Skip to main content
SpringerLink
Log in

Antimicrobial Activity of Marine Bacterial Symbionts Retrieved from Shallow Water Hydrothermal Vents

  • Short Communication
  • Published:
Marine Biotechnology Aims and scope Submit manuscript

Abstract

Marine sponges and other sessile macro-organisms were collected at a shallow water hydrothermal site in Eyjafjörður, Iceland. Bacteria were isolated from the organisms using selective media for actinomycetes, and the isolates were screened for antimicrobial activity. A total of 111 isolates revealed antimicrobial activity displaying different antimicrobial patterns which indicates production of various compounds. Known test strains were grown in the presence of ethyl acetate extracts from one selected isolate, and a clear growth inhibition of Staphylococcus aureus was observed down to 0.1 % extract concentration in the medium. Identification of isolates shows different species of Actinobacteria with Streptomyces sp. playing the largest role, but also members of Bacilli, Alphaproteobacteria and Gammaproteobacteria. Sponges have an excellent record regarding production of bioactive compounds, often involving microbial symbionts. At the hydrothermal vents, however, the majority of active isolates originated from other invertebrates such as sea anemones or algae. The results indicate that antimicrobial assays involving isolates in full growth can detect activity not visible by other methods. The macro-organisms inhabiting the Eyjafjörður hydrothermal vent area host diverse microbial species in the phylum Actinobacteria with antimicrobial activity, and the compounds responsible for the activity will be subject to further research.

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
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Abbas S, Kelly M, Bowling J, Sims J, Waters A, Hamann M (2011) Advancement into the Arctic region for bioactive sponge secondary metabolites. Mar Drugs 9:2423–2437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Abdelmohsen UR, Bayer K, Hentschel U (2014) Diversity, abundance and natural products of marine sponge-associated actinomycetes. Nat Prod Rep 31:381–399

    Article  CAS  PubMed  Google Scholar 

  • Abriouel H, Franz CMAP, Ben Omar N, Galvez A (2011) Diversity and applications of Bacillus bacteriocins. FEMS Microbiol Rev 35:201–232

    Article  CAS  PubMed  Google Scholar 

  • Augustine N, Peter WA, Kerkar S, Thomas S (2012) Arctic actinomycetes as potential inhibitors of Vibrio cholerae biofilm. Curr Microbiol 64:338–342

    Article  CAS  PubMed  Google Scholar 

  • Aunpad R, Na-Bangchang K (2007) Pumilicin 4, a novel bacteriocin with anti-MRSA and anti-VRE activity produced by newly isolated bacteria Bacillus pumilus strain WAPB4. Curr Microbiol 55:308–313

    Article  CAS  PubMed  Google Scholar 

  • Bertrand S, Bohni N, Schnee S, Schumpp O, Gindro K, Wolfender J (2014) Metabolite induction via microorganism co-culture: a potential way to enhance chemical diversity for drug discovery. Biotechnol Adv 32:1180–1204

    Article  CAS  PubMed  Google Scholar 

  • Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR (2012) Marine natural products. Nat Prod Rep 29:144–222

    Article  CAS  PubMed  Google Scholar 

  • Brack C, Mikolasch A, Schauer F (2014) 2,5-diketopiperazines produced by Bacillus pumilus during bacteriolysis of Arthrobacter citreus. Mar Biotechnol 16:385–395

    Article  CAS  PubMed  Google Scholar 

  • Bragadeeswaran S, Thangaraj S, Prabhu K, Raj Sophia Rani S (2011) Antifouling activity by sea anemone (Heteractis magnifica and H. aurora) extracts against marine biofilm bacteria. Lat Am J Aquat Res 39:385–389

    Article  Google Scholar 

  • Bredholt H, Fjaervik E, Johnsen G, Zotchev SB (2008) Actinomycetes from sediments in the Trondheim fjord, Norway: diversity and biological activity. Mar Drugs 6:12–24

    Article  PubMed  PubMed Central  Google Scholar 

  • Dashti Y, Grkovic T, Abdelmohsen UR, Hentschel U, Quinn RJ (2014) Production of induced secondary metabolites by a co-culture of sponge-associated actinomycetes, Actinokineospora sp. EG49 and Nocardiopsis sp. RV163. Mar Drugs 12:3046–3059

    Article  PubMed  PubMed Central  Google Scholar 

  • Dembitsky V (2006) Astonishing diversity of natural surfactants: 7. Biologically active hemi- and monoterpenoid glycosides. Lipids 41:1–27

    Article  CAS  PubMed  Google Scholar 

  • Dupont S, Carre-Mlouka A, Domart-Coulon I, Vacelet J, Bourguet-Kondracki M (2014) Exploring cultivable bacteria from the prokaryotic community associated with the carnivorous sponge Asbestopluma hypogea. FEMS Microbiol Ecol 88:160–174

    Article  CAS  PubMed  Google Scholar 

  • Han S, Nedashkovskaya O, Mikhailov V, Kim S, Bae K (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  CAS  PubMed  Google Scholar 

  • Hannington M, Herzig P, Stoffers P, Scholten J, Botz R, Garbe-Schonberg D, Jonasson IR, Roest W, Party SS (2001) First observations of high-temperature submarine hydrothermal vents and massive anhydrite deposits off the north coast of Iceland. Mar Geol 177:199–220

    Article  CAS  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 

  • Hentschel U (2003) Microbial diversity of marine sponges. Boll Mus Ist Biol Univ Genova 68:365–372

    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 

  • Ivanova EP, Nicolau DV, Yumoto N, Taguchi T, Okamoto K, Tatsu Y, Yoshikawa S (1998) Impact of conditions of cultivation and adsorption on antimicrobial activity of marine bacteria. Mar Biol 130:545–551

    Article  Google Scholar 

  • Jaeschke A, Jorgensen SL, Bernasconi SM, Pedersen RB, Thorseth IH, Frueh-Green GL (2012) Microbial diversity of Loki’s Castle black smokers at the Arctic mid-ocean ridge. Geobiology 10:548–561

    Article  CAS  PubMed  Google Scholar 

  • Langer O, Palme O, Wray V, Tokuda H, Lang S (2006) Production and modification of bioactive biosurfactants. Process Biochem 41:2138–2145

    Article  CAS  Google Scholar 

  • Lee Y, Kwon K, Cho K, Kim H, Park J, Lee H (2003) Culture and identification of bacteria from marine biofilms. J Microbiol 41:183–188

    CAS  Google Scholar 

  • Liu Z, Yang L, Huang Y, Zhao H, Liu H, Tang S, Li W, Chen Y (2013) Rothia marina sp nov., isolated from an intertidal sediment of the South China Sea. Antonie Van Leeuwenhoek 104:331–337

    Article  PubMed  Google Scholar 

  • Marteinsson VT, Kristjansson JK, Kristmannsdottir H, Dahlkvist M, Saemundsson K, Hannington M, Petursdottir SK, Geptner A, Stoffers P (2001) Discovery and description of giant submarine smectite cones on the seafloor in Eyjafjordur, Northern Iceland, and a novel thermal microbial habitat. Appl Environ Microbiol 67:827–833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mearns-Spragg A, Bregu M, Boyd KG, Burgess JG (1998) Cross-species induction and enhancement of antimicrobial activity produced by epibiotic bacteria from marine algae and invertebrates, after exposure to terrestrial bacteria. Lett Appl Microbiol 27:142–146

    Article  CAS  PubMed  Google Scholar 

  • Meron D, Buia M, Fine M, Banin E (2013) Changes in microbial communities associated with the sea anemone Anemonia viridis in a natural pH gradient. Microb Ecol 65:269–276

    Article  CAS  PubMed  Google Scholar 

  • Moitinho-Silva L, Bayer K, Cannistraci CV, Giles EC, Ryu T, Seridi L, Ravasi T, Hentschel U (2014) Specificity and transcriptional activity of microbiota associated with low and high microbial abundance sponges from the Red Sea. Mol Ecol 23:1348–1363

    Article  CAS  PubMed  Google Scholar 

  • Montalvo NF, Hill RT (2011) Sponge-associated bacteria are strictly maintained in two closely related but geographically distant sponge hosts. Appl Environ Microbiol 77:7207–7216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Newman DJ, Cragg GM (2014) Marine-sourced anti-cancer and cancer pain control agents in clinical and late preclinical development. Mar Drugs 12:255–278

    Article  PubMed  PubMed Central  Google Scholar 

  • Olson JB, Harmody DK, Bej AK, McCarthy PJ (2007) Tsukamurella spongiae sp nov., a novel actinomycete isolated from a deep-water marine sponge. Int J Syst Evol Microbiol 57:1478–1481

    Article  CAS  PubMed  Google Scholar 

  • Pathom-aree W, Stach JEM, Ward AC, Horikoshi K, Bull AT, Goodfellow M (2006) Diversity of actinomycetes isolated from challenger deep sediment (10,898 m) from the Mariana Trench. Extremophiles 10:181–189

    Article  CAS  PubMed  Google Scholar 

  • Phelan RW, O’Halloran JA, Kennedy J, Morrissey JP, Dobson ADW, O’Gara F, Barbosa TM (2012) Diversity and bioactive potential of endospore-forming bacteria cultured from the marine sponge Haliclona simulans. J Appl Microbiol 112:65–78

    Article  CAS  PubMed  Google Scholar 

  • Porporato EMD, Lo Giudice A, Michaud L, De Domenico E, Spano N (2013) Diversity and antibacterial activity of the bacterial communities associated with two Mediterranean Sea pens, Pennatula phosphorea and Pteroeides spinosum (Anthozoa: Octocorallia). Microb Ecol 66:701–714

    Article  CAS  PubMed  Google Scholar 

  • Prieto ML, O’Sullivan L, Tan SP, McLoughlin P, Hughes H, O’Connor PM, Cotter PD, Lawlor PG, Gardiner GE (2012) Assessment of the bacteriocinogenic potential of marine bacteria reveals lichenicidin production by seaweed-derived Bacillus spp. Mar Drugs 10:2280–2299

    Article  CAS  PubMed  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 

  • Schander C, Rapp HT, Kongsrud JA, Bakken T, Berge J, Cochrane S, Oug E, Byrkjedal I, Todt C, Cedhagen T, Fosshagen A, Gebruk A, Larsen K, Levin L, Obst M, Pleijel F, Stohr S, Waren A, Mikkelsen NT, Hadler-Jacobsen S, Keuning R, Petersen KH, Thorseth IH, Pedersen RB (2010) The fauna of hydrothermal vents on the Mohn Ridge (North Atlantic). Mar Biol Res 6:155–171

    Article  Google Scholar 

  • Shubenkova OV, Likhoshvai AV, Kanapatskii TA, Pimenov NV (2010) Microbial community of reduced pockmark sediments (Gdansk Deep, Baltic Sea). Microbiology 79:799–808

    Article  CAS  Google Scholar 

  • Slattery M, Rajbhandari I, Wesson K (2001) Competition-mediated antibiotic induction in the marine bacterium Streptomyces tenjimariensis. Microb Ecol 41:90–96

    CAS  PubMed  Google Scholar 

  • Strahl ED, Dobson WE, Lundie LL (2002) Isolation and screening of brittlestar-associated bacteria for antibacterial activity. Curr Microbiol 44:450–459

    Article  CAS  PubMed  Google Scholar 

  • Thangaraj S, Bragadeeswaran S, Suganthi K, Kumaran NS (2011) Antimicrobial properties of sea anemone Stichodactyla mertensii and Stichodactyla gigantea from Mandapam coast of India. Asian Pac J Trop Biomed 1:S43–S46

    Article  Google Scholar 

  • Urich T, Lanzén A, Stokke R, Pedersen RB, Bayer C, Thorseth IH, Schleper C, Steen IH, Øvreas L (2014) Microbial community structure and functioning in marine sediments associated with diffuse hydrothermal venting assessed by integrated meta-omics. Environ Microbiol 16:2699–2710

    Article  CAS  PubMed  Google Scholar 

  • Webster NS, Taylor MW (2012) Marine sponges and their microbial symbionts: love and other relationships. Environ Microbiol 14:335–346

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    CAS  PubMed  PubMed Central  Google Scholar 

  • Williams GP, Babu S, Ravikumar S, Kathiresan K, Prathap SA, Chinnapparaj S, Marian MP, Alikhan SL (2007) Antimicrobial activity of tissue and associated bacteria from benthic sea anemone Stichodactyla haddoni against microbial pathogens. J Environ Biol 28:789–793

    PubMed  Google Scholar 

  • Yuan M, Yu Y, Li H, Dong N, Zhang X (2014) Phylogenetic diversity and biological activity of Actinobacteria isolated from the Chukchi Shelf marine sediments in the Arctic Ocean. Mar Drugs 12:1281–1297

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

The authors wish to thank Erlendur Bogason for the collection of underwater samples and Dr. Kristinn P. Magnusson and Dr. Oddur Vilhelmsson for the helpful comments regarding molecular methods. The work was supported by the Icelandic Research Fund, University of Akureyri Research Fund, KEA University Fund and the Fisheries Project Fund of the Icelandic Ministry of Fisheries and Agriculture.

Author information

Authors and Affiliations

  1. Faculty of Natural Resource Sciences, University of Akureyri, Borgum, Nordurslod 4, 600, Akureyri, Iceland

    Arnheidur Eythorsdottir & Hjorleifur Einarsson

  2. Faculty of Pharmaceutical Sciences, University of Iceland, Haga, Hofsvallagotu 53, 107, Reykjavík, Iceland

    Arnheidur Eythorsdottir & Sesselja Omarsdottir

Authors
  1. Arnheidur Eythorsdottir
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sesselja Omarsdottir
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hjorleifur Einarsson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hjorleifur Einarsson.

Ethics declarations

Conflict of Interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Table 1

Antimicrobial activity observed in ethyl acetate extracts of the different isolates’ (rows) broth cultures by agar diffusion assay, presented for each test strain (columns). Inhibition zones are shown (mm) as measured from the edge of the filter disc to a visible growth lawn of the test strain. All isolates were obtained from incubation at 15 °C. Three additional test strains were used compared to the streaking test: S. aureus DSM 1104, S. aureus DSM 2569 and P. aeruginosa DSM 1117. (DOCX 15 kb)

Table 2

Antimicrobial activity and association with macro-organisms of bacterial isolates from the hydrothermal vent area. Activity was measured as distance (mm) between the growing isolate and growth of test strain on ISP2 medium. Results are presented as: + = 5–14 mm; ++ = 15–25 mm; +++ = > 25 mm; − = < 5 mm; n/a = not tested; +/− = growth very poor compared to control. *n/ident refers to a small sample which was not defined completely, but contained at least sea anemone larvae, a nudibranch and skeleton shrimps (Caprella sp.). Eight isolates have been removed, regarded as duplicates according to morphology, DGGE patterns, antimicrobial activity response, and/or 16S BLAST results. S.a.: S. aureus DSM 799; E.c.: E. coli; E.f.: Enterococcus faecalis; P.a.: Pseudomonas aeruginosa DSM 1128; C.a.: Candida albicans; L.m.: Listeria monocytogenes. (DOCX 31 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Eythorsdottir, A., Omarsdottir, S. & Einarsson, H. Antimicrobial Activity of Marine Bacterial Symbionts Retrieved from Shallow Water Hydrothermal Vents. Mar Biotechnol 18, 293–300 (2016). https://doi.org/10.1007/s10126-016-9695-7

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-016-9695-7

Keywords

Search

Navigation