Skip to main content

Advertisement

SpringerLink
Log in

Diversity and antimicrobial potential of bacterial isolates associated with the soft coral Alcyonium digitatum from the Baltic Sea

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

Abstract

It is well recognized that microorganisms associated with marine invertebrates, in particular sponges and hard corals, are an excellent source of new natural products. Therefore, the diversity of bacteria associated with marine invertebrates and their potential to produce bioactive compounds have received much attention in recent years. We report here for the first time on the biodiversity of bacteria associated with the soft coral Alcyonium digitatum, which is abundant in the Baltic Sea. In order to increase the cultured diversity, bacteria were isolated using four different media, identified with support of 16S rRNA gene sequences and screened for antimicrobial activity using two different media. Activity of crude extracts was tested against Bacillus subtilis, Staphylococcus epidermidis, Escherichia coli, and the yeast Candida albicans. A total of 251 coral-associated bacterial isolates were classified and found to belong to 41 species in 14 genera of the Firmicutes, Actinobacteria, Gammaproteobacteria, and Alphaproteobacteria. The genus Bacillus was most abundant and diverse with 17 recognized species. Forty-eight percent of all 251 isolates exhibited antimicrobial activity. All isolates of Bacillus methylotrophicus and Bacillus amyloliquefaciens displayed inhibition of at least three out of the four tested microorganisms. It became obvious during this study that the production of antibiotic substances not only is strain-specific, but in many cases also depends on the media composition and growth conditions. In addition, the antimicrobial potential of bacteria associated with A. digitatum may represent a promising source for antimicrobial substances.

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

Similar content being viewed by others

References

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • Ben-Haim Y, Zicherman-Keren M, Rosenberg E (2003) Temperature-regulated bleaching and lysis of the coral Pocillopora damicornis by the novel pathogen Vibrio coralliilyticus. Appl Environ Microbiol 69:4236–4242

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bourne DG, Munn CB (2005) Diversity of bacteria associated with the coral Pocillopora damicornis from the Great Barrier Reef. Environ Microbiol 7:1162–1174

    Article  CAS  PubMed  Google Scholar 

  • de Castro AP, Araujo JSD, Reis AMM, Moura RL, Francini-Filho RB, Pappas G, Rodrigues TB, Thompson FL, Krüger RH (2010) Bacterial community associated with healthy and diseased reef coral Mussismilia hispida from Eastern Brazil. Microb Ecol 59:658–667

    Article  PubMed  Google Scholar 

  • Dobretsov S, Qian PY (2004) The role of epibotic bacteria from the surface of the soft coral Dendronephthya sp. in the inhibition of larval settlement. J Exp Mar Biol Ecol 299:35–50

    Article  Google Scholar 

  • Galkiewicz JP, Pratte ZA, Gray MA, Kellogg CA (2011) Characterization of culturable bacteria isolated from the cold-water coral Lophelia pertusa. FEMS Microbiol Ecol 77:333–346

    Article  CAS  PubMed  Google Scholar 

  • Gosner KL (1978) A field guide to atlantic seashore. Houghton Mifflin Company, Boston

    Google Scholar 

  • Gray MA, Stone RP, Mclaughlin MR, Kellogg CA (2011) Microbial consortia of gorgonian corals from the Aleutian islands. FEMS Microbiol Ecol 76:109–120

    Article  CAS  PubMed  Google Scholar 

  • Harder T, Lau SCK, Dobretsov S, Fang TK, Qian PY (2003) A distinctive epibiotic bacterial community on the soft coral Dendronephthya sp. and antibacterial activity of coral tissue extracts suggest a chemical mechanism against bacterial epibiosis. FEMS Microbiol Ecol 43:337–347

    Article  CAS  PubMed  Google Scholar 

  • Hartnoll RG (1975) The annual cycle of Alcyonium digitatum. Estuar Coast Mar Sci 3:71–78

    Article  Google Scholar 

  • Heindl H, Wiese J, Thiel V, Imhoff JF (2010) Phylogenetic diversity and antimicrobial activities of bryozoan-associated bacteria isolated from Mediterranean and Baltic Sea habitats. Syst Appl Microbiol 33:94–104

    Article  CAS  PubMed  Google Scholar 

  • Imhoff JF, Labes A, Wiese J (2011) Bio-mining the microbial treasures of the ocean: new natural products. Biotechnol Adv 29:468–482

    Article  CAS  PubMed  Google Scholar 

  • Kennedy J, Baker P, Piper C, Cotter PD, Walsh M, Mooij MJ, Bourke MB, Rea MC, O’Connor PM, Ross RP, Hill C, O’Gara F, Dobson ADW (2009) Isolation and analysis of bacteria with antimicrobial activities from the marine sponge Haliclona simulans collected from Irish waters. Mar Biotechnol 11:384–396

    Article  CAS  PubMed  Google Scholar 

  • Kushmaro A, Loya Y, Fine M, Rosenberg E (1996) Bacterial infection and coral bleaching. Nature 380:396

    Article  CAS  Google Scholar 

  • Kushmaro A, Rosenberg E, Fine M, Loya Y (1997) Bleaching of the coral Oculina patagonica by Vibrio AK-1. Mar Ecol Prog Ser 147:159–165

    Article  Google Scholar 

  • 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 5:1041–1054

    Article  Google Scholar 

  • Lampert Y, Kelman D, Dubinsky Z, Nitzan Y, Hill RT (2006) Diversity of culturable bacteria in the mucus of the Red Sea coral Fungia scutaria. FEMS Microbiol Ecol 58:99–108

    Article  CAS  PubMed  Google Scholar 

  • Lampert Y, Kelman D, Nitzan Y, Dubinsky Z, Behar A, Hill RT (2008) Phylogenetic diversity of bacteria associated with the mucus of Red Sea corals. FEMS Microbiol Ecol 64:187–198

    Article  CAS  PubMed  Google Scholar 

  • Lane DJ (1991) 16S/23S rRNA sequencing. In: Stackebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics. Wiley, Chichhester, pp 115–175

    Google Scholar 

  • McKew BA, Dumbrell AJ, Daud SD, Hepburn L, Thorpe E, Mogensen L, Whitby C (2012) Characterization of geographically distinct bacterial communities associated with coral mucus produced by Acropora spp. and Porites spp. Appl Environ Microbiol 78:5229–5237

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Neulinger SC, Järnegren J, Ludvigsen M, Lochte K, Dullo WC (2008) Phenotype-specific bacterial communities in the cold-water coral Lophelia pertusa (Scleractinia) and their implications for the coral’s nutrition, health, and distribution. Appl Environ Microbiol 74:7272–7285

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Nissimov J, Rosenberg E, Munn CB (2009) Antimicrobial properties of resident coral mucus bacteria of Oculina patagonica. FEMS Microbiol Lett 292:210–215

    Article  CAS  PubMed  Google Scholar 

  • Nithyanand P, Pandian SK (2009) Phylogenetic characterization of culturable bacterial diversity associated with the mucus and tissue of the coral Acropora digitifera from the Gulf of Mannar. FEMS Microbiol Ecol 69:384–394

    Article  CAS  PubMed  Google Scholar 

  • Palomo S, González I, de la Cruz M, Martín J, Tormo JR, Anderson M, Hill RT, Vicente F, Reyes F, Genilloud O (2013) Sponge-derived Kocuria and Micrococcus spp. as sources of the new thiazolyl peptide antibiotic kocurin. Mar Drugs 11:1071–1086

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Peng J, Zhang X, Xu X, He F, Qi S (2013) Diversity and chemical defense role of culturable non-actinobacterial bacteria isolated from the South China Sea Gorgonians. J Microbiol Biotechnol 23:437–443

    Article  CAS  PubMed  Google Scholar 

  • Raina JB, Tapiolas D, Willis BL, Bourne DG (2009) Coral-associated bacteria and their role in the biogeochemical cycling of sulfur. Appl Environ Microbiol 75:3492–3501

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Raina JB, Dinsdale EA, Willis BL, Bourne DG (2010) Do the organic sulfur compounds DMSP and DMS drive coral microbial associations? Trends Microbiol 18:101–108

    Article  CAS  PubMed  Google Scholar 

  • Ritchie K (2006) Regulation of microbial populations by coral surface mucus and mucus-associated bacteria. Mar Ecol Prog Ser 322:1–14

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Romanenko LA, Uchino M, Kalinovskaya NI, Mikhailov VV (2008) Isolation, phylogenetic analysis and screening of marine mollusc-associated bacteria for antimicrobial, hemolytic and surface activities. Microbiol Res 163:633–644

    Article  PubMed  Google Scholar 

  • Shnit-Orland M, Kushmaro A (2009) Coral mucus-associated bacteria: a possible first line of defense. FEMS Microbiol Ecol 67:371–380

    Article  CAS  PubMed  Google Scholar 

  • Shnit-Orland M, Sivan A, Kushmaro A (2012) Antibacterial activity of Pseudoalteromonas in the coral holobiont. Microb Ecol 64:851–859

    Article  CAS  PubMed  Google Scholar 

  • Stackebrandt E, Ebers J (2006) Taxonomic parameters revisited: tarnished gold standards. Microbiol Today 33:152–155

    Google Scholar 

  • Staufenberger T, Thiel V, Wiese J, Imhoff JF (2008) Phylogenetic analysis of bacteria associated with Laminaria saccharina. FEMS Microbiol Ecol 64:65–77

    Article  CAS  PubMed  Google Scholar 

  • Tait E, Carman M, Sievert SM (2007) Phylogenetic diversity of bacteria associated with ascidians in Eel Pond (Woods Hole, Massachusetts, USA). J Exp Mar Biol Ecol 342:138–146

    Article  Google Scholar 

  • Thiel V, Imhoff JF (2003) Phylogenetic identification of bacteria with antimicrobial activities isolated from Mediterranean sponges. Biomol Eng 20:421–423

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Ward-Rainey N, Rainey FA, Stackebrandt E (1996) A study of the bacterial flora associated with Holothuria atra. J Exp Mar Biol Ecol 203:11–26

    Article  Google Scholar 

  • Webster NS, Bourne D (2007) Bacterial community structure associated with the Antarctic soft coral, Alcyonium antarcticum. FEMS Microbiol Ecol 59:81–94

    Article  CAS  PubMed  Google Scholar 

  • Wiese J, Thiel V, Nagel K, Staufenberger T, Imhoff JF (2009) Diversity of antibiotic-active bacteria associated with the brown alga Laminaria saccharina from the Baltic Sea. Mar Biotechnol 11:287–300

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Sun Y, Bao J, He F, Xu X, Qi S (2012) Phylogenetic survey and antimicrobial activity of culturable microorganisms associated with the South China Sea black coral Antipathes dichotoma. FEMS Microbiol Lett 336:122–130

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the Ministry of Education and Training of Vietnam with the framework of the project 322. We thank Gregor Steffen for sampling of the soft coral Alcyonium digitatum from the Baltic Sea. We thank the Institute of Clinical Molecular Biology of the UKSH (University Medical Center Schleswig-Holstein, Kiel, Germany) for providing Sanger sequencing.

Author information

Author notes

  1. Thi Mien Pham

    Present address: Department of Marine Ecology, Institute of Oceanography, 01 Cau Da, Nha Trang, Khanh Hoa, Vietnam

Authors and Affiliations

  1. Department of Marine Microbiology, GEOMAR Helmholtz Centre for Ocean Research Kiel, Düsternbrooker Weg 20, 24105, Kiel, Germany

    Thi Mien Pham, Jutta Wiese, Arlette Wenzel-Storjohann & Johannes F. Imhoff

Authors
  1. Thi Mien Pham
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jutta Wiese
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Arlette Wenzel-Storjohann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Johannes F. Imhoff
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Johannes F. Imhoff.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pham, T.M., Wiese, J., Wenzel-Storjohann, A. et al. Diversity and antimicrobial potential of bacterial isolates associated with the soft coral Alcyonium digitatum from the Baltic Sea. Antonie van Leeuwenhoek 109, 105–119 (2016). https://doi.org/10.1007/s10482-015-0613-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10482-015-0613-1

Keywords

Search

Navigation