Bacterial communities associated with the ctenophores Mnemiopsis leidyi and Beroe ovata

FEMS Microbiology Ecology

Volumn 82, Issue 1, 2012, Pages 90-101

  Daniels, Camille ^a   Breitbart, Mya ^a  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

16S; Bacterial community; Ctenophore; T RFLP; Temporal

Indexed keywords

BACTERIAL DNA; RNA 16S;

BACTERIUM; CLONE; EUKARYOTE; MARINE ECOSYSTEM; MICROBIAL COMMUNITY; POLYMORPHISM; SPECIES DIVERSITY; WATER COLUMN; ZOOPLANKTON;

ANIMAL; ARTICLE; BACTERIUM; CLASSIFICATION; COMPARATIVE STUDY; CTENOPHORA; GENETICS; METAGENOME; MICROBIOLOGY; NUCLEOTIDE SEQUENCE; RESTRICTION FRAGMENT LENGTH POLYMORPHISM; RNA GENE; UNITED STATES; ZOOPLANKTON;

ANIMALS; BACTERIA; BASE SEQUENCE; CTENOPHORA; DNA, BACTERIAL; FLORIDA; GENES, RRNA; METAGENOME; POLYMORPHISM, RESTRICTION FRAGMENT LENGTH; RNA, RIBOSOMAL, 16S; WATER MICROBIOLOGY; ZOOPLANKTON;

FLORIDA [UNITED STATES]; TAMPA BAY; UNITED STATES;

ACTINIARIA; BACTERIA (MICROORGANISMS); BEROE OVATA; CTENOPHORA (COELENTERATES); EUKARYOTA; INVERTEBRATA; MNEMIOPSIS LEIDYI; OTUS;

EID: 84866048090     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1111/j.1574-6941.2012.01409.x     Document Type: Article

References (77)

1. Altschul SF, Gish W, Miller W, Myers EW & Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410.
2. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26: 32-46.
3. Anderson MJ (2006) Distance-based tests for homogeneity of multivariate dispersions. Biometrics 62: 245-253.
4. Arai MN (2005) Predation on pelagic coelenterates: a review. J Mar Biol Assoc UK 85: 523-536.
5. Bailey TG, Youngbluth MJ & Owen GP (1995) Chemical composition and metabolic rates of gelatinous zooplankton from midwater and benthic boundary layer environments off Cape Hatteras, North Carolina, USA. Mar Ecol Prog Ser 122: 121-134.
6. Bray JR & Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 27: 325-349.
7. Cassler M, Peterson CL, Ledger A, Pomponi SA, Wright AE, Winegar R, McCarthy PJ & Lopez JV (2008) Use of real-time qPCR to quantify members of the unculturable heterotrophic bacterial community in a deep sea marine sponge, Vetulina sp. Microb Ecol 55: 384-394.
8. Cavanaugh CM, Gardiner SL, Jones ML, Jannasch HW & Waterbury JB (1981) Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila: possible chemoautotrophic symbionts. Science 213: 340-342.
9. Clarke KR (1993) Nonparametric multivariate analyses of changes in community structure. Aust J Ecol 18: 117-143.
10. Cole JR, Wang Q, Cardenas E et al. (2009) The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucleic Acids Res 37: D141-D145.
11. Condon RH, Steinberg DK, Del Giorgio PA, Bouvier TC, Bronk DA, Graham WM & Ducklow HW (2011) Jellyfish blooms result in a major microbial respiratory sink of carbon in marine systems. P Natl Acad Sci USA 108: 10225-10230.
12. Daniels C, Zeifman A, Heym K, Ritchie K, Watson C, Berzins I & Breitbart M (2011) Spatial heterogeneity of bacterial communities in the mucus of Montastraea annularis. Mar Ecol Prog Ser 426: 29-40.
13. Danovaro R, Luna GM, Dell'Anno A & Pietrangeli B (2006) Comparison of two fingerprinting techniques, terminal restriction fragment length polymorphism and automated ribosomal intergenic spacer analysis, for determination of bacterial diversity in aquatic environments. Appl Environ Microbiol 72: 5982-5989.
14. Decker MB, Breitburg DL & Purcell JE (2004) Effects of low dissolved oxygen on zooplankton predation by the ctenophore Mnemiopsis leidyi. Mar Ecol Prog Ser 280: 163-172.
15. Delannoy CMJ, Houghton JDR, Fleming NEC & Ferguson HW (2011) Mauve Stingers (Pelagia noctiluca) as carriers of the bacterial fish pathogen Tenacibaculum maritimum. Aquaculture 311: 255-257.
16. Diaz RJ & Rosenberg R (2008) Spreading dead zones and consequences for marine ecosystems. Science 321: 926-929.
17. Dumont HJ, Shiganova TA & Niermann U (2004) Aquatic Invasions in the Black, Caspian, and Mediterranean Seas. Springer, Norwell, MA, pp. 322.
18. Dunn CW, Hejnol A, Matus DQ et al. (2008) Broad phylogenomic sampling improves resolution of the animal tree of life. Nature 452: 745-749.
19. Ferguson H, Delannoy C, Hay S, Nicolson J, Sutherland D & Crumlish M (2010) Jellyfish as vectors of bacterial disease for farmed salmon (Salmo salar). J Vet Diagn Invest 22: 376-382.
20. Gasca R, Suarez-Morales E & Haddock S (2007) Symbiotic associations between crustaceans and gelatinous zooplankton in deep and surface waters off California. Mar Biol 151: 233-242.
21. Ghabooli S, Shiganova T, Zhan A, Cristescu M, Eghtesadi-Araghi P & MacIsaac H (2011) Multiple introductions and invasion pathways for the invasive ctenophore Mnemiopsis leidyi in Eurasia. Biol Invasions 13: 679-690.
22. Gorokhova E, Lehtiniem M, Viitasalo-Frösen S & Haddock SHD (2009) Molecular evidence for the occurrence of ctenophore Mertensia ovum in the northern Baltic Sea and implications for current distribution of the invasive species Mnemiopsis leidyi. Limnol Oceanogr 54: 2025-2033.
23. Gupta RS & Mok A (2007) Phylogenomics and signature proteins for the alpha proteobacteria and its main groups. BMC Microbiol 7: 106.
24. Haddad A, Camacho F, Durand P & Cary SC (1995) Phylogenetic characterization of the epibiotic bacteria associated with the hydrothermal vent polychaete Alvinella pompejana. Appl Environ Microbiol 61: 1679-1687.
25. Hay S (2006) Marine ecology: gelatinous bells may ring change in marine ecosystems. Curr Biol 16: R679-R682.
26. Hentschel U, Hopke J, Horn M, Friedrich AB, Wagner M, Hacker J & Moore BS (2002) Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microbiol 68: 4431-4440.
27. Hentschel U, Usher KM & Taylor MW (2006) Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55: 167-177.
28. Hutz A, Schubert K & Overmann J (2011) Thalassospira sp. isolated from the oligotrophic eastern Mediterranean Sea exhibits chemotaxis toward inorganic phosphate during starvation. Appl Environ Microbiol 77: 4412-4421.
29. Ivanov VP, Kamakin AM, Ushivtzev VB, Shiganova TA, Zhukova O, Aladin N, Wilson SI, Harbison GR & Dumont HJ (2000) Invasion of the Caspian Sea by the comb jellyfish Mnemiopsis leidyi (Ctenophora). Biol Invasions 2: 255-258.
30. Jezbera J, Jezberova J, Brandt U & Hahn MW (2011) Ubiquity of Polynucleobacter necessarius subspecies asymbioticus results from ecological diversification. Environ Microbiol 13: 922-931.
31. Johnston AWB, Todd JD, Sun L, Nikolaidou-Katsaridou MN, Curson ARJ & Rogers R (2008) Molecular diversity of bacterial production of the climate-changing gas, dimethyl sulphide, a molecule that impinges on local and global symbioses. J Exp Bot 59: 1059-1067.
32. Kellogg CA, Lisle JT & Galkiewicz JP (2009) Culture-independent characterization of bacterial communities associated with the cold-water coral Lophelia pertusa in the northeastern Gulf of Mexico. Appl Environ Microbiol 75: 2294-2303.
33. Kersters K, Devos P, Gillis M, Swings J, Vandamme P & Stackebrandt E (2006) Introduction to the Proteobacteria. The Prokaryotes (Dworkin M, Falkow S, Rosenberg E, Schleifer KH & Stackebrandt E, eds), pp. 3-37. Springer, New York.
34. Lane DJ (1991) 16S/23S rRNA sequencing. Nucleic Acid Techniques in Bacterial Systematics (Stackebrandt E & Goodfellow M, eds), pp. 115-175. John Wiley and Sons, New York, NY.
35. Lee OO, Wang Y, Yang J, Lafi FF, Al-Suwailem A & Qian PY (2011) Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea. ISME J 5: 650-664.
36. Littman R, Willis B & Bourne D (2009) Bacterial communities of juvenile corals infected with different Symbiodinium (dinoflagellate) clades. Mar Ecol Prog Ser 389: 45-59.
37. Liu WT, Marsh TL, Cheng H & Forney LJ (1997) Characterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 63: 4516-4522.
38. Luna GM, Dell'Anno A & Danovaro R (2006) DNA extraction procedure: a critical issue for bacterial diversity assessment in marine sediments. Environ Microbiol 8: 308-320.
39. Lynam CP, Gibbons MJ, Axelsen BE, Sparks CA, Coetzee J, Heywood BG & Brierley AS (2006) Jellyfish overtake fish in a heavily fished ecosystem. Curr Biol 16: R492-R493.
40. McManus GB & Katz LA (2009) Molecular and morphological methods for identifying plankton: what makes a successful marriage? J Plankton Res 31: 1119-1129.
41. Medlin L, Elwood HJ, Stickel S & Sogin ML (1988) The characterization of enzymatically amplified eukaryotic 16S like rRNA-coding regions. Gene 71: 491-499.
42. Mills CE & Haddock SHD (2007) Ctenophora. Light and Smith's Manual: Intertidal Invertebrates of the Central California Coast, 4th edn (Carlton JT, ed), pp. 189-199. University of California Press, Berkeley, CA.
43. Moss AG, Estes AM, Muellner LA & Morgan DD (2001) Protistan epibionts of the ctenophore Mnemiopsis mccradyi Mayer. Hydrobiologia 451: 295-304.
44. Neulinger SC, Gartner A, Jarnegren J, Ludvigsen M, Lochte K & Dullo WC (2009) Tissue-associated "Candidatus Mycoplasma corallicola" and filamentous bacteria on the cold-water coral Lophelia pertusa (Scleractinia). Appl Environ Microbiol 75: 1437-1444.
45. Nyholm SV & McFall-Ngai MJ (2004) The winnowing: establishing the squid-vibrio symbiosis. Nat Rev Microbiol 2: 632-642.
46. Oguz T, Fach B & Salihoglu B (2008) Invasion dynamics of the alien ctenophore Mnemiopsis leidyi and its impact on anchovy collapse in the Black Sea. J Plankton Res 30: 1385-1397.
47. Penn K, Wu D, Eisen JA & Ward N (2006) Characterization of bacterial communities associated with deep-sea corals on Gulf of Alaska seamounts. Appl Environ Microbiol 72: 1680-1683.
48. Pitcher DG & Nicholas RA (2005) Mycoplasma host specificity: fact or fiction? Vet J 170: 300-306.
49. Podar M, Haddock SH, Sogin ML & Harbison GR (2001) A molecular phylogenetic framework for the Phylum Ctenophora using 18S rRNA genes. Mol Phylogenet Evol 21: 218-230.
50. Purcell JE (2012) Jellyfish and ctenophore blooms coincide with human proliferations and environmental perturbations. Ann Rev Mar Sci 4: 1-22.
51. Purcell JE & Arai MN (2001) Interactions of pelagic cnidarians and ctenophores with fish: a review. Hydrobiologia 451: 27-44.
52. Purcell JE, Shiganova TA, Decker MB & Houde ED (2001) The ctenophore Mnemiopsis in native and exotic habitats: US estuaries versus the Black Sea basin. Hydrobiologia 451: 145-176.
53. Ramette A (2007) Multivariate analyses in microbial ecology. FEMS Microbiol Ecol 62: 142-160.
54. Ramette A (2009) Quantitative community fingerprinting methods for estimating the abundance of operational taxonomic units in natural microbial communities. Appl Environ Microbiol 75: 2495-2505.
55. Rapoza R, Novak D & Costello JH (2005) Life-stage dependent, in situ dietary patterns of the lobate ctenophore Mnemiopsis leidyi Agassiz 1865. J Plankton Res 27: 951-956.
56. Reitzel AM, Sullivan JC, Brown BK et al. (2007) Ecological and developmental dynamics of a host-parasite system involving a sea anemone and two ctenophores. J Parasitol 93: 1392-1402.
57. Richardson AJ, Bakun A, Hays GC & Gibbons MJ (2009) The jellyfish joyride: causes, consequences and management responses to a more gelatinous future. Trends Ecol Evol 24: 312-322.
58. Ritchie KB (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322: 1-14.
59. Ritchie KB & Smith GW (2004) Microbial communities of coral surface mucopolysaccharide layers. Coral Health and Disease (Rosenberg E & Loya Y, eds), pp. 259-263. Springer-Verlag, New York.
60. Rohwer F, Seguritan V, Azam F & Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243: 1-10.
61. Rottem S (2003) Interaction of mycoplasmas with host cells. Physiol Rev 83: 417-432.
62. Schutte UM, Abdo Z, Bent SJ, Shyu C, Williams CJ, Pierson JD & Forney LJ (2008) Advances in the use of terminal restriction fragment length polymorphism (T-RFLP) analysis of 16S rRNA genes to characterize microbial communities. Appl Microbiol Biotechnol 80: 365-380.
63. Scolardi KM, Daly KL, Pakhomov EA & Torres JJ (2006) Feeding ecology and metabolism of the Antarctic cydippid ctenophore Callianira antarctica. Mar Ecol Prog Ser 317: 111-126.
64. Seibel BA & Drazen JC (2007) The rate of metabolism in marine animals: environmental constraints, ecological demands and energetic opportunities. Philos Trans R Soc Lond B Biol Sci 362: 2061-2078.
65. Shiganova TA & Dumont HJ (2011) Non-Native Species in the Southern Seas of Eurasia: Distribution, Impacts, Pathways, and Vectors. Springer Monograph Series, The Netherlands.
66. Smith K, Dodson M, Santos S, Gast R, Rogerson A, Sullivan B & Moss AG (2007) Pentapharsodinium tyrrhenicum is a parasitic dinoflagellate of the ctenophore Mnemiopsis leidyi. J Phycol 43: 119.
67. Southern EM (1979) Measurement of DNA length by gel electrophoresis. Anal Biochem 100: 319-323.
68. Taylor MW, Radax R, Steger D & Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71: 295-347.
69. Thompson FL, Chimetto LA, Cleenwerck I, Brocchi M, Willems A & De Vos P (2011) Marinomonas brasilensis sp nov., isolated from the coral Mussismilia hispida, and reclassification of Marinomonas basaltis as a later heterotypic synonym of Marinomonas communis. Int J Syst Evol Microbiol 61: 1170-1175.
70. Todd JD, Rogers R, Li YG, Wexler M, Bond PL, Sun L, Curson ARJ, Malin G, Steinke M & Johnston AWB (2007) Structural and regulatory genes required to make the gas dimethyl sulfide in bacteria. Science 315: 666-669.
71. Urios L, Michotey V, Intertaglia L, Lesongeur F & Lebaron P (2008) Nisaea denitrificans gen. nov., sp. nov. and Nisaea nitritireducens sp. nov., two novel members of the class Alphaproteobacteria from the Mediterranean Sea. Int J Syst Evol Microbiol 58: 2336-2341.
72. Vinogradov M, Sapozhnikov V & Shushkina E (1992) The Black Sea Ecosystem (in Russian). Nauka, Moscow.
73. Wang JT, Chou YJ, Chou JH, Chen CA & Chen WM (2008) Tenacibaculum aiptasiae sp. nov., isolated from a sea anemone Aiptasia pulchella. Int J Syst Evol Microbiol 58: 761-766.
74. Webster NS, Wilson KJ, Blackall LL & Hill RT (2001) Phylogenetic diversity of bacteria associated with the marine sponge Rhopaloeides odorabile. Appl Environ Microbiol 67: 434-444.
75. Webster NS, Taylor MW, Behnam F, Lucker S, Rattei T, Whalan S, Horn M & Wagner M (2009) Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ Microbiol 12: 2070-2082.
76. Wegley L, Edwards R, Rodriguez-Brito B, Liu H & Rohwer F (2007) Metagenomic analysis of the microbial community associated with the coral Porites astreoides. Environ Microbiol 9: 2707-2719.
77. Yu Y, Breitbart M, McNairnie P & Rohwer F (2006) FastGroupII: a web-based bioinformatics platform for analyses of large 16S rDNA libraries. BMC Bioinformatics 7: 57.