Phylogenetically and Spatially Close Marine Sponges Harbour Divergent Bacterial Communities

PLoS ONE

Volumn 7, Issue 12, 2012, Pages

  Hardoim, Cristiane C P ^a   Esteves, Ana I S ^a   Pires, Francisco R ^b   Gonçalves, Jorge M S ^a   Cox, Cymon J ^a   Xavier, Joana R ^b,c   Costa, Rodrigo ^a  

^a UNIVERSITY OF ALGARVE   (Portugal)

^b UNIVERSITY OF THE AZORES   (Portugal)

^c CENTRE D ESTUDIS AVANÇATS DE BLANES CEAB CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACTINOBACTERIA; ALPHAPROTEOBACTERIA; ARTICLE; BACTERIUM IDENTIFICATION; CHLOROFLEXI; CONTROLLED STUDY; DENATURING GRADIENT GEL ELECTROPHORESIS; GAMMAPROTEOBACTERIA; HOST PATHOGEN INTERACTION; IRCINIA VARIABILIS; MARINE SPECIES; MICROBIAL COMMUNITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYMERASE CHAIN REACTION; POPULATION ABUNDANCE; RHODOVULUM; SARCOTRAGUS SPINULOSUS; SPECIES DIFFERENCE; SPECIES DIVERSITY; UNINDEXED SEQUENCE;

ANIMAL DISTRIBUTION; ANIMALS; BACTERIA; BIODIVERSITY; MOLECULAR SEQUENCE DATA; PHYLOGENY; PORIFERA; SEAWATER;

ACIDIMICROBIALES; ACTINOBACTERIA; ALPHAPROTEOBACTERIA; BACTERIA (MICROORGANISMS); CHLOROFLEXI; CHLOROFLEXI (CLASS); CHROMATIALES; GAMMAPROTEOBACTERIA; IRCINIA VARIABILIS; IRCINIDAE; PROKARYOTA; RHODOVULUM; SARCOTRAGUS;

EID: 84871657844     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0053029     Document Type: Article

References (89)

1. Taylor MW, Radax R, Steger D, Wagner M, (2007) Sponge-associated microorganisms: Evolution, ecology, and biotechnological potential. Microbiol Mol Biol R 71: 295-347.
2. Henstchel U, Piel J, Degnan SM, Taylor MW, (2012) Genomic insights into the marine sponge microbiome. Nat Rev Microbiol 10: 641-654.
3. Vacelet J, Donadey C, (1977) Electron-microscope study of association between some sponges and bacteria. J Exp Mar Biol Ecol 30: 301-314.
4. Friedrich AB, Merkert H, Fendert T, Hacker J, Proksch P, et al. (1999) Microbial diversity in the marine sponge Aplysina cavernicola (formerly Verongia cavernicola) analyzed by fluorescence in situ hybridization (FISH). Mar Biol 134: 461-470.
5. Hentschel U, Usher KM, Taylor MW, (2006) Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55: 167-177.
6. Hardoim CCP, Costa R, Araujo FV, Hajdu E, Peixoto R, et al. (2009) Diversity of bacteria in the marine sponge Aplysina fulva in Brazilian coastal waters. Appl Environ Microb 75: 3331-3343.
7. Thomas TRA, Kavlekar DP, LokaBharathi PA, (2010) Marine drugs from sponge-microbe association- A Review. Mar Drugs 8: 1417-1468.
8. Webster NS, Taylor MW, Behnam F, Lücker S, Rattei T, et al. (2010) Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ Microbiol 12: 2070-2082.
9. Lee OO, Wang Y, Yang JK, Lafi FF, Al-Suwailem A, et al. (2011) Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea. ISME J 5: 650-664.
10. Usher K, Kuo J, Fromont J, Toze S, Sutton D, (2006) Comparative morphology of five species of symbiotic and non-symbiotic coccoid Cyanobacteria. Eur J Phycol 41: 179-188.
11. Schmitt S, Weisz J, Lindquist N, Hentschel U, (2007) Vertical transmission of a phylogenetically complex microbial consortium in the viviparous sponge Ircinia felix. Appl Environ Microb 73: 2067-2078.
12. Weisz J, Hentschel U, Lindquist N, Martens C, (2007) Linking abundance and diversity of sponge-associated microbial communities to metabolic differences in host sponges. Mar Biol 152: 475-483.
13. Mohamed NM, Colman AS, Tal Y, Hill RT, (2008) Diversity and expression of nitrogen fixation genes in bacterial symbionts of marine sponges. Environ Microbiol 10: 2910-2921.
14. Mohamed N, Cicirelli E, Kan J, Chen F, Fuqua C, et al. (2008) Diversity and quorum-sensing signal production of Proteobacteria associated with marine sponges. Environ Microbiol 10: 75-86.
15. Mohamed N, Rao V, Hamann M, Kelly M, Hill R, (2008) Monitoring bacterial diversity of the marine sponge Ircinia strobilina upon transfer into aquaculture. Appl Environ Microb 74: 4133-4143.
16. Mohamed NM, Saito K, Tal Y, Hill RT, (2010) Diversity of aerobic and anaerobic ammonia-oxidizing bacteria in marine sponges. ISME J 4: 38-48.
17. Yang JK, Sun J, Lee OO, Wong YH, Qian PY, (2011) Phylogenetic diversity and community structure of sponge-associated bacteria from mangroves of the Caribbean Sea. Aquat Microb Ecol 62: 231-240.
18. Erwin PM, López-Legentil S, Gonzalez-Pech R, Turon X, (2012) A specific mix of generalists: bacterial symbionts in Mediterranean Ircinia spp. FEMS Microbiol Ecol 79: 619-637.
19. Cichewicz R, Valeriote F, Crews P, (2004) Psymberin, a potent sponge-derived cytotoxin from Psammocinia distantly related to the pederin family. Org Lett 6: 1951-1954.
20. Emura C, Higuchi R, Miyamoto T, (2006) Irciniasulfonic acid B, a novel taurine conjugated fatty acid derivative from a Japanese marine sponge, Ircinia sp. Tetrahedron 62: 5682-5685.
21. Liu Y, Zhang S, Abreu P, (2006) Heterocyclic terpenes: linear furano- and pyrroloterpenoids. Nat Prod Rep 23: 630-651.
22. Xu S, Liao X, Du B, Zhou X, Huang Q, et al. (2008) A series of new 5,6-epoxysterols from a Chinese sponge Ircinia aruensis. Steroids 73: 568-573.
23. Wätjen W, Putz A, Chovolou Y, Kampkötter A, Totzke F, et al. (2009) Hexa-, hepta- and nonaprenylhydroquinones isolated from marine sponges Sarcotragus muscarum and Ircinia fasciculata inhibit NF-kappa B signalling in H4IIE cells. J Pharm Pharmacol 61: 919-924.
24. Orhan I, Sener B, Kaiser M, Brun R, Tasdemir D, (2010) Inhibitory activity of marine sponge-derived natural products against parasitic Protozoa. Mar Drugs 8: 47-58.
25. De Rosa S, Mitova M, Tommonaro G, (2003) Marine bacteria associated with sponge as source of cyclic peptides. Biomol Eng 20: 311-316.
26. Mitova M, Tommonaro G, De Rosa S, (2003) A novel cyclopeptide from a bacterium associated with the marine sponge Ircinia muscarum. Z Naturforschung C 58c: 740-745.
27. Fisch K, Gurgui C, Heycke N, van der Sar S, Anderson S, et al. (2009) Polyketide assembly lines of uncultivated sponge symbionts from structure-based gene targeting. Nat Chem Biol 5: 494-501.
28. Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, et al. (2011) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J 6: 564-576.
29. Kvennefors ECE, Sampayo E, Ridgway T, Barnes AC, Hoegh-Guldberg O, (2010) Bacterial communities of two ubiquitous Great Barrier Reef corals reveals both site-and species-specificity of common bacterial associates. PLoS ONE 5: e10401 doi:10.1371/journal.pone.0010401.
30. Fierer N, Lauber CL, Zhou N, McDonald D, Costello EK, et al. (2010) Forensic identification using skin bacterial communities. P Natl Acad Sci USA 107: 6477-6481.
31. Arumugam M, Raes J, Pelletier E, Le Paslier D, Yamada T, et al. (2011) Enterotypes of the human gut microbiome. Nature 473: 174-180.
32. Bull AT, Stach JEM, (2007) Marine Actinobacteria: new opportunities for natural product search and discovery. Trends Microbiol 15: 491-499.
33. Webster NS, Taylor MW, (2012) Marine sponges and their microbial symbionts: love and other relationships. Environ Microbiol 14: 335-346.
34. Simister RL, Deines P, Botté ES, Webster NS, Taylor MW, (2012) Sponge-specific clusters revisited: a comprehensive phylogeny of sponge-associated microorganisms. Environ Microbiol 14: 514-524.
35. Cook SC, Bergquist PR (2002) Family Irciniidae Gray, 1867, In: Hooper JNA, van Soest RWM, editors. System Porifera: a guide to the classification of sponges. Kluwer Academic/Plenum Publishers, New York, NY. 1022-1027.
36. Erpenbeck D, Breeuwer J, van der Velde H, van Soest R, (2002) Unravelling host and symbiont phylogenies of halichondrid sponges (Demospongiae, Porifera) using a mitochondrial marker. Mar Biol 141: 377-386.
37. Wörheide G, Erpenbeck D, (2007) DNA taxonomy of sponges- progress and perspectives. J Mar Biol Assoc UK 87: 1629-1633.
38. Erpenbeck D, Duran S, Rutzler K, Paul V, Hooper JNA, et al. (2007) Towards a DNA taxonomy of Caribbean demosponges: a gene tree reconstructed from partial mitochondrial CO1 gene sequences supports previous rDNA phylogenies and provides a new perspective on the systematics of Demospongiae. J Mar Biol Assoc UK 87: 1563-1570.
39. Cardenas P, Menegola C, Rapp HT, Diaz MC (2009) Morphological description and DNA barcodes of shallow-water Tetractinellida (Porifera: Demospongiae) from Bocas del Toro, Panamá, with description of a new species. Zootaxa: 1-39.
40. Pöppe J, Sutcliffe P, Hooper JNA, Wörheide G, Erpenbeck D, (2010) CO I barcoding reveals new clades and radiation patterns of Indo-Pacific sponges of the Family Irciniidae (Demospongiae: Dictyoceratida). PLoS ONE 5: e9950 doi:10.1371/journal.pone.0009950.
41. Xavier JR, Van Soest RWM, Breeuwer JAJ, Martins AMF, Menken SBJ, (2010) Phylogeography, genetic diversity and structure of the poecilosclerid sponge Phorbas fictitius at oceanic islands. Contrib Zool 79: 119-129.
42. Thacker R, Starnes S, (2003) Host specificity of the symbiotic cyanobacterium Oscillatoria spongeliae in marine sponges, Dysidea spp. Mar Biol 142: 643-648.
43. Montalvo NF, Hill RT, (2011) Sponge-associated bacteria are strictly maintained in two closely related but geographically distant sponge hosts. Appl Environ Microb 77: 7207-7216.
44. Santavy DL, Willenz P, Colwell RR, (1990) Phenotypic study of bacteria associated with the caribbean sclerosponge, Ceratoporella nicholsoni. Appl Environ Microb 56: 1750-1762.
45. Friedrich AB, Fischer I, Proksch P, Hacker J, Hentschel U, (2001) Temporal variation of the microbial community associated with the mediterranean sponge Aplysina aerophoba. FEMS Microbiol Ecol 38: 105-113.
46. Webster NS, Hill RT, (2001) The culturable microbial community of the Great Barrier Reef sponge Rhopaloeides odorabile is dominated by an alpha-Proteobacterium. Mar Biol 138: 843-851.
47. Vicente VP, (1990) Response of sponges with autotrophic endosymbionts during the coral-bleaching episode in Puerto Rico. Coral Reefs 8: 199-202.
48. Weisz JB, Lindquist N, Martens CS, (2008) Do associated microbial abundances impact marine demosponge pumping rates and tissue densities? Oecologia 155: 367-376.
49. Taylor MW, Schupp PJ, Dahllof I, Kjelleberg S, Steinberg PD, (2004) Host specificity in marine sponge-associated bacteria, and potential implications for marine microbial diversity. Environ Microbiol 6: 121-130.
50. Taylor MW, Schupp PJ, de Nys R, Kjelleberg S, Steinberg PD, (2005) Biogeography of bacteria associated with the marine sponge Cymbastela concentrica. Environ Microbiol 7: 419-433.
51. Fan L, Reynolds D, Liu M, Stark M, Kjelleberg S, et al. (2012) Functional equivalence and evolutionary convergence in complex communities of microbial sponge symbionts. P Natl Acad Sci USA 109: E1878-E1887.
52. Stackebrandt E, Rainey FA, Ward-Rainey NL, (1997) Proposal for a new hierarchic classification system, Actinobacteria classis nov. Int J Syst Bacteriol 47: 479-491.
53. Lee OO, Chui PY, Wong YH, Pawlik JR, Qian PY, (2009) Evidence for vertical transmission of bacterial symbionts from adult to embryo in the Caribbean sponge Svenzea zeai. Appl Environ Microb 75: 6147-6156.
54. Schmitt S, Angermeier H, Schiller R, Lindquist N, Hentschel U, (2008) Molecular microbial diversity survey of sponge reproductive stages and mechanistic insights into vertical transmission of microbial symbionts. Appl Environ Microb 74: 7694-7708.
55. Clark DA, Norris PR, (1996) Acidimicrobium ferrooxidans gen nov, sp nov: Mixed-culture ferrous iron oxidation with Sulfobacillus species. Microbiol UK 142: 785-790.
56. Clum A, Nolan M, Lang E, Del Rio TG, Tice H, et al. (2009) Complete genome sequence of Acidimicrobium ferrooxidans type strain (ICP(T)). Stand Genomic Sci 1: 38-45.
57. Davis-Belmar CS, Norris PR, (2009) Ferrous iron and pyrite oxidation by "Acidithiomicrobium" species. Adv Mater Res 71-73: 271-274.
58. Johnson DB, Bacelar-Nicolau P, Okibe N, Thomas A, Hallberg KB, (2009) Ferrimicrobium acidiphilum gen. nov., sp. nov. and Ferrithrix thermotolerans gen. nov., sp. nov.: heterotrophic, iron-oxidizing, extremely acidophilic Actinobacteria. Int J Syst Evol Micr 59: 1082-1089.
59. Imhoff JF (2005) Order I. Chromatiales ord. nov. In: Brenner DJ, Krieg NR, Staley NR, Garrity GM, editors. Bergeýs Manual of Systematic Bacteriology, 2nd edn, vol. 2 (The Proteobacteria), part B (The Gammaproteobacteria). New York: Springer. 1-3.
60. Proctor LM, (1997) Nitrogen-fixing, photosynthetic, anaerobic bacteria associated with pelagic copepods. Aquat Microb Ecol 12: 105-113.
61. Schmitt S, Deines P, Behnam F, Wagner M, Taylor MW, (2011) Chloroflexi bacteria are more diverse, abundant, and similar in high than in low microbial abundance sponges. FEMS Microbiol Ecol 78: 497-510.
62. Bruck WM, Bruck TB, Self WT, Reed JK, Nitecki SS, et al. (2010) Comparison of the anaerobic microbiota of deep-water Geodia spp. and sandy sediments in the Straits of Florida. ISME J 4: 686-699.
63. Siegl A, Hentschel U, (2010) PKS and NRPS gene clusters from microbial symbiont cells of marine sponges by whole genome amplification. Environ Microbiol Rep 2: 507-513.
64. Garrity (2006) Order III. Rhodobacterales ord. nov. In: Brenner DJ, Krieg NR, Staley NR, Garrity GM, editors. Bergeýs Manual of systematic Bacteriology, 2nd edn, vol. 2 (The Proteobacteria), part C (The Alphaproteobacteria, Betaproteobacteria, Deltaproteobacteria and Epsilonproteobacteria). New York: Springer. 161-167.
65. Hiraishi A, Ueda Y, (1995) Isolation and characterization of Rhodovulum strictum sp. nov. and some other purple nonsulfur bacteria from colored blooms in tidal and seawater pools. Int J Syst Bacteriol 45: 319-326.
66. Srinivas T, Kumar PA, Sasikala C, Ramana CV, (2007) Rhodovulum imhoffii sp. nov. Int J Syst Evol Micr 57: 228-232.
67. Imhoff JF (2005) Genus XIV. Rhodovulum Hiraishi and Ueda 1994. In: Brenner DJ, Krieg NR, Staley NR, Garrity GM, editors. Bergeýs Manual of systematic Bacteriology, 2nd edn, vol. 2 (The Proteobacteria), part C (The Alphaproteobacteria, Betaproteobacteria, Deltaproteobacteria and Epsilonproteobacteria),. New York: Springer. 205-209.
68. Brusca RC, Brusca GJ (2002) Phylum Porifera: the sponges,. In Sunauer AD, editor. Invertebrates. Sinauer Associates, Inc.,Cambridge, MA. 179-208.
69. Hentschel U, Hopke J, Horn M, Friedrich AB, Wagner M, et al. (2002) Molecular evidence for a uniform microbial community in sponges from different oceans. Appl Environ Microb 68: 4431-4440.
70. McLachlan J, (1964) Some considerations of growth of marine algae in artificial media. Can J Microbiol 10: 769-772.
71. Meyer CP, Geller JB, Paulay G, (2005) Fine scale endemism on coral reefs: Archipelagic differentiation in turbinid gastropods. Evolution 59: 113-125.
72. Folmer O, Black M, Hoeh W, Lutz R Vrijenhoek. R. 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotech 3: 294-299.
73. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.
74. Garson MJ, Flowers AE, Webb RI, Charan RD, McCaffrey EJ, (1998) A sponge/dinoflagellate association in the haplosclerid sponge Haliclona sp.: cellular origin of cytotoxic alkaloids by Percoll density gradient fractionation. Cell Tissue Res 293: 365-373.
75. Weisburg WG, Barns SM, Pelletier DA, Lane DJ, (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173: 697-703.
76. Heuer H, Krsek M, Baker P, Smalla K, Wellington EMH, (1997) Analysis of actinomycete communities by specific amplification of genes encoding 16S rRNA and gel-electrophoretic separation in denaturing gradients. Appl Environ Microb 63: 3233-3241.
77. Costa R, Götz M, Mrotzek N, Lottmann J, Berg G, et al. (2006) Effects of site and plant species on rhizosphere community structure as revealed by molecular analysis of microbial guilds. FEMS Microbiol Ecol 56: 236-249.
78. Gomes NCM, Heuer H, Schonfeld J, Costa R, Mendonça-Hagler L, et al. (2001) Bacterial diversity of the rhizosphere of maize (Zea mays) grown in tropical soil studied by temperature gradient gel electrophoresis. Plant Soil 232: 167-180.
79. Rademaker J, de Bruijn FJ (2004) Computer-assisted analysis of molecular fingerprint profiles and database construction, In: GA Kowalchuk, FJ de Bruijn, IM Head, AD Akkermans, JD van Elsas editors. Molecular Microbial Ecology Manual. Kluwer Academic Publishers, Dordrecht, The Netherlands. 1397-1446.
80. Costa R, Salles JF, Berg G, Smalla K, (2006) Cultivation-independent analysis of Pseudomonas species in soil and in the rhizosphere of field-grown Verticillium dahliae host plants. Environ Microbiol 8: 2136-2149.
81. Pruesse E, Quast C, Knittel K, Fuchs BM, Ludwig WG, et al. (2007) SILVA: a comprehensive online resource for quality checked and aligned ribosomal RNA sequence data compatible with ARB. Nucleic Acids Res 35: 7188-7196.
82. Ludwig W, Strunk O, Westram R, Richter L, Meier H, et al. (2004) ARB: a software environment for sequence data. Nucleic Acids Res 32: 1363-1371.
83. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28: 2731-2739.
84. Hardoim CCP, Cox CJ, Peixoto RS, Rosado AS, Costa R, et al. (2012) Diversity of the candidate phylum Poribacteria in the marine sponge Aplysina fulva. Braz J Microbiol. In press.
85. Keane TM, Creevey CJ, Pentony MM, Naughton TJ, McInerney JO, (2006) Assessment of methods for amino acid matrix selection and their use on empirical data shows that ad hoc assumptions for choice of matrix are not justified. BMC Evol Biol 6: 29.
86. Rodriguez F, Oliver JL, Marin A, Medina JR, (1990) The general stochastic-model of nucleotide substitution. J Theor Biol 142: 485-501.
87. Huelsenbeck JP, Ronquist F, (2001) MrBayes: Bayesian inference of phylogenetic trees. Bioinformatics 17: 754-755.
88. Ronquist F, Huelsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
89. Stamatakis A, (2006) RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22: 2688-2690.