We’re sorry, something doesn't seem to be working properly.

Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.

Skip to main content

Advertisement

SpringerLink
Log in

Diversity of culturable actinobacteria isolated from marine sponge Haliclona sp.

  • Original Paper
  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

This study describes actinobacteria isolated from the marine sponge Haliclona sp. collected in shallow water of the South China Sea. A total of 54 actinobacteria were isolated using media selective for actinobacteria. Species diversity and natural product diversity of isolates from marine sponge Haliclona sp. were analysed. Twenty-four isolates were selected on the basis of their morphology on different media and assigned to the phylum Actinobacteria by a combination of 16S rRNA gene based restriction enzymes digestion and 16S rRNA gene sequence analysis. The 16S rRNA genes of 24 isolates were digested by restriction enzymes TaqI and MspI and assigned to different groups according to their restriction enzyme pattern. The phylogenetic analysis based on 16S rRNA gene sequencing showed that the isolates belonged to the genera Streptomyces, Nocardiopsis, Micromonospora and Verrucosispora; one other isolate was recovered that does not belong to known genera based on its unique 16S rRNA gene sequence. To our knowledge, this is the first report of a bacterium classified as Verrucosispora sp. that has been isolated from a marine sponge. The majority of the strains tested belong to the genus Streptomyces and three isolates may be new species. All of the 24 isolates were screened for genes encoding polyketide synthases (PKS) and nonribosomal peptide synthetases (NRPS). PKS and NRPS sequences were detected in more than half of the isolates and the different “PKS-I—PKS-II—NRPS” combinations in different isolates belonging to the same species are indicators of their potential natural product diversity and divergent genetic evolution.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Atlas RM, Park LC (2000) Handbook of Microbiological Media, CRC Press, Inc., Boca Raton, Florida

  • Ayuso-Sacido A, Genilloud O (2005) New PCR primers for the screening of NRPS and PKS-I systems in actinomycetes: detection and distribution of these biosynthetic gene sequences in major taxonomic groups. Microb Ecol 49:10–24

    Article  PubMed  CAS  Google Scholar 

  • Bernan S, Greenstein M, Maiese WM (1997) Marine microorganisms as a source of new natural products. Adv Appl Microbiol 43:57–90

    Article  PubMed  CAS  Google Scholar 

  • Blunt JW, Copp BR, Munro MHG, Northcote PT, Prisep MR (2004) Marine natural products. Nat Prod Rep 21:1–49

    Article  PubMed  CAS  Google Scholar 

  • Brantley SE, Molinski TF, Preston CM, DeLong EF (1995) Brominated acetylenic fatty acids from Xestospongia sp., a marine sponge bacterial association. Tetrahedron 51:7667–7672

    Article  CAS  Google Scholar 

  • Bull AT (2004) Bountiful oceans: prospecting marine microbial diversity. Trends Drug Discov 5:14–16

    Google Scholar 

  • Bull AT, Stach JEM, Ward AC, Goodfellow M (2005) Marine actinobacteria: perspectives, challenges and future directions. Antonie van Leeuwenhoek 87:65–79

    Article  Google Scholar 

  • Bultel-Poncé V, Debitus C, Blond A, Cerceau C, Guyot M (1997) Lutoside: an acyl-1-(acyl-69-mannobiosyl)-3-glycerol isolated from the sponge associated bacterium Micrococcus luteus. Tetrahedron Lett 38:5805–5808

    Article  Google Scholar 

  • Colquhoun JA, Heald SC, Li L, Tamaoka J, Kato C, Horikoshi K, Bull AT (1998) Taxonomy and biotransformation activities of some deepsea actinomycetes. Extremophiles 2:269–277

    Article  PubMed  CAS  Google Scholar 

  • Conte RM, Fattorusso E, Lanzotti V, Magno S, Mayol L (1994) Lintenolides, new pentacyclic bioactive sesterterpenes from the Caribbean sponge Cacospongia cf. linteiformis. Tetrahedron 50:849–856

    Article  CAS  Google Scholar 

  • Cook AE, Meyers PR (2003) Rapid identification of filamentous actinomycetes to the genus level using genus-specific 16S rRNA gene restriction fragment patterns. Int J Syst Evol Microbiol 53: 1907–1915

    Article  PubMed  CAS  Google Scholar 

  • Courtois S, Cappellano CM, Ball M, Francou FX, Normand P, Helynck G, Martinez A, Kolvek SJ, Hopke J, Osburne MS, August PR, Nalin R, Guerineau M, Jeannin P, Simonet P, Pernodet JL (2003) Recombinant environmental libraries provide access to microbial diversity for drug discovery from natural products. Appl Environ Microbiol 69:49–55

    Article  PubMed  CAS  Google Scholar 

  • Elyakov GB, Kuznetsova T, Mikhailov VV, Maltsev II, Voinov VG, Fedoreyev SA (1991) Brominated diphenyl ethers from a marine bacterium associated with the sponge Dysidea sp. Experientia 47:632–633

    Article  CAS  Google Scholar 

  • Faulkner DJ (2000) Marine natural products. Nat Prod Rep 17:7–55

    Article  PubMed  CAS  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Fiedler HP, Brunner C, Bull AT, Ward AC, Goodfellow M, Mihm G (2005) Marine actinomycetes as a source of novel secondary metabolites. Antonie van Leeuwenhoek 87(1):37–42

    Article  PubMed  CAS  Google Scholar 

  • Finking R, Marahiel AM (2004) Biosynthesis of nonribosomal peptides. Annu Rev Microbiol 28:453–488

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Ginolhac A, Jarrin C, Gillet B, Robe P, Pujic P, Tuphile K, Bertrand H, Vogel TM, Perriere G, Simonet P, Nalin R (2004) Phylogenetic analysis of polyketide synthase I domains from soil metagenomic libraries allows selection of promising clones. Appl Environ Microbiol 70:5522–5527

    Article  PubMed  CAS  Google Scholar 

  • Haefner B (2003) Drugs from the deep: marine natural products as drug candidates. Drug Discov Today 8:536–544

    Article  PubMed  CAS  Google Scholar 

  • Han SK, Nedashkovskaya OI, Mikhailov V, Kim SB, Bae KS (2003) Salinibacterium amurskyense gen. nov., sp. nov., a novel genus of the family Microbacteriaceae from the marine environment. Int J Syst Evol Microbiol 53:2061–2066

    Article  PubMed  CAS  Google Scholar 

  • Haygood MG, Schmidt EW, Davidson SK, Faulkner DJ (1999) Microbial symbionts of marine invertebrates: opportunities for microbial biotechnology. J Mol Microbiol Biotechnol 1:33–43

    PubMed  CAS  Google Scholar 

  • 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(9):4431–4440

    Article  PubMed  CAS  Google Scholar 

  • Hirota H, Tomono Y, Fusetani N (1996) Terpenoids with antifouling activity against barnacle larvae from the marine sponge Acanthella cavernosa. Tetrahedron 52:2359

    Article  CAS  Google Scholar 

  • Imamura N, Nishijima M, Adachi K, Sano H (1993) Novel antimycin antibiotics, urauchimycins A and B, produced by marine actinomycete. J Antibiot (Tokyo) 46:241–246

    CAS  Google Scholar 

  • Imhoff JF, Stöhr R (2003) Sponge-associated bacteria: general overview and special aspects of bacteria association with Halichondria panacea. In: Müller WEG (ed) Sponge (Porifera). Springer, Berlin, pp 35–58

  • Jensen PR, Dwight R, Fenical W (1991) Distribution of actinomycetes in near-shore tropical marine sediments. Appl Environ Microbiol 57:1102–1108

    PubMed  CAS  Google Scholar 

  • Jensen PR, Mincer TJ, Williams PG, Fenical W (2005) Marine actinomycete diversity and natural product discovery. Antonie Van Leeuwenhoek. 87(1):43–8

    Article  PubMed  CAS  Google Scholar 

  • Ketela MM, Halo L, Manukka E, Hakala J, Mantsala P, Ylihonko K (2002) Molecular evolution of aromatic polyketides and comparative sequence analysis of polyketide ketosynthase and 16S ribosomal DNA genes from various Streptomyces species. Appl Environ Microbiol 68:4472–4479

    Article  CAS  Google Scholar 

  • Ketela MM, Virpi S, Halo L, Hautala A, Hakala J, Mantsala P, Ylihonko K (1999) An efficient approach for screening minimal PKS genes from Streptomyces. FEMS Microbiol Lett 180:1–6

    Google Scholar 

  • Kumar S, Tamura K, Nei M (2004) MEGA3: Integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5:150–163

    Article  PubMed  CAS  Google Scholar 

  • Lanoot B, Vancanneyt M, Hoste B, Vandemeulebroecke K, Cnockaert MC, Dawyndt P, Liu ZH, Huang Y, Swings J (2005) Grouping of streptomycetes using 16S-ITS RFLP fingerprinting. Res Microbiol 156:755–762

    Article  PubMed  CAS  Google Scholar 

  • Lazzarini A, Cavaletti L, Toppo G, Marinelli F (2000) Rare genera of actinomycetes as potential producers of new antibiotics. Antonie van Leeuwenhoek 78: 399–405

    Article  PubMed  CAS  Google Scholar 

  • Lee YK, Lee JH, Lee HK (2001) Microbial symbiosis in marine sponges. J Microbiol 39:254–264

    Google Scholar 

  • Li X, De Boer SH (1995) Selection of polymerase chain reaction primers from an RNA intergenic spacer region for specific detection of Clavibacter michiganensis subsp. sepedonicus. Phytopathol 85(8):837–842

    Article  CAS  Google Scholar 

  • Liu W, Ahlert J, Gao Q, Pienkowski EW, Shen B, Thorson JS (2003) Rapid PCR amplification of minimal enediyne polyketide synthase cassettes leads to a predictive familial classification model. Proc Natl Acad Sci 100:11959–11963

    Article  PubMed  CAS  Google Scholar 

  • Maldonado LA, Stach JEM, Pathom-aree W, Ward AC, Bull AT, Goodfellow M (2005) Diversity of culturable actinobacteria in geographically widespread marine sediments. Antonie van Leeuwenhoek 87:11–18

    Article  PubMed  Google Scholar 

  • McVeigh HP, Munro J, Embley TM (1996) Molecular evidence for the presence of novel actinomycete lineages in a temperate forest soil. J Ind Microbiol 17:197–204

    Article  CAS  Google Scholar 

  • Metsä-Ketelä M, Salo V, Halo L, Hautala A, Hakala J, Mäntsälä P, Ylihonko K (1999) An efficient approach for screening minimal PKS genes from Streptomyces. FEMS Microbiol Lett 180:1–6

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Moore BS (1999) Biosynthesis of marine natural products: microorganisms and macroalgae. Nat Prod Rep 16:653–674

    Article  PubMed  CAS  Google Scholar 

  • Moran MA, Rutherford LT, Hodson RE (1995) Evidence for indigenous Streptomyces populations in a marine environment determined with a 16S rRNA probe. Appl Environ Microbiol 61:3695–3700

    PubMed  CAS  Google Scholar 

  • Musat N, Werner U, Knittel K, Kolb S, Dodenhof T, van Beusekom JE, de Beer D, Dubilier N, Amann R (2006) Microbial community structure of sandy intertidal sediments in the North Sea, Sylt-Romo Basin, Wadden Sea. Syst Appl Microbiol 29(4):333–348

    Article  PubMed  Google Scholar 

  • Pathom-aree W, Nogi Y, Sutcliffe IC, Ward AC, Horikoshi K, Bull AT, Goodfellow M (2006) Dermacoccus abyssi sp. nov., a piezotolerant actinomycete isolated from the Mariana Trench. Int J Syst Evol Microbiol 56(6):1233–1237

    Article  PubMed  CAS  Google Scholar 

  • Perry NP, Ettouati L, Litaudon M, Blunt JW, Munro MHG (1994) Alkaloids from the Antarctic sponge Kirkpatrickia varialosa. Part 1. Variolin B, a new antitumour and antiviral compound. Tetrahedron 50:3987–3992

    Article  CAS  Google Scholar 

  • Rainey FA, Ward-Rainey N, Kroppenstedt RM, Stackebrandt E (1996) The genus Nocardiopsis represents a phylogenetically coherent taxon and a distinct actinomycete lineage: proposal of Nocardiopsaceae fam. nov. Int J Syst Bacteriol 46:1088–1092

    Article  PubMed  CAS  Google Scholar 

  • Rheims H, Schumann P, Rohde M, Stackebrandt E (1998) Verrucosispora gifhornensis gen. nov., sp. nov., a new member of the actinobacterial family Micromonosporaceae. Int J Syst Bacteriol 48:1119–1127

    PubMed  CAS  Google Scholar 

  • Riedlinger J, Reicke A, Zähner H, Krismer B, Bull AT, Maldonado LA, Ward AC, Goodfellow M, Bister B, Bischo D, Sűssmuth RD, Fiedler HP (2004) Abyssomicins, inhibitors of the para-aminobenzoic acid pathway produced by the marine Verrucosispora strain AB-18-032. J Antibiot 57:271–279

    PubMed  CAS  Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Bio Evol 4:406–425

    CAS  Google Scholar 

  • Salomon CE, Margarvey NA, Sherman DH (2004) Merging the potential of microbial genetics with biological and chemical diversity: an even brighter future for marine natural product drug discovery. Nat Prod Rep 21:105–121

    Article  PubMed  CAS  Google Scholar 

  • Schmidt EW, Obraztsova AY, Davidson SK, Faulkner DJ, Haygood MG (2000) Identification of the antifungal peptide-containing symboiont of the marine sponge Theonella swinhoei as a novel d-proteobacterium, “Candidatus Entotheonella palauensis”. Mar Biol 136:969–977

    Article  CAS  Google Scholar 

  • Stierle AC, Cardellina JHI, Singleton FL (1988) A marine Micrococcus produces metabolites ascribed to the sponge Tedania ignis. Experientia 44:1021

    Article  PubMed  CAS  Google Scholar 

  • Takizawa M, Colwell RR, Hill RT (1993) Solation and diversity of actinomycetes in the Chesapeake Bay. Appl Environ Microbiol 59:997–1002

    PubMed  Google Scholar 

  • Vacelet J (1975) Étude en microscopie électronique de l’association entre bactéries et spongiaires du genre Verongia (Dictyoceratida). J Microsc Biol Cell 23:271–288

    Google Scholar 

  • Vacelet J, Donadey C (1977) Electron microscope study of the association between some sponges and bacteria. J Exp Mar Ecol 30:301–314

    Article  Google Scholar 

  • Ward AC, Goodfellow M (2004) Phylogeny and functionality: taxonomy as a roadmap to genes. In: Bull AT (ed) Microbial diversity and bioprospecting. ASM Press, Washington, D.C., pp 288–313

  • Warnecke F, Amann R, Pernthaler J (2004) Actinobacterial 16S rRNA genes from freshwater habitats cluster in four distinct lineages. Environ Microbiol 6:242–253

    Article  PubMed  CAS  Google Scholar 

  • Webster NS, Hill RT (2001) The culturable microbial community of the Great Barrier Reef sponge Rhopaloeides odorabile is dominated by α–proteobacterium. Mar Biol 138:843–851

    Article  CAS  Google Scholar 

  • Woese CR, Gutell R, Gupta R, Noller HF (1983) Detailed analysis of the higher-order structure of 16S-like ribosomal ribonucleic acids. Microbiol Rev 47(4):621–69

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

This research was funded by the Hundred Talents Program of Chinese Academy of Sciences. We also thank the funding of Guangdong Natural Science Fundation (06301287) and the Research Foundation of Science and Technology Planning Project of Guangdong Province (2006B36501004).

Author information

Authors and Affiliations

  1. Key Laboratory of Marine Bio-resources Sustainable Utilization (LMB-CAS), Guangdong Key Laboratory of Marine Materia Medica (LMMM-GD), South China Sea Institute of Oceanology, Chinese Academy of Sciences, Guangzhou, 510301, P.R. China

    Shumei Jiang, Wei Sun, Minjie Chen, Shikun Dai, Yonghong Liu & Xiang Li

  2. Floriculture Research Institute of Guangdong Academy of Agricultural Sciences, Guangzhou, 510640, P.R. China

    Long Zhang

  3. Department of Biology, Hannam University, 133 Ojungdong, Daedukgu, Daejeon, Korea

    Kyung Jin Lee

Authors
  1. Shumei Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wei Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Minjie Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shikun Dai
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Long Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yonghong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Kyung Jin Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xiang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Xiang Li.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jiang, S., Sun, W., Chen, M. et al. Diversity of culturable actinobacteria isolated from marine sponge Haliclona sp.. Antonie van Leeuwenhoek 92, 405–416 (2007). https://doi.org/10.1007/s10482-007-9169-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-007-9169-z

Keywords

Search

Navigation