Pyrosequencing reveals highly diverse and species-specific microbial communities in sponges from the Red Sea

ISME Journal

Volumn 5, Issue 4, 2011, Pages 650-664

  Lee, On On ^a   Wang, Yong ^a,b   Yang, Jiangke ^a   Lafi, Feras F ^b   Al Suwailem, Abdulaziz ^b   Qian, Pei Yuan ^a  

^a HONG KONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Hong Kong)

^b KING ABDULLAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Saudi Arabia)

Author keywords

microbial community structure; pyrosequencing; sponge; sponge specific

Indexed keywords

RNA 16S; SEA WATER;

BACTERIUM; COMMUNITY STRUCTURE; MARINE ECOSYSTEM; MICROBIAL COMMUNITY; SEAWATER; SPECIES RICHNESS; SPONGE; SYMBIOSIS;

ANIMAL; ARCHAEBACTERIUM; ARTICLE; BACTERIUM; BIODIVERSITY; CLASSIFICATION; DNA SEQUENCE; GENETICS; INDIAN OCEAN; ISOLATION AND PURIFICATION; MICROBIOLOGY; PHYLOGENY; SPECIES DIFFERENCE; SPONGE (PORIFERA);

ANIMALS; ARCHAEA; BACTERIA; BIODIVERSITY; INDIAN OCEAN; PHYLOGENY; PORIFERA; RNA, RIBOSOMAL, 16S; SEAWATER; SEQUENCE ANALYSIS, DNA; SPECIES SPECIFICITY;

INDIAN OCEAN; RED SEA [INDIAN OCEAN];

ARCHAEA; BACTERIA (MICROORGANISMS); HYRTIOS ERECTUS; OTUS; STYLISSA CARTERI; XESTOSPONGIA;

EID: 79953028506     PISSN: 17517362     EISSN: 17517370     Source Type: Journal    
DOI: 10.1038/ismej.2010.165     Document Type: Article

References (73)

1. Al-Farawati R, Al-Maradni A, Niaz R. (2008). Chemical characteristics (nutrients, fecal sterols and polyaro-matic hydrocarbons) of the surface waters for Sharm Obhur, Jeddah, Eastern Coast of the Red Sea. JKAU: Mar Sci 19: 95-119.
2. Al-Harbi SM, Khomayis HS. (2005). Seasonal variations of chlorophyll a and micro-nutrients in Obhur Creek, Red Sea. JKAU: Mar Sci 16: 91-104.
3. Amann RI, Ludwig W, Schleifer KH. (1995). Phylogenetic identification and in situ detection of individual microbial cells without cultivation. Microbiol Rev 59: 143-169.
4. Baker GC, Smith JJ, Cowan DA. (2003). Review and re-analysis of domain-specific 16S primers. J Microb Methods 55: 541-555. (Pubitemid 37357207)
5. Binladen J, Gilbert MTP, Bollback JP, Panitz F, Bendixen C, Nielsen R et al. (2007). The use of coded PCR primers enables high-throughput sequencing of multiple homolog amplification products by 454 parallel sequencing. PLoS One 2: e197.
6. Borchiellini C, Chombard C, Manuel M, Alivon E, Vacelet J, Boury-Esnault N. (2004). Molecular phylogeny of Demospongiae: implications for classification and scenarios of character evolution. Mol Phyl Evol 32: 823-837. (Pubitemid 39033539)
7. Boury-Esnault N. (2006). Systematics and evolution of Demospongiae. Can J Zool 84: 205-224. (Pubitemid 43900032)
8. Claesson MJ, O'Sullivan O, Wang Q, Nikkilä J, Marchesi JR, Smidt H et al. (2009). Comparative analysis of pyrosequencing and a phylogenetic microarray for exploring microbial community structure in the human distal intestine. PLos One 4: e6669.
9. Chao A. (1984). Non-parametric estimation of the number of classes in a population. Scand J Stat 11: 265-270.
10. Chao A, Lee SM. (1992). Estimating the number of classes via sample coverage. J Ame Stat Assoc 87: 210-217.
11. Clarke KR. (1993). Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117-143. (Pubitemid 24409223)
12. Clarke KR, Warwick RM. (1994). Change in Marine Communities: An Approach to Statistical Analysis and Interpretation. Plymouth Marine Laboratory: Plymouth, United Kingdom.
13. Cole JR, Wang Q, Cardenas E, Fish J, Chai B, Farris RJ et al. (2008). The Ribosomal Database Project: improved alignments and new tools for rRNA analysis. Nucl Acids Res 37: 141-145.
14. Edgar RC. (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucl Acids Res 32: 1792-1797. (Pubitemid 38832724)
15. Eilers H, Pernthaler J, Gloeckner FO, Amann R. (2000). Culturability and in situ abundance of pelagic bacteria the north sea. Appl Environ Microbiol 66: 3044-3051. (Pubitemid 30497616)
16. Eisen JA. (2002). The complete genome sequence of the green sulfur bacterium Chlorobium tepidum. Proc Natl Acad Sci USA 99: 9509-9514. (Pubitemid 34764644)
17. Friedrich AB, Fischer I, Proksch P, Hacker J, Hentschel U. (2001). Temporal variation of the microbial commu-nity associated with the Mediterranean sponge Aplysina aerophoba. FEMS Microbiol Ecol 38: 105-113. (Pubitemid 34084864)
18. Garrity GM, Holt JG. (2001). Phylum BVII. Thermomicro-bia phy. nov. In: Boone DR, Castenholz RW, Garrity GM (eds). Bergey's Manual of Systematic Bacteriology, Vol. 1, The Archaea and the Deeply Branching and Phototrophic Bacteria, 2nd edn. Springer: New York. pp 447.
19. Garson MG, Flowers AE, Webb RI, Charan RD, McCaffrey EJ. (1998). A sponge/dinoflagellate association in the haposclerid sponge Haliclona sp.: cellular origin of cytotoxic alkaloids by Percoll density gradient fractionation. Cell Tissue Res 293: 365-373. (Pubitemid 28382984)
20. Ghiglione JF, Palacios C, Marty JC, Mével G, Labrune C, Conan P et al. (2008). Role of environmental factors for the vertical distribution (0-1000 m) ofmarine bacterial communities in the NW Mediterranean Sea. Biogeo-sciences 5: 1751-1764.
21. Giovannoni SJ, Stingl U. (2005). Molecular diversity and ecology of microbial plankton. Nature 437: 343-348. (Pubitemid 41613489)
22. Hardoim CC, Costa R, Araujo FV, Hajdu E, Peixoto R, Lins U et al. (2009). Diversity of bacteria in the marine sponge Aplysina fulva in Brazilian coastal waters. Appl Environ Microbiol 75: 3331-3343.
23. Hentschel U, Fieseler L, Wehrl M, Gernert C, Steinert M, Hacker J et al. (2003). Microbial diversity of marine sponges. In: Müller WEG (ed). Sponges (Porifera). Springer: Heidelberg, Germany. pp 59-83.
24. Hentschel U, Hopke J, Horn M, Friedrich AB, Wagner M, Hacker J et al. (2002). Molecular evidence for a uniform microbial community in sponges from differ-ent oceans. Appl Environ Microbiol 68: 4431-4440. (Pubitemid 34988126)
25. Hentschel U, Schmid M, Wanger M, Fieseler L, Gernert C, Hacker J. (2001). Isolation and phylogenetic analysis of bacteria with antimicrobial activities from the Mediterranean sponges Aplysina aerophoba and Aplysina cavernicola. FEMS Microb Ecol 35: 305-312. (Pubitemid 32320007)
26. Hughes JB, Hellmann JJ, Ricketts TH, Bohannan BJ. (2001). Counting the uncountable: statistical approaches to estimating microbial diversity. Appl Environ Microbiol 67: 4399-4406. (Pubitemid 33646064)
27. Ilan M, Gugel J, Van Soest RWM. (2004). Taxonomy, reproduction and ecology of new and known Red Sea sponges. Sarsia 89: 388-410. (Pubitemid 40141299)
28. Joachimiak MP, Weisman JL, May BCH. (2006). J Color Grid: software for the visualization of biological measure-ments. BMCBioinformatics 7: 225-229.
29. Katoh T. (2008). Recent developments in the MAFFT multiple sequence alignment program. Briefings in Bioinformatics 9: 286-298.
30. Lee EY, Lee HK, Lee YK, Sim CK, Lee JH. (2003). Diversity of symbiotic archaeal communities in marine sponges from Korea. Biomol Eng 20: 299-304. (Pubitemid 36959679)
31. Lee OO, Chui PY, Wong YH, Pawlik JR, Qian PY. (2009a). Evidence for vertical transmission of bacterial sym-bionts from adult to embryo in the Caribbean sponge Svenzea zeai. Appl Envioron Microbiol 75: 6147-6156.
32. Lee OO, Wong YH, Qian PY. (2009b). Inter-and intraspe-cific variations of bacterial communities associated with marine sponges from San Juan Island, Washing-ton. Appl Environ Microbiol 75: 3513-3521.
33. Lee OO, Yang LH, Li X, Pawlik JR, Qian PY. (2007). Surface bacterial community, fatty acid profile, and antifouling activity of two congeneric sponges from Hong Kong and the Bahamas. Mar Ecol Prog Ser 339: 25-40. (Pubitemid 47025315)
34. Liu WT, Marsh TL, Cheng H, Forney LJ. (1997). Char-acterization of microbial diversity by determining terminal restriction fragment length polymorphisms of genes encoding 16S rRNA. Appl Environ Microbiol 63: 4516-4522. (Pubitemid 27485783)
35. Liu Z, DeSantis TZ, Andersen GL, Knight R. (2008). Accurate taxonomy assignments from 16S rRNA sequences produced by highly parallel pyrosequen-cers. Nucl Acids Res 36: e120.
36. Lozupone C, Hamady M, Knight R. (2006). UniFrac\An online tool for comparing microbial community diversity in a phylogenetic context. BMC Bioinfor-matics 7: 371.
37. Lozupone C, Knight R. (2005). UniFrac: a new phyloge-netic method for comparing microbial communities. Appl Environ Microbiol 71: 8228-8235. (Pubitemid 41803949)
38. Ludwig W, Klenk HP (2001). Overview: a phylogenetic backbone and taxonomic framework for prokaryotic systematics. In: Boone DR, Castenholz RW (eds). Bergey's Manual ofSystematic Bacteriology. Springer-Verlag: Berlin. pp 49-65.
39. Macy JM, Nunan K, Hagen KD, Dixon DR, Harbour PJ, Cahill M et al. (1996). Chrysiogenes arsenatis gen. nov., sp. nov., a new arsenate-respiring bacterium isolated from gold mine wastewater. Int J Syst Bacteriol 46: 1153-1157. (Pubitemid 26339247)
40. Maldonado M, Cortadellas N, Trillas MI, Rützler K. (2005). Endosymbiotic yeast maternally transmitted in a marine sponge. Biol Bull 209: 94-106. (Pubitemid 41654917)
41. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA et al. (2005). Genome sequencing in microfabricated high-density picolitre reactors. Nature 437: 376-380. (Pubitemid 41613494)
42. Martiny JB, Bohannan BJ, Brown JH, Colwell RK, Fuhrman JA, Green JL et al. (2006). Microbial biogeography: putting microorganisms on the map. Nat Rev Micro-biol 4: 102-112. (Pubitemid 43158153)
43. Morris RM, Rappe MS, Connon SA, Vergin KL, Siebold WA, Carlson CA et al. (2002). SAR11 clade dominates ocean surface bacterioplankton communities. Nature 420: 806-810. (Pubitemid 36019626)
44. Müller WEG, Müller IM. (2003). Origin of the metazoan immune system: identification of the molecules and their functions in sponges. Integr Comp Biol 43: 281-292. (Pubitemid 36953154)
45. Oren M, Steindler L, Ilan M. (2005). Transmission, plasticity and the molecular identification of cyano-bacterial symbionts in the Red Sea sponge Diacarnus erythraenus. Mar Biol 148: 35-41. (Pubitemid 41605629)
46. Pommier T, Canback B, Riemann L, Bostrom KH, Simu K, Lundberg P et al. (2007). Global patterns of diversity and community structure in marine bacterioplankton. Mol Ecol 16: 867-880. (Pubitemid 46233106)
47. Preston CM, Wu KY, Molinski TF, DeLong EF. (1996). A psychrophilic crenarchaeon inhabits a marine sponge: Cenarchaeum symbiosum gen. nov., sp. nov. Proc Natl Acad Sci USA 93: 6241-6246. (Pubitemid 26230289)
48. Qian PY, Dobretsov S, Dahms HU, Pawlik J. (2006). Antifouling activity and microbial diversity of two congeneric sponges, Callyspongia spp. from Hong Kong and the Bahamas. Mar Ecol Prog Ser 324: 151-165. (Pubitemid 44862408)
49. Radwan M, Hanora A, Zan J, Mohamed NM, Abo-Elmatty DM, Abou-El-Ela SH et al. (2010). Bacterial commu-nity analyses of two Red Sea Sponges. Mar Biotechnol 12: 350-360.
50. Santavy DL, Willenz P, Colwell RR. (1990). Phenotypic study of bacteria associated with the Caribbean sclerosponge, Ceratoporella nicholsoni. Appl Environ Microbiol 56: 1750-1762. (Pubitemid 20202141)
51. Schloss PD, Handelsman J. (2005). Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71: 1501-1506. (Pubitemid 40396689)
52. 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 sym-bionts. Appl Environ Microbiol 74: 7694-7708.
53. Sharp KH, Eam B, Faulkner DJ, Haygood MG. (2007). Vertical transmission of diverse microbes in the tropical sponge Corticium sp. Appl Environ Microbiol 73: 622-629. (Pubitemid 46147594)
54. Simpson TL. (1984). The Cell Biology of Sponges. Springer-Verlag: New York, NY, USA.
55. Sogin ML, Morrison HG, Huber JA, Welch DM, Huse SM, Neal PR et al. (2006). Microbial diversity in the deep sea and the underexplored 'rare biosphere'. Proc Natl Acad Sci USA 103: 12115-12120. (Pubitemid 44215820)
56. Steger D, Ettinger-Epstein P, Whalan S, Hentschel U, de Nys R, Wagner M et al. (2008). Diversity and mode of transmission of ammonia-oxidizing archaea in marine sponges. Environ Microbiol 10: 1087-1094. (Pubitemid 351406093)
57. Taylor MW, Radax R, Steger D, Wagner M. (2007). Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microb Mol Biol Rev 71: 295-347. (Pubitemid 46954308)
58. Taylor MW, Schupp PJ, Dahllof I, Kjelleberg S, Steinberg PD. (2004). Host specificity in marine sponge-asso-ciated bacteria, and potential implications for marine microbial diversity. Environ Microbiol 6: 121-130. (Pubitemid 38204137)
59. Taylor MW, Schupp PJ, de Nys R, Kjelleberg S, Steinberg PD. (2005). Biogeography of bacteria associated with the marine sponge Cymbastela concentric. Environ Microbiol 7: 419-433. (Pubitemid 40290130)
60. Thacker RW, Starnes S. (2003). Host specificity of the symbiotic cyanobacterium Oscillatoria spongeliae in marine sponge, Dysides spp. Mar Biol 142: 643-648. (Pubitemid 36704438)
61. Vacelet J. (1982). Algal-sponge symbioses in the coral reef of New Caledonia: a morphological study. In: Gomez ED, Birkeland CE (eds). Proceedings of the 4th International Coral Reef Symposium, Vol. 2 Marine Sciences Center, University of the Philippines: Manila. pp 713-719.
62. Vacelet J, Donadey C. (1977). Electron microscope study of the association between some sponges and bacteria. J Exp Mar Biol Ecol 30: 301-314.
63. Venter J, Remington K, Heidelberg J, Halpern A, Rusch D, Eisen J et al. (2004). Environmental genome shotgun sequencing of the Sargasso Sea. Science 304: 66-74. (Pubitemid 38451457)
64. Vogel G. (2008). The inner lives of sponges. Science 320: 1028-1030. (Pubitemid 351929516)
65. Wang Y, Qian PY. (2009). Conservative fragments in bacterial 16S rRNA genes and primer design for 16S ribosomal DNA amplicons in metagenomic studies. PLoS ONE 4: e7401.
66. Webster NS, Cobb RE, Negri AP. (2008). Temperature thresholds for bacterial symbiosis with a sponge. ISME J 2: 830-842.
67. Webster NS, Hill RT. (2001). The culturable microbial community of the Great Barrier Reef sponge Rhopa-loeides odorabile is dominated by α-proteobacterium. Mar Biol 138: 843-851. (Pubitemid 32406429)
68. Webster NS, Negri AP, Munro MMHG, Battershill CN. (2004). Diverse microbial communities inhabit Ant-arctic sponges. Environ Microbiol 6: 288-300. (Pubitemid 38261027)
69. Webster NS, Taylor MW, Behnam F, Lücker S, Rattei T, Whalan S et al. (2010). Deep sequencing reveals exceptional diversity and modes of transmission for bacterial sponge symbionts. Environ Microb 12: 2070-2082.
70. Webster NS, Watts JEM, Hill RT. (2001). Detection and phylogenetic analysis of novel Crenarchaeote and Euryarchaeote 16S ribosomal RNA gene sequences from a Great Barrier Reef sponge. Mar Biotech 3: 600-608. (Pubitemid 34115376)
71. Wichels A, Wurtz S, Dopke H, Schutt C, Gerdts G (2006). Bacterial diversity in the breadcrumb sponge Hali-chondria panicea (Pallas). FEMS Microbiol Ecol 56: 102-118.
72. Wilkinson CR. (1984). Immunological evidence for the Precambrian origin of bacterial symbioses in marine sponges. Proc R Soc Lond B 220: 509-517. (Pubitemid 14159707)
73. Zhu P, Li Q, Wang G (2008). Unique microbial signatures of the alien Hawaiian marine sponge Suberites zeteki. Microb Ecol 55: 406-414. (Pubitemid 351421330)