Jellyfish-associated bacterial communities and bacterioplankton in Indonesian Marine lakes

FEMS Microbiology Ecology

Volumn 92, Issue 5, 2016, Pages

  Cleary, Daniel F R ^a   Becking, Leontine E ^b,c,d   Polónia, Ana R M ^a   Freitas, Rossana M ^a   Gomes, Newton C M ^a  

^a UNIVERSITY OF AVEIRO   (Portugal)

^b NATURALIS BIODIVERSITY CENTER   (Netherlands)

^c WAGENINGEN UNIVERSITY   (Netherlands)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Anchialine; Bacterioplankton; Mastigias; Pyrosequencing; Tripedalia

Indexed keywords

BACTERIOPLANKTON; BIVALVE; FRESHWATER ECOSYSTEM; HOST-PARASITE INTERACTION; JELLYFISH; MICROBIAL COMMUNITY; TAXONOMY;

BORNEO; INDONESIA;

ALPHAPROTEOBACTERIA; BACTERIA (MICROORGANISMS); BIVALVIA; CUBOZOA; ENTOMOPLASMATALES; GAMMAPROTEOBACTERIA; MASTIGIAS; MASTIGIAS PAPUA; MOLLICUTES; OTUS; RHODOBACTERALES; SCYPHOZOA; SPIROCHAETES; TRIPEDALIA; TRIPEDALIA CYSTOPHORA;

BACTERIAL RNA; RNA 16S;

ANIMAL; AQUATIC SPECIES; BACTERIUM; CLASSIFICATION; CNIDARIA; GENETICS; INDONESIA; ISOLATION AND PURIFICATION; LAKE; MICROBIOLOGY; PLANKTON;

ANIMALS; AQUATIC ORGANISMS; BACTERIA; CNIDARIA; INDONESIA; LAKES; PLANKTON; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S;

EID: 84964811029     PISSN: 01686496     EISSN: 15746941     Source Type: Journal    
DOI: 10.1093/femsec/fiw064     Document Type: Article

References (76)

1. Apprill A, Hughen K, Mincer T.Major similarities in the bacterial communities associated with lesioned and healthy Fungiidae corals. Environ Microbiol 2013;15:2063-72.
2. Bayer T, Neave MJ, Alsheikh-Hussain A et al. The microbiome of the Red Sea coral Stylophora pistillata is dominated by tissue-associated Endozoicomonas bacteria. Appl Environ Microb 2013;79:4759-62.
3. Becking LE. Revision of the genus Placospongia (Porifera: Hadromerida: Placospongiidae) in the Indo-West Pacific. Zookeys 2013;298:39-76.
4. Becking LE, Cleary DFR, de Voogd NJ. Sponge species composition, abundance and cover in marine lakes and coastal mangroves of Berau, Indonesia. Mar Ecol-Prog Ser 2013;481: 105-20.
5. Becking LE, de Leeuw C, Vogler C. Newly discovered "jellyfish lakes" in Misool, Raja Ampat, Papua, Indonesia. Mar Biodiv 2014;45:597-8.
6. Becking LE, Erpenbeck D, Peijnenburg KTCA et al. Phylogeography of the sponge Suberites diversicolor in Indonesia: insights into the evolution of marine lake populations. PLoS One 2013;8:e75996.
7. Becking LE, Renema W, Santodomingo NK et al. Recently discovered landlocked basins in Indonesia reveal high habitat diversity in anchialine systems. Hydrobiologia 2011;677:89-105
8. Bowen JL, Morrison HG, Hobbie JE et al. Salt marsh sediment diversity: a test of the variability of the rare biosphere among environmental replicates. ISME J 2012;6:2014-23.
9. Bhosale SH, Nagle VL, Jagtap TG. Antifouling potential of some marine organisms from India against species of Bacillus and Pseudomonas. Mar Biotechnol 2002;4:111-8.
10. Breznak JA. Phylogenetic diversity and physiology of termite gut Spirochetes. Integr Comp Biol 2002;42:313-8.
11. Caporaso JG, Kuczynski J, Stombaugh J et al. QIIME allows analysis of high-throughp community sequencing data. Nat Methods 2010;7:335-6.
12. Chen Y. Comparative genomics of methylated amine utilization by marine Roseobacter clade bacteria and development of functional gene markers (tmm, gmaS). Environ Microbiol 2012;14:2308-22.
13. Cleary DFR. An examination of scale of assessment, logging and ENSO-induced fires on butterfly diversity in Borneo. Oecologia 2003;135:313-21.
14. Cleary DFR, Becking LE, Polónia ARM et al. Composition and putative functional ecology of mussels inhabiting Indonesian marine lakes. A Van Leeuw J Microb 2015;107:821-34.
15. Cleary DFR, Becking LE, Voogd NJ et al. Habitat-and host-related variation in sponge bacterial symbiont communities in Indonesian waters. FEMS Microbiol Ecol 2013;85:465-82.
16. Cock PJ, Antao T, Chang JT et al. Biopython: freely available Python tools for computationalmolecular biology and bioinformatics. Bioinformatics 2009;25:1422-3.
17. Condon RH, Steinberg DK, Del Giorgio PA et al. Jellyfish blooms result in a major microbial respiratory sink of carbon in marine systems. P Nat Acad Sci USA 2011;108:10225-30.
18. Correa H, Haltli B, Duque C et al. Bacterial communities of the gorgonian octocoral Pseudopterogorgia elisabethae. Microb Ecol 2013;66:972-85.
19. Daniels C, Breitbart M. Bacterial communities associated with the ctenophores Mnemiopsis leidyi and Beroe ovata. FEMS Microbiol Ecol 2012;82:90-101.
20. Dawson MN, Hamner WM. Rapid evolutionary radiation of marine zooplankton in peripheral environments. P Natl Acad Sci USA 2005;102:9235-40.
21. 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.
22. DeLong EF, Preston CM, Mincer T et al. Community genomics among stratified microbial assemblages in the ocean's interior. Science 2006;311:496-503.
23. de Voogd NJ, Cleary DFR, Polónia ARM et al. Bacterial communities of four different biotopes and their functional genomic nitrogen signature from the thousand-island reef complex, West-Java, Indonesia. FEMS Microb Ecol 2015; 91, DOI: 10.1093/femsec/fiv019.
24. 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.
25. Edgar R, Haas B, Clemente J et al. UCHIME improves sensitivity and speed of chimera detection. Bioinformatics 2011;27: 2194-200.
26. Edgar RC. UPARSE: highly accurate OTU sequences from microbial amplicon reads. Nat Methods 2013;10:996-8.
27. Ferguson H, Delannoy C, Hay S et al. Jellyfish as vectors of bacterial disease for farmed salmon (Salmo salar). J Vet Diagn Invest 2010;22:376-82.
28. Fuhrman JA, Steele JA, Hewson I et al. A latitudinal diversity gradient in planktonic marine bacteria. P Natl Acad Sci USA 2008;105:7774-8.
29. Fukatsu T, Nikoh N. Endosymbiotic microbiota of the bamboo pseudococcid Antonina crawii (Insecta, Homoptera). Appl Environ Microb 2000;66:643-50.
30. Fukatsu T, Tsuchida T, Nikoh N et al. Spiroplasma symbiont of the pea aphid, Acyrthosiphon pisum (Insecta:Homoptera). Appl Environ Microb 2001;67:1284-91.
31. Funaro CF, Kronauer DJ, Moreau CS et al. Army ants harbor a host-specific clade of Entomoplasmatales bacteria. Appl Environ Microb 2011;77:346-50.
32. Garm A, Bielecki J, Petie R et al. Opposite patterns of diurnal activity in the box jellyfish Tripedalia cystophora and Copula sivickisi. Biol Bull 2012;222:35-45.
33. Genner MJ, Seehausen O, Lunt DH et al. Age of Cichlids: new dates for ancient lake fish radiations. Mol Biol Evol 2007;24:1269-82.
34. Glöckner FO, Fuchs BM, Amann R. Bacterioplankton compositions of lakes and oceans: a first comparison based on fluorescence in situ hybridization. Appl Environ Microb 1999;65:3721-6.
35. Godoy-Vitorino F, Goldfarb KC, Karaoz U et al. Comparative analyses of foregut and hindgut bacterial communities in hoatzins and cows. ISME J 2012;6:531-41.
36. Gomes NCM, Cleary DFR, Pinto FN et al. Taking root: enduring effect of rhizosphere bacterial colonization in mangroves. PLoS One 2010;5:e14065.
37. Gomes NCM, Heuer H, Schönfeld J et al. Bacterial diversity of the rhizosphere of maize (Zea mays) grown in tropical soil studied by temperature gradient gel electrophoresis. Plant Soil 2001;232:167-80.
38. Hao W, Gerdts G, Peplies J et al. Bacterial communities associated with four ctenophore genera from the German Bight (North Sea). FEMS Microbiol Ecol 2015;91, DOI: 10.1093/femsec/fiu006.
39. Hentschel U, Hopke J, Horn M et al. Molecular evidence for a uniform microbial community in sponges fromdifferent oceans. Appl Environ Microb 2002;68:4431-40.
40. Hofmann DK, Fitt WK, Fleck J. Checkpoints in the life-cycle of Cassiopea spp.: control of metagenesis and metamorphosis in a tropical jellyfish. Int J Dev Biol 1996;40:331-8.
41. Hyun DW, Shin NR, Kim MS et al. Endozoicomonas atrinae sp. nov., a bacterium isolated from the intestine of a comb pen shell Atrina pectinata. Int J Syst Evol Micr 2014;64:2312-8.
42. Kirchman DL ed. Microbial Ecology of the Oceans, 2nd edn, New Jersey: John Wiley & Sons, Inc., 2008, 606 pp.
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. Lee O, Wang Y, Yang J et al. Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea. ISME J 2011;5:650-64.
45. Legendre P, Gallagher ED. Ecologically meaningful transformations for ordination of species data. Oecologia 2001;129: 271-80.
46. Lenk S, Moraru C, Hahnke S et al. Roseobacter clade bacteria are abundant in coastal sediments and encode a novel combination of sulfur oxidation genes. ISME J 2012; 6:2178-87.
47. Lilburn TG, Schmidt TM, Breznak JA. Phylogenetic diversity of termite gut spirochaetes. Environ Microbiol 1999;1:331-45.
48. Liu J, Li F, Kim EL et al. Antibacterial polyketides from the jellyfish-derived fungus Paecilomyces variotii. J Nat Prod 2011;74:1826-9.
49. Lundgren JG, Lehman RM, Chee-Sanford J. Bacterial communities within digestive tracts of ground beetles (Coleoptera: Carabidae). Ann Entomol Soc Am 2007;100:275-82.
50. Mendoza M, Güiza L, Martinez X et al. A novel agent (Endozoicomonas elysicola) responsible for epitheliocystis in cobia Rachycentrum canadum larvae. Dis Aquat Organ 2013;106:31-7.
51. Moore CM, Mills MM, Arrigo KR et al. Processes and patterns of oceanic nutrient limitation. Nat GeoSci 2013;6:701-10.
52. Neave MJ, Michell CT, Apprill A et al. Whole-genome sequences of three symbiotic Endozoicomonas bacteria. Genome Announc 2014;2:e00802-14.
53. Niggl W, Naumann MS, Struck U et al. Organic matter release by the benthic upside-down jellyfish Cassiopea sp. fuels pelagic food webs in coral reefs. J Exp Mar Biol Ecol 2010;384:99-106.
54. NishijimaM, Adachi K, Katsuta A et al. Endozoicomonas numazuensis sp. nov., a gammaproteobacterium isolated from marine sponges, and emended description of the genus Endozoicomonas Kurahashi and Yokota 2007. Int J Syst Evol Micr 2013;63:709-14.
55. Oksanen J, Kindt R, Legendre P et al. vegan: Community Ecology Package. R package version 1.15-2. 2009, http://CRAN.Rproject.org/package=vegan (22 March 2016, date last accessed).
56. Ovchinnikova TV, Balandin SV, Aleshina GM et al. Aurelin, a novel antimicrobial peptide from jellyfish Aurelia aurita with structural features of defensins and channel-blocking toxins. Biochem Bioph Res Co 2006;348:514-23.
57. Polónia ARM, Cleary DRF, Duarte LN et al. Composition of archaea in seawater, sediment and sponges in the Kepulauan Seribu reef system, Indonesia. Microbial Ecology 2013;67: 553-67.
58. R Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing, 2013, http://www.R-project.org/(22March 2016, date last accessed).
59. 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.
60. Riemann L, Titelman J, Bamstedt U. Links between jellyfish and microbes in a jellyfish dominated fjord. Mar Ecol-Prog Ser 2006;325:29-42.
61. Schmahl G. Induction of stolon settlement in the scyphopolyps of Aurelia aurita (Cnidaria, Scyphozoa, Semaeostomeae) by glycolipids of marine bacteria. Helgoländer Meeresun 1985;39:117-27.
62. Schuett C, Doepke H. Endobiotic bacteria and their pathogenic potential in cnidarian tentacles. Helgoland Mar Res 2010;64:205-12.
63. Schuett C, Doepke H, Groepler W et al. Diversity of intra-tunical bacteria in the tunic matrix of the colonial ascidian Diplosoma migrans. Helgoland Mar Res 2005;59:136-40.
64. Sipkema D, Franssen M, Osinga R et al. Marine sponges as pharmacy. Mar Biotechnol 2005;7:142-62.
65. Sogin ML, Morrison HG, Huber JA et al. Microbial diversity in the deep sea and the underexplored 'rare biosphere'. P Natl Acad Sci USA 2006;103:12115-20.
66. Speck MD, Donachie SP. Widespread Oceanospirillaceae bacteria in Porites spp. J Mar Biol 2012;746720. http://dx.doi.org/10.1155/2012/746720 (22 March 2016, date last accessed).
67. Tinta T, Kogovšek T, Malej A et al. Jellyfish modulate bacterial dynamic and community structure. PLoS One 2012;7: e39274.
68. Titelman J, Riemann L, Sørnes TA et al. Turnover of dead jellyfish: stimulation and retardation of microbial activity. Mar Ecol-Prog Ser 2006;325:43-58.
69. Turk V, Lučić D, Flander-Putrie V et al. 2008. Feeding of Aurelia sp. (Scyphozoa) and links to themicrobial food web. Mar Ecol 2006;29:495-505.
70. Wang Q, Garrity G, Tiedje J et al. Naive bayesian classifier for rapid assignment of rRNA Sequences into the newbacterial taxonomy. Appl Environ Microb 2007;73:5261-7.
71. Weiland-Bräuer N, Neulinger SC, Pinnow N et al. Composition of bacterial communities associated with Aurelia aurita changes with compartment, life stage, and population. Appl Environ Microb 2015;81:6038-52.
72. Wiese J, Thiel V, Gärtner A et al. Kiloniella laminariae gen. nov., sp. nov., an Alphaproteobacterium from the marine macroalga Laminaria saccharina. Int J Syst Evol Micr 2009; 59:350-6.
73. Woollacott RM, Hadfield MG. Induction of metamorphosis in larvae of a sponge. Invertebr Biol 1996;115:257-62.
74. Yu Y, Lee C, Kim J et al. Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol Bioeng 2005;89:670-9.
75. Zbinden M, Cambon-Bonavita MA. Occurrence of Deferribacterales and Entomoplasmatales in the deep-sea Alvinocarid shrimp Rimicaris exoculata gut. FEMS Microbiol Eco 2003;46: 23-30.
76. Zhang Z, Schwartz S, Wagner L et al. A greedy algorithm for aligning DNA sequences. J Comput Biol 2000;7:203-14.