudaki, S., Christou, E. D., Skirta, A. Y., and Dumont, H. J. (2001). Population development of the invader ctenophore Mnemiopsis leidyi, in the Black Sea and in other seas of the Mediterranean basin. Mar. Biol. 139,431-445.
38. Sjöstedt, J., Koch-Schmidt, P., Pontarp, M., Canback, B., Tunlid, A., Lundberg, P., Hagström, Å., and Riemann, L. (2012). Recruitment of members from the rare biosphere of marine bacterioplankton communities after an environmental disturbance. Appl. Environ. Microbiol. 78, 1361-1369.
39. Slightom, R. N., and Buchan, A. (2009). Surface colonization by marine Roseobacters: integrating genotype and phenotype. Appl. Environ. Microbiol. 75, 6027-6037.
40. Tang, K. W. (2005). Copepods as microbial hotspots in the ocean: effects of host feeding activities on attached bacteria. Aquat. Microb. Ecol. 38,31-40.
41. Tang, K. W., Turk, V., and Grossart, H.-P. (2010). Linkage between crustacean zooplankton and aquatic bacteria. Aquat. Microb. Ecol. 61, 261-277.
42. Tendal, O. S., Jensen, K. R., and Remington, K. (2007). Invasive ctenophore Mnemiopsis leidyi widely distributed in danish waters. Aquat. Invasions 2, 455-460.
43. Tinta, T., Kogovšek, T., Malej, A., and Turk, V. (2012). Jellyfish modulate bacterial dynamic and community structure. PLoS ONE 7:e39274. doi: 10.1371/journal.pone.0039274
44. Tinta, T., Malej, A., Kos, M., and Turk, V. (2010). Degradation of the adriatic medusa Aurelia sp. by ambient bacteria. Hydrobiologia 645, 179-191.
45. Tiselius, P., and Riemann, L. (2012). Cascading effects of the ctenophore Mnemiopsis leidyi on the planktonic food web in a nutrient limited estu-arine system. Mar. Ecol. Prog. Ser. 460, 49-61.
46. Titelman, J., Riemann, L., Sörnes, T. A., Nilsen, T., Griekspoor, P., and Båmstedt, U. (2006). Turnover of dead jellyfish: stimulation and retardation of microbial activity. Mar. Ecol. Prog. Ser. 325, 43-58.
47. Wang, Q., Garrity, G. M., Tiedje, J. M., and Cole, J. R. (2007). Naive bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl. Environ. Microbiol. 73, 5261-5267.