Bacterial communities associated with four ctenophore genera from the German Bight (North Sea)

FEMS Microbiology Ecology

Volumn 91, Issue 1, 2015, Pages 1-11

  Hao, Wenjin ^a   Gerdts, Gunnar ^b   Peplies, Jörg ^c   Wichels, Antje ^b  

^a BINZHOU MEDICAL UNIVERSITY   (China)

^b ALFRED WEGENER INSTITUTE FOR POLAR AND MARINE RESEARCH   (Germany)

^c RIBOCON GMBH   (Germany)

Author keywords

ARISA fingerprint; Bacterial community composition; Ctenophore; Ribosomal amplicon pyrosequencing

Indexed keywords

ABUNDANCE; AQUATIC ORGANISM; AUTOMATION; BACTERIUM; CILIATE; COMMUNITY COMPOSITION; DOMINANCE; JELLYFISH; MOLECULAR ANALYSIS;

ATLANTIC OCEAN; GERMAN BIGHT; GERMANY; HELGOLAND; NORTH FRISIAN ISLANDS; NORTH SEA; SCHLESWIG-HOLSTEIN;

ALPHAPROTEOBACTERIA; BACTERIA (MICROORGANISMS); BEROE; BOLINOPSIS INFUNDIBULUM; CTENOPHORA (COELENTERATES); GAMMAPROTEOBACTERIA; MARINOMONAS; MNEMIOPSIS LEIDYI; PLEUROBRACHIA PILEUS; PROTEOBACTERIA; PSEUDOALTEROMONAS; PSYCHROBACTER; SCYPHOZOA; THALASSOSPIRA;

RIBOSOMAL SPACER DNA; RNA 16S; SEA WATER;

ALPHAPROTEOBACTERIA; ANIMAL; CTENOPHORA; DNA SEQUENCE; ECOSYSTEM; GAMMAPROTEOBACTERIA; GENETICS; MICROBIAL CONSORTIUM; MICROBIOLOGY; NORTH SEA; NUCLEOTIDE SEQUENCE; PROTEOBACTERIA; SPECIES DIFFERENCE;

ALPHAPROTEOBACTERIA; ANIMALS; BASE SEQUENCE; CTENOPHORA; DNA, RIBOSOMAL SPACER; ECOSYSTEM; GAMMAPROTEOBACTERIA; MICROBIAL CONSORTIA; NORTH SEA; PROTEOBACTERIA; RNA, RIBOSOMAL, 16S; SEAWATER; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

EID: 84938785058     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1093/femsec/fiu006     Document Type: Article

References (87)

1. Beardsley C, Pernthaler J,Wosniok W, et al.Are readily culturable bacteria in coastal North Sea waters suppressed by selective grazing mortality? App Environ Microb 2003;69:2624-30.
2. Bernardet J-F, Nakagawa Y. An introduction to the family Flavobacteriaceae. In: Dworkin M, Falkow S, Rosenberg E, et al. (eds). The Prokaryotes. New York: Springer, 2006, 455-80.
3. Bickel SL, Tang KW. Zooplankton-associated and free-living bacteria in the York River, Chesapeake Bay: comparison of seasonal variations and controlling factors. Hydrobiologia 2014;722:305-18.
4. Boersma M, Malzahn AM, Greve W, et al. The first occurrence of the ctenophore Mnemiopsis leidyi in the North Sea. Helgoland Mar Res 2007;61:153-5.
5. Bowman J. Bioactive compound synthetic capacity and ecological significance of marine bacterial genus Pseudoalteromonas. Mar Drugs 2007;5:220-41.
6. Brodeur RD, Sugisaki H, Hunt J, et al. Increases in jellyfish biomass in the Bering Sea: implications for the ecosystem. Mar Ecol-Prog Ser 2002;233:89-103.
7. Brown M. Coupling 16S-ITS rDNA clone libraries and automated ribosomal intergenic spacer analysis to show marine microbial diversity development and application to a time series. Environ Microbiol 2005;7:1466-79.
8. Byern J, Mills C, Flammang P. Bonding tactics in ctenophores-morphology and function of the colloblast system. In: Byern J, Grunwald I (eds). Biological Adhesive Systems. Vienna: Springer, 2010, 29-40.
9. Chimetto LA, Cleenwerck I, Brocchi M, et al.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 Micr 2011;61:1170-5.
10. Clarke K, Gorley R. PRIMER v6: User Manual/Tutorial. Plymouth, UK: PRIMER-E, 2006.
11. Clarke KR, Warwick RM. Change in Marine Communities: An Approach to Statistical Analysis and Interpretation, 2nd edn. Plymouth, UK: Primer-E Ltd, 2001.
12. Condon RH, Steinberg D. Development, biological regulation, and fate of ctenophore blooms in the York River estuary, Chesapeake Bay. Mar Ecol-Prog Ser 2008;369:153-68.
13. Condon RH, Duarte CM, Pitt KA, et al. Recurrent jellyfish blooms are a consequence of global oscillations. P Natl Acad Sci USA 2013;110:1000-5.
14. Condon RH, Steinberg DK, del Giorgio PA, et al. Jellyfish blooms result in a major microbial respiratory sink of carbon in marine systems. P Natl Acad Sci USA 2011;108:10225-30.
15. Daniels C, Breitbart M. Bacterial communities associated with the ctenophores Mnemiopsis leidyi and Beroe ovata. FEMS Microbiol Ecol 2012;82:90-101.
16. Delannoy CMJ, Houghton JDR, Fleming NEC, et al. Mauve Stingers (Pelagia noctiluca) as carriers of the bacterial fish pathogen Tenacibaculum maritimum. Aquaculture 2011;311:255-7.
17. Denner EBM, Mark B, Busse H-J, et al. Psychrobacter proteolyticus sp. nov., a psychrotrophic, halotolerant bacterium isolated from the Antarctic krill Euphausia superba Dana, excreting a cold-adapted metalloprotease. Syst Appl Microbiol 2001;24:44-53.
18. Dinasquet J, Granhag L, Riemann L. Stimulated bacterioplankton growth and selection for certain bacterial taxa in the vicinity of the ctenophore Mnemiopsis leidyi. Front Microbiol 2012;3:302, doi:10.3389/fmicb.2012.00302.
19. Eilers H, Pernthaler J, Amann R. Succession of pelagic marine bacteria during enrichment: a close look at cultivationinduced shifts. Appl Environ Microb 2000;66:4634-40.
20. Eilers H, Pernthaler J, Glöckner FO, et al. Culturability and in situ abundance of pelagic bacteria from the North Sea. Appl Environ Microb 2000;66:3044-51.
21. Eilers H, Pernthaler J, Peplies J, et al. Isolation of novel pelagic bacteria fromthe German Bight and their seasonal contributions to surface picoplankton. Appl EnvironMicrob 2001;67:5134-42.
22. Faasse MA, Bayha KM. The ctenophore Mnemiopsis leidyi A. Agassiz 1865 in coastal waters of the Netherlands: an unrecognized invasion. Aquat Invasions 2006;1:270-7.
23. Ferguson HW, Christian MJD, Hay S, et al. Jellyfish as vectors of bacterial disease for farmed salmon (Salmo salar). J Vet Diagn Invest 2010;22:376-82.
24. Fisher MM, Triplett EW. Automated approach for ribosomal intergenic spacer analysis of microbial diversity and its applications to freshwater bacterial communities. Appl EnvironMicrobiol 1999;65:4630-6.
25. Frias-Lopez J, Klaus JS, Bonheyo GT, et al. Bacterial community associated with black band disease in corals. Appl EnvironMicrob 2004;70:5955-62.
26. Friedrich AB, Fischer I, Proksch P, et al. Temporal variations of themicrobial community associated with theMediterranean sponge Aplysina aerophoba. FEMS Microbiol Ecol 2001;38:105-13.
27. Fuentes VL, Angel DL, Bayha KM, et al. Blooms of the invasive ctenophore, Mnemiopsis leidyi, span the Mediterranean Sea in 2009. Hydrobiologia 2010;645:23-37.
28. Gawel NJ, Jarret RL. A modified CTAB DNA extraction procedure for Musa and Ipomoea. Plant Mol Biol Rep 1991;9:262-6.
29. Gerdts G, Wichels A, Döpke H, et al. 40-year long-term study of microbial parameters near Helgoland (German Bight, North Sea): historical view and future perspectives. Helgoland Mar Res 2004;58:230-42.
30. GESAMP, Opportunistic settlers and the problem of the ctenophore Mnemiopsis leidyi invasion in the Black Sea. Reports and Studies 58, International Martime Organisation London 1997.
31. Ghabooli S, Shiganova T, Zhan A, et al. Multiple introductions and invasion pathways for the invasive ctenophore Mnemiopsis leidyi in Eurasia. Biol Invasions 2011;13:679-90.
32. Graham W, Bayha K. Biological invasions by marine Jellyfish. In: NentwigW(eds). Biological Invasions, Vol. 193. Berlin, Heidelberg: Springer, 2007, 239-55.
33. Greve W. Cultivation experiments on North Sea ctenophores. Helgoland Wiss Meer 1970;20:304-17.
34. Greve W. Phylum Ctenophora. Fiches identification zooplankton. 1975;146:1-6.
35. Hamer HH, Malzahn AM, Boersma M. The invasive ctenophore Mnemiopsis leidyi: a threat to fish recruitment in the North Sea? J Plankton Res 2011;33:137-44.
36. Hansson LJ, Norrman B. Release of dissolved organic carbon (DOC) by the scyphozoan jellyfish Aurelia aurita and its potential influence on the production of planktic bacteria. Mar Biol 1995;121:527-32.
37. Heindl H, Wiese J, Thiel V, et al. Phylogenetic diversity and antimicrobial activities of bryozoan-associated bacteria isolated from Mediterranean and Baltic Sea habitats. Syst Appl Microbiol 2010;33:94-104.
38. Heuchert A, Glöckner FO, Amann R, et al. Psychrobacter nivimaris sp. nov., a heterotrophic bacterium attached to organic particles isolated from the South Atlantic (Antarctica). Syst Appl Microbiol 2004;27:399-406.
39. Holmström C, Egan S, Franks A, et al. Antifouling activities expressed by marine surface associated Pseudoalteromonas species. FEMS Microbiol Ecol 2002;41:47-58.
40. Holmström C, Kjelleberg S. Marine Pseudoalteromonas species are associated with higher organisms and produce biologically active extracellular agents. FEMS Microbiol Ecol 1999;30:285-93.
41. Hütz A, Schubert K, Overmann J. Thalassospira sp. isolated from the oligotrophic eastern mediterranean sea exhibits chemotaxis toward Inorganic phosphate during starvation. Appl Environ Microb 2011;77:4412-21.
42. Ionescu D, Siebert C, Polerecky L, et al. Microbial and chemical characterization of underwater fresh water springs in the Dead Sea. PLoS ONE 2012;7:e38319, doi:10.1371/journal.pone.0038319.
43. Kittelmann S, Harder T. Species-and site-specific bacterial communities associated with four encrusting bryozoans from the North Sea, Germany. J Exp Mar Biol Ecol 2005;327: 201-9.
44. Kodama Y, Stiknowati LI, Ueki A, et al. Thalassospira tepidiphila sp. nov., a polycyclic aromatic hydrocarbon-degrading bacterium isolated from seawater. Int J Syst Evol Micr 2008;58:711-5.
45. Kovacs A. A systematic assessment of automated ribosomal intergenic spacer analysis (ARISA) as a tool for estimating bacterial richness. Res Microbiol 2010;161:192-7.
46. Krause E, Wichels A, Giménez L, et al. Small Changes in pH have direct effects on marine bacterial community composition: a microcosm approach. PLoS ONE 2012;7:e47035, doi:10.1371/journal.pone.0047035.
47. Li Z, Hu Y, Liu Y, et al. 16S rDNA clone library-based bacterial phylogenetic diversity associated with three South China Sea sponges. World J Microb Biot 2007;23:1265-72.
48. Lucas-Elio P, Hernandez P, Sanchez-Amat A, et al. Purification and partial characterization of marinocine, a new broadspectrum antibacterial protein produced by Marinomonas mediterranea. BBA-Gen Subjects 2005;1721:193-203.
49. Ludwig W, Strunk O, Westram R, et al. ARB: a software environment for sequence data. Nucleic Acids Res 2004;32:1363-71.
50. McFall-Ngai M, Ruby EG. Symbiont recognition and subsequent morphogenesis as early events in an animal-bacterialmutualism. Science 1991;254:1491-4.
51. Maruyama A, Honda D, Yamamoto H, et al. Phylogenetic analysis of psychrophilic bacteria isolated from the Japan Trench, including a description of the deep-sea species Psychrobacter pacificensis sp. nov. Int J Syst Evol Micr 2000;50:835-46.
52. Mills CE. Jellyfish blooms: are populations increasing globally in response to changing ocean conditions? Hydrobiologia 2001;451:55-68.
53. Mitchell SO, Baxter EJ, Rodger HD. Gill pathology in farmed salmon associated with the jellyfish Aurelia aurita. Vet Rec 2011;169:609, doi:10.1136/vr.100045.
54. Nemazie DA, Purcell JE, Glibert PM. Ammonium excretion by gelatinous zooplankton and their contribution to the ammonium requirements of microplankton in Chesapeake Bay. Mar Biol 1993;116:451-8.
55. Neulinger SC, Järnegren J, Ludvigsen M, et al. Phenotypespecific bacterial communities in the cold-water coral Lophelia pertusa (Scleractinia) and their implications for the coral's nutrition, health, and distribution. Appl EnvironMicrob 2008;74:7272-85.
56. Nyholm SV, McFall-Ngai M. The winnowing: establishing the squid-vibrio symbiosis. Nat Rev Microbiol 2004;2:632-42.
57. Pitt KA, Welsh DT, Condon RH. Influence of jellyfish blooms on carbon, nitrogen and phosphorus cycling and plankton production. Hydrobiologia 2009;616:133-49.
58. Pruesse E. SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 2007;35:71-88.
59. Pukall R, Kramer I, Rohde M, et al. Microbial diversity of cultivatable bacteria associated with the North Sea bryozoan Flustra foliacea. Syst Appl Microbiol 2001;24:623-33.
60. Purcell J, Shiganova T, Decker M, et al. The ctenophore Mnemiopsis in native and exotic habitats: U.S. estuaries versus the Black Sea basin. In: Jellyfish Blooms: Ecological and Societal Importance, Vol. 155. Netherlands: Springer, 2001, 145-76.
61. Purcell JE. Predation on zooplankton by large jellyfish, Aurelia labiata, Cyanea capillata and Aequorea aequorea, in Prince William Sound, Alaska. Mar Ecol-Prog Ser 2003;246: 137-52.
62. Purcell JE. Climate effects on formation of jellyfish and ctenophore blooms: a review. JMar Biol Assoc UK 2005;85:461-76.
63. Purcell JE. Jellyfish and ctenophore blooms coincide with human proliferations and environmental perturbations. Annu Rev Mar Sci 2012;4:209-35.
64. Purcell JE, Arai MN. Interactions of pelagic cnidarians and ctenophores with fish: a review. Hydrobiologia 2001;451:27-44.
65. Purcell JE, Uye SI, Lo WT. Anthropogenic causes of jellyfish blooms and their direct consequences for humans: A review. Mar Ecol-Prog Ser 2007;350:153-74.
66. Ranjard L, Brothier E, Nazaret S. Sequencing bands of ribosomal intergenic spacer analysis fingerprints for characterization and microscale distribution of soil bacterium populations responding to mercury spiking. Appl Environ Microb 2000;66:5334-9.
67. Rapoza R, Novak D, Costello JH. Life-stage dependent, in situ dietary patterns of the lobate ctenophore Mnemiopsis leidyi Agassiz 1865. J Plankton Res 2005;27:951-6.
68. Richardson AJ, Bakun A, Hays GC, et al. The jellyfish joyride: causes, consequences and management responses to a more gelatinous future. Trends Ecol Evol 2009;24:312-22.
69. Ritchie KB. Regulation of microbial populations by coral surfacemucus andmucus-associated bacteria. Mar Ecol-Prog Ser 2006;322:1-14.
70. Rohwer F, Seguritan V, Azam F, et al. Diversity and distribution of coral-associated bacteria. Mar Ecol-Prog Ser 2002;243:1-10.
71. Romanenko LA, Lysenko AM, Rohde M, et al. Psychrobacter maritimus sp. nov. and Psychrobacter arenosus sp. nov., isolated from coastal sea ice and sediments of the Sea of Japan. Int J Syst Evol Micr 2004;54:1741-5.
72. Sanchez-Amat A, Lucas-Elío P, Fernández E, et al. Molecular cloning and functional characterization of a unique multipotent polyphenol oxidase from Marinomonas mediterranea. Biochim Biophys Acta 2001;1547:104-16.
73. Schneider G, Behrends G. Top-down control in a neritic plankton system by Aurelia aurita medusae-a summary. Ophelia 1998;48:71-82.
74. Sharp KH, Eam B, Faulkner DJ, et al. Vertical transmission of diverse microbes in the tropical sponge Corticium sp. Appl Environ Microb 2007;73:622-9.
75. Shcherbakova VA, Chuvil'skaya NA, Rivkina EM, et al. Novel halotolerant bacterium from cryopeg in permafrost: Description of Psychrobacter muriicola sp. nov. Microbiology 2009;78:84-91.
76. Shivaji S, Reddy GSN, Suresh K, et al. Psychrobacter vallis sp. nov. and Psychrobacter aquaticus sp. nov., from Antarctica. Int J Syst Evol Micr 2005;55:757-62.
77. Solano F, Sanchez-Amat A. Studies on the phylogenetic relationships of melanogenic marine bacteria: proposal of Marinomonas mediterranea sp. nov. In J Syst Bacteriol 1999;49: 1241-6.
78. Sommer U, Stibor H, Katechakis A, et al. Pelagic food web configurations at different levels of nutrient richness and their implications for the ratio fish production: primary production. Hydrobiologia 2002;484:11-20.
79. Sullivan BK, Van Keuren D, Clancy M. Timing and size of blooms of the ctenophore Mnemiopsis leidyi in relation to temperature in Narragansett Bay, RI. Hydrobiologia 2001;451:113-20.
80. Teeling H, Fuchs BM, Becher D, et al. Substrate-controlled succession of marine bacterioplankton populations induced by a phytoplankton bloom. Science 2012;336:608-11.
81. Thakur NL, Anil AC, Muelle WEG. Culturable epibacteria of the marine sponge Ircinia fusca: temporal variations and their possible role in the epibacterial defense of the host. Aquat Microb Ecol 2004;37:295-304.
82. Thakur NL, Hentschel U, Krasko A, et al. Antibacterial activity of the sponge Suberites domuncula and its primmorphs: potential basis for epibacterial chemical defense. Aquat Microb Ecol 2003;31:77-83.
83. Wahl M, Jensen PR, Fenical W. Chemical control of bacterial epibiosis on ascidians. Mar Ecol-Prog Ser 1994;110:45-57.
84. Wahl M, Jormalainen V, Eriksson B, et al. Stress ecology in Fucus: abiotic, biotic and genetic interactions. Adv Mar Biol 2011;59:37-105.
85. Wang W, Wen B, Gasparich GE, et al. A spiroplasma associated with tremor disease in the Chinese mitten crab (Eriocheir sinensis). Microbiology 2004;150:3035-40.
86. Webster NS, Taylor MW, Behnam F, et al. Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ Microb 2010;12:2070-82.
87. Wichels A, Würtz S, Döpke H, et al. Bacterial diversity in the breadcrumb sponge Halichondria panicea (Pallas). FEMS Microbiol Ecol 2006;56:102-18.