Abstract
Red Sea sponges offer potential as sources of novel drugs and bioactive compounds. Sponges harbor diverse and abundant prokaryotic communities. The diversity of Egyptian sponge-associated bacterial communities has not yet been explored. Our study is the first culture-based and culture-independent investigation of the total bacterial assemblages associated with two Red Sea Demosponges, Hyrtios erectus and Amphimedon sp. Denaturing gradient gel electrophoresis fingerprint-based analysis revealed statistically different banding patterns of the bacterial communities of the studied sponges with H. erectus having the greater diversity. 16S rRNA clone libraries of both sponges revealed diverse and complex bacterial assemblages represented by ten phyla for H. erectus and five phyla for Amphimedon sp. The bacterial community associated with H. erectus was dominated by Deltaproteobacteria. Clones affiliated with Gammaproteobacteria were the major component of the clone library of Amphimedon sp. About a third of the 16S rRNA gene sequences in these communities were derived from bacteria that are novel at least at the species level. Although the overall bacterial communities were significantly different, some bacterial groups, including members of Alphaproteobacteria, Gammaproteobacteria, Acidobacteria, and Actinobacteria, were found in both sponge species. The culture-based component of this study targeted Actinobacteria and resulted in the isolation of 35 sponge-associated microbes. The current study lays the groundwork for future studies of the role of these diverse microbes in the ecology, evolution, and development of marine sponges. In addition, our work provides an excellent resource of several candidate bacteria for production of novel pharmaceutically important compounds.
Similar content being viewed by others
References
Abd-El-Haleem D, Moawad H, Zaki EA, Zaki S (2002) Molecular characterization of phenol-degrading bacteria isolated from different Egyptian ecosystems. Microb Ecol 43:217–224
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Burton M (1926) Report on the sponges (zoological results of the Suez Canal expedition). T Zool Soc Lond 22:71–83
Burton M (1937) Supplement to the littoral fauna of the Krusadai Island in the gulf of Manaar, Porifera. Bull Madras Govt Mus:1–58
Burton M (1952) The Mahanine expedition to the Gulf of Aqaba, sponges. Bull Br Mus Nat Hist/Zool 1:163–174
Burton M (1959) Sponges. Scientific reports of the John Murray expedition 1933–34. London. Brit Mus Nat Hist 10:151–281
Cole JR, Chai B, Marsh TL, Farris RJ, Wang Q, Kulam SA, Chandra S, McGarrell DM, Schmidt TM, Garrity GM, Tiedje JM (2003) The Ribosomal Database Project (RDP-II): previewing a new autoaligner that allows regular updates and the new prokaryotic taxonomy. Nucleic Acids Res 31:442–443
Edlund A, Hardeman F, Jansson JK, Sjoling S (2008) Active bacterial community structure along vertical redox gradients in Baltic Sea sediment. Environ Microbiol 10:2051–2063
Emura C, Higuchi R, Miyamoto T, Soest RWMV (2005) Amphimelibiosides A–F, six new ceramide dihexosides isolated from a Japanese marine sponge Amphimedon sp. J Org Chem 70:3031–3038
Enticknap JJ, Thompson R, Peraud O, Lohr JE, Hamann MT, Hill RT (2005) Molecular analysis of a Florida Keys sponge: implications for natural products discovery. Mar Biotechnol 6:S288–S293
Fieseler L, Horn M, Wagner M, Hentschel U (2004) Discovery of the novel candidate phylum Poribacteria in marine sponges. Appl Environ Microbiol 70:3724–3732
Hardoim CCP, Costa R, Araujo F, Hadju E, Peixoto R, Miranda E, Lins U, Rosado AS, Van Elsas JD (2009) Microbial diversity in the marine sponge Aplysina fulva in Brazilian coastal waters. Appl Environ Microbiol 75:3331–3343
He LM, Li Z, Wu J, Hu Y, Jiang Q (2006) Revelation and phylogenetic analysis of the predominant bacterial community associated with sponges in the South China Sea based on PCR-DGGE fingerprints. Wei Sheng Wu Xue Bao 46:487–491
Heck KL, Van Belle G, Simberloff D (1975) Explicit calculation of the rarefaction diversity measurement and the determination of sufficient sample size. Ecol 56:1459–1461
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
Hentschel U, Usher KM, Taylor MW (2006) Marine sponges as microbial fermenters. FEMS Microbiol Ecol 55:167–177
Hill M, Hill A, Lopez N, Harriott O (2006) Sponge-specific bacterial symbionts in the Caribbean sponge, Chondrilla nucula (Demospongiae, Chondrosida). Mar Biol 148:1221–1230
Hurlbet SH (1971) The nonconcept of species diversity: a critique and alternative parameters. Ecol 52:577–586
Ilan M, Gugel J, Van Soest RWM (2004) Taxonomy, reproduction and ecology of new and known Red Sea sponges. Sarsia 89:388–410
Imhoff JF, Stöhr R (2003) Sponge-associated bacteria: general overview and special aspects of bacteria associated with Halichondria panicea. Prog Mol Subcell Biol 37:35–57
Jensen PR, Mincer TJ, Williams PG, Fenical W (2005) Marine actinomycete diversity and natural product discovery. Antonie Van Leeuwenhoek 87:43–48
Jiang S, Sun W, Chen M, Dai S, Zhang L, Liu Y, Lee KJ, Li X (2007) Diversity of culturable actinobacteria isolated from marine sponge Haliclona sp. Antonie Van Leeuwenhoek 92:405–416
Keller C (1889) Die Spongienfauna des rothen Meeres. 1. Hälfte. Z Wiss Zool 48:311–405
Keller C (1891) Die Spongienfauna des rothen Meeres. 2. Hälfte. Z Wiss Zool 52:294–368
Kelly-Borges M, Vacelet J (1995) A revision of Diacarnus Burton and Negombata de Laubenfels (Demospongiae:Latrunculiidae) with descriptions from the west central Pacific and the Red Sea. Mem Queensl Mus 38:477–503
Kelman D, Kashman Y, Rosenberg E, Ilan M, Ifrach I, Loya Y (2001) Antimicrobial activity of the reef sponge Amphimedon viridis from the Red Sea: evidence for selective toxicity. Aquat Microb Ecol 24:9–16
Kennedy J, Codling CE, Dobson ADW, Jones BV, Marchesi JR (2008) Diversity of bacteria associated with an Irish marine sponge, Haliclona simulans and identification of polyketide synthase genes from the sponge metagenome. Environ Microbiol 10:1888–1902
Kobayashi J, Ishibashi M (1993) Bioactive metabolites of symbiotic marine microorganisms. Chem Rev 93:8305–8308
Koren O, Rosenberg E (2008) Bacteria associated with the bleached and cave coral Oculina patagonica. Microb Ecol 55:523–529
Lazzarini AL, Cavaletti GT, Marinelli F (2000) Rare genera of actinomycetes as potential producers of new antibiotics. Antonie Van Leeuwenhoek 78:99–405
Lévi C (1965) Spongiaires recoltés par l’ expedition israélienne dans le sud de la mer rouge. Bull Sea Fisheries Res Sta Haifa 39:3–27
Lévi C (1991) Lithistid sponges from the Norfolk Rise, recent and Mesozoic genera. In: Reitner J, Keupp H (eds) Fossil and recent sponges. Springer, Berlin
Li Z, He L, Miao X (2007) Cultivable bacterial community from South China Sea sponge as revealed by DGGE fingerprinting and 16S rDNA phylogenetic analysis. Curr Microbiol 55:465–472
Li ZY, Liu Y (2006) Marine sponge Craniella austrialiensis-associated bacterial diversity revelation based on 16S rDNA library and biologically active Actinomycetes screening, phylogenetic analysis. Lett Appl Microbiol 43:410–416
Ludwig W, Strunk O, Westram R, Richter L, Meier H, Yadhukumar BA, Lai T, Steppi S, Jobb G, Förster W, Brettske I, Gerber S, Ginhart AW, Gross O, Grumann S, Hermann S, Jost R, König A, Liss T, Lüssmann R, May M, Nonhoff B, Reichel B, Strehlow R, Stamatakis A, Stuckmann N, Vilbig A, Lenke M, Ludwig T, Bode A, Schleifer KH (2004) ARB: a software package environment for sequence data. Nucleic Acids Res 32:1363–1371
Matsunaga S, Miyata Y, Soest RWMV, Fusetani N (2004) Tetradehydrohalicyclamine A and 22-hydroxyhalicyclamine A, new cytotoxic bis-piperidine alkaloids from a marine sponge Amphimedon sp. J Nat Prod 67:1758–1760
Meyer B, Kuever J (2008) Phylogenetic diversity and spatial distribution of the microbial community associated with the Caribbean deep-water sponge Polymastia cf. corticata by 16 S rRNA, aprA, and amoA gene analysis. Microb Ecol 56:306–321
Mincer TJ, Jensen PR, Kauffman CA, Fenical W (2002) Widespread and persistent populations of a major new marine actinomycete taxon in ocean sediments. Appl Environ Microbiol 68:5005–5011
Mohamed NM, Rao V, Hamann MT, Kelly M, Hill RT (2008) Monitoring bacterial diversity of the marine sponge Ircinia strobilina upon transfer into aquaculture. Appl Environ Microbiol 74:4133–4143
Montalvo NF, Mohamed NM, Enticknap JJ, Hill RT (2005) Novel actinobacteria from marine sponges. Antonie Van Leeuwenhoek 87:29–36
Muscholl-Silberhorn A, Thiel V, Imhoff JF (2008) Abundance and bioactivity of cultured sponge-associated bacteria from the Mediterranean sea. Microb Ecol 55:94–106
Muyzer G, De Waal EC, Uitterlinden AG (1993) Profiling of complex microbial populations by denaturing gradient gel electrophoresis analysis of polymerase chain reaction amplified genes coding for 16S rRNA. Appl Environ Microbiol 59:695–700
Piel J, Hui D, Wen G, Butzke D, Platzer M, Fusetani N, Matsunaga S (2004) Antitumor polyketide biosynthesis by an uncultivated bacterial symbiont of the marine sponge Theonella swinhoei. Proc Natl Acad Sci USA 101:16222–16227
Pile AJ, Patterson MR, Witman JD (1996) In situ grazing on plankton < 10 µm by the boreal sponge Mycale lingua. Mar Ecol Prog Ser 141:95–102
Pitcher DG, Saunders NA, Owen RJ (1989) Rapid extraction of bacterial genomic DNA with guanidium thiocyanate. Lett Appl Microbiol 8:151–156
Rappe MS, Giovannoni SJ (2003) The uncultured microbial majority. Annu Rev Microbiol 57:369–394
Reysenbach AL, Giver LJ, Wickham GS, Pace NR (1992) Differential amplification of rRNA genes by polymerase chain reaction. Appl Environ Microbiol 58:3417–3418
Rohwer F, Breitbart M, Jara J, Azam F, Knowlton N (2001) Diversity of bacteria associated with the Caribbean coral Montastraea franksi. Coral Reefs 20:85–91
Rohwer F, Seguritan V, Azam F, Knowlton N (2002) Diversity and distribution of coral-associated bacteria. Mar Ecol Prog Ser 243:1–10
Row RWH (1909) Report on the sponges, collected by Mr. Cyril Crossland in 1904–5. Part I. Calcarea. J Linnean Soc (Zool) 31:181–214
Row RWH (1911) Report on the sponges, collected by Mr. Cyril Crossland in 1904–5. Part II. Non-Calcarea. J Linnean Soc (Zool) 31:287–400
Schloss PD, Larget BR, Handelsman J (2004) Integration of microbial ecology and statistics: a test to compare gene libraries. Appl Environ Microbiol 70:5485–5492
Sfanos K, Harmody D, Dang P, Ledger A, Pomponi S, McCarthy P, Lopez J (2005) A molecular systematic survey of cultured microbial associates of deep-water marine invertebrates. Syst Appl Microbiol 28:242–264
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
Shaw AK, Halpern AL, Beeson K, Tran B, Venter JC, Martiny JB (2008) It's all relative: ranking the diversity of aquatic bacterial communities. Environ Microbiol 10:2200–2210
Sundquist A, Bigdeli S, Jalili R, Druzin ML, Waller S, Pullen KM, El-Sayed YY, Taslimi MM, Batzoglou S, Ronaghi M (2007) Bacterial flora-typing with targeted, chip-based Pyrosequencing. BMC Microbiol 7:108
Takahashi Y, Kubota T, Fromont J, Kobayashi J (2009) Zamamidines a and B, new manzamine alkaloids from the sponge Amphimedon species. Org Lett 11:21–24
Taylor MW, Schupp PJ, Dahllöf 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
Taylor MW, Radax R, Steger D, Wagner M (2007) Sponge-associated microorganisms: evolution, ecology, and biotechnological potential. Microbiol Mol Biol Rev 71:295–347
Thakur NL, Anil AC (2000) Antibacterial activity of the sponge Ircinia ramosa: importance of its surface-associated bacteria. J Chem Ecol 26:57–71
Thiel V, Imhoff JF (2003) Phylogenetic identification of bacteria with antimicrobial activities isolated from Mediterranean sponges. Biomol Eng 20:421–423
Thiel V, Leininger S, Schmaljohann R, Brümmer F, Imhoff JF (2007) Sponge-specific bacterial associations of the Mediterranean sponge Chondrilla nucula (Demospongiae, Tetractinomorpha). Microb Ecol 54:101–111
Topsent E (1892) Éponges de la mer rouge. Mem Soc Zool Fr 5:21–29
Tringe SG, Hugenholtz P (2008) A renaissance for the pioneering 16S rRNA gene. Curr Opin Microbiol 11:442–446
Vacelet J, Al Sofyani A, Al Lihaibi S, Kornprobst JM (2001) A new haplosclerid sponge species from the Red Sea. J Mar Biol Assn UK 81:943–948
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
Webster NS, Negri AP, Munro MM, Battershill CN (2004) Diverse microbial communities inhabit Antarctic sponges. Environ Microbiol 6:288–300
Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703
Wilkinson CR, Nowak M, Austin B, Colwell RR (1981) Specificity of bacterial symbionts in Mediterranean and Great Barrier reef sponges. Microb Ecol 7:13–21
Williams ST, Goodfellow M, Wellington EM, Vickers JC, Alderson G, Sneath PH, Sackin MJ, Mortimer AM (1983) A probability matrix for identification of some Streptomycetes. J Gen Microbiol 129:1815–1830
Youssef DTA (2005) Hyrtioerectines A–C, cytotoxic alkaloids from the Red Sea sponge Hyrtios erectus. J Nat Prod 68:1416–1419
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
Zhang HT, Lee YK, Zhang W, Lee HK (2006) Culturable actinobacteria from the marine sponge Hymeniacidon perleve: isolation and phylogenetic diversity by 16S rRNA gene-RFLP analysis. Antonie Van Leeuwenhoek 90:159–169
Acknowledgment
This work was financially supported by the U.S.–Egypt Science and Technology Joint Fund in cooperation with the USDA and Ministry of Scientific Research in Egypt under Project (BIO8-002-011). The authors thank Matthew Anderson and Arnheidur Eythorsdottir for their help with various aspects of this work. Michelle Kelly at the National Institute of Water and Atmospheric Research (NIWA) Ltd., Auckland, New Zealand is thanked for sponge identifications.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Radwan, M., Hanora, A., Zan, J. et al. Bacterial Community Analyses of Two Red Sea Sponges. Mar Biotechnol 12, 350–360 (2010). https://doi.org/10.1007/s10126-009-9239-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10126-009-9239-5