Skip to main content

Advertisement

SpringerLink
Log in

Screening of the Antarctic marine sponges (Porifera) as a source of bioactive compounds

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

Sponges (Porifera) currently represent one of the richest sources of natural products and account for almost half of the pharmacologically active compounds of marine origin. However, to date very little is known about the pharmacological potential of the sponges from polar regions. In this work we report on screening of ethanolic extracts from 24 Antarctic marine sponges for different biological activities. The extracts were tested for cytotoxic effects against normal and transformed cell lines, red blood cells, and algae, for modulation of the activities of selected physiologically important enzymes (acetylcholinesterase, butyrylcholinesterase, and α-amylase), and for inhibition of growth of pathogenic and ecologically relevant bacteria and fungi. An extract from Tedania (Tedaniopsis) oxeata was selectively cytotoxic against the cancer cell lines and showed growth inhibition of all of the tested ecologically relevant and potentially pathogenic fungal isolates. The sponge extracts from Isodictya erinacea and Kirkpatrickia variolosa inhibited the activities of the cholinesterase enzymes, while the sponge extracts from Isodictya lankesteri and Inflatella belli reduced the activity of α-amylase. Several sponge extracts inhibited the growth of multiresistant pathogenic bacterial isolates of different origins, including extended-spectrum beta-lactamase and carbapenem-resistant strains, while sponge extracts from K. variolosa and Myxilla (Myxilla) mollis were active against a human methicillin-resistant Staphylococcus aureus strain. We conclude that Antarctic marine sponges represent a valuable source of biologically active compounds with pharmacological potential.

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

Similar content being viewed by others

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 

  • Abdo DA, Motti CA, Battershill CN, Harvey ES (2007) Temperature and spatiotemporal variability of salicylihalamide A in the sponge Haliclona sp. J Chem Ecol 33:1635–1645

    Article  CAS  PubMed  Google Scholar 

  • Ali H, Houghton PJ, Soumyanath A (2006) α-Amylase inhibitory activity of some Malaysian plants used to treat diabetes, with particular reference to Phyllanthus amarus. J Ethnopharmacol 107:449–455

    Article  PubMed  Google Scholar 

  • Avila C, Taboada S, Núňez-Pons L (2008) Antarctic marine chemical ecology: what is next? Mar Ecol 29:1–71

    Article  CAS  Google Scholar 

  • Bernfeld P (1955) Amylases, α and β. In: Colowick S, Kaplan N (eds) Methods in enzymology. Academic Press, Waltham, pp 149–158

    Google Scholar 

  • Brezovšek P, Eleršek T, Filipič M (2014) Toxicities of four anti-neoplastic drugs and their binary mixtures tested on the green alga Pseudokirchneriella subcapitata and the cyanobacterium Synechococcus leopoliensis. Water Res 52:168–177

    Article  PubMed  Google Scholar 

  • de Hoog GS, Guarro J, Gene J, Figueras MJ (2009) Atlas of clinical fungi. http://www.cbs.knaw.nl/index.php/atlas-of-clinical-fungi. Accessed 21 Oct 2015

  • Duckworth AR, Battershill CN (2001) Population dynamics and chemical ecology of New Zealand Demospongiae Latrunculia sp. nov. and Polymastia croceus (Poecilosclerida: Latrunculiidae: Polymastiidae). New Zeal J Mar Freshw Res 35:935–949

    Article  Google Scholar 

  • Ellman GL, Courtney D, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95

    Article  CAS  PubMed  Google Scholar 

  • Ferretti C, Vacca S, De Ciucis C et al (2009) Growth dynamics and bioactivity variation of the Mediterranean demosponges Agelas oroides (Agelasida, Agelasidae) and Petrosia ficiformis (Haplosclerida, Petrosiidae). Mar Ecol 30:327–336

    Article  Google Scholar 

  • Fusetani N, Shinoda K, Matsunaga S (1993) Bioactive marine metabolites. 48. Cinachyrolide A: a potent cytotoxic macrolide possessing two spiro ketals from marine sponge Cinachyra sp. J Am Chem Soc 115:3977–3981

    Article  CAS  Google Scholar 

  • Garnica M, Nucci M (2013) Epidemiology of fusariosis. Curr Fungal Infect Rep 7:301–305

    Article  Google Scholar 

  • Gerwick WH, Moore BS (2012) Lessons from the past and charting the future of marine natural products drug discovery and chemical biology. Chem Biol 19:85–98

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gopi M, Kumaran S, Kumar TT, Deivasigamani B, Alagappan K, Prasad SG (2012a) Antibacterial potential of sponge endosymbiont marine Enterobacter sp at Kavaratti Island, Lakshadweep Archipelago. Asian Pac J Trop Med 5:142–146

    Article  PubMed  Google Scholar 

  • Gopi M, Ajith Kumar TT, Balagurunathan R, Vinoth R, Dhaneesh KV, Rajasekaran R, Balasubramanian T (2012b) Phylogenetic study of sponge-associated bacteria from the Lakshadweep Archipelago and the antimicrobial activities of their secondary metabolites. World J Microbiol Biotechnol 28:761–766

    Article  CAS  PubMed  Google Scholar 

  • Gostinčar C, Turk M, Plemenitaš A, Gunde-Cimerman N (2009) The expressions of Δ9-, Δ12-desaturases and an elongase by the extremely halotolerant Hortaea werneckii are salt dependent. FEMS Yeast Res 9:247–256

    Article  PubMed  Google Scholar 

  • Hood KA, West LM, Northcote PT, Berridge MV, Miller JH (2001) Induction of apoptosis by the marine sponge (Mycale) metabolites, mycalamide A and pateamine. Apoptosis 6:207–219

    Article  CAS  PubMed  Google Scholar 

  • Hu GP, Yuan J, Sun L, She ZG, Wu JH, Lan XJ, Zhu X, Lin YC, Chen SP (2011) Statistical research on marine natural products based on data obtained between 1985 and 2008. Mar Drugs 9:514–525

    Article  PubMed  PubMed Central  Google Scholar 

  • Janussen D, Downey RV (2014) Porifera. In: De Broyer C, Koubbi P, Griffiths HJ et al (eds) Biogeographic atlas of the Southern ocean. Scientific Committee on Antarctic Research, Cambridge, pp 94–102

    Google Scholar 

  • Kaur J, Zhang MQ (2000) Molecular modelling and QSAR of reversible acetylcholinesterase inhibitors. Curr Med Chem 7:273–294

    Article  CAS  PubMed  Google Scholar 

  • Kersken D, Göcke C, Brandt A, Lejzerowicz F, Schwabe E, Seefeldt AM, Veit-Köhler G, Janussen D (2014) The Infauna of three widely distributed sponge species (Hexactinellida and Demospongiae) from the deep Ekström Shelf in the Weddell-Sea, Antarctica. Deep Sea Res II 108:101–112

    Article  Google Scholar 

  • Laport MS, Santos OC, Muricy G (2009) Marine sponges: potential sources of new antimicrobial drugs. Curr Pharm Biotechnol 10:86–105

    Article  CAS  PubMed  Google Scholar 

  • Leal MC, Puga J, Serôdio J, Gomes NCM, Calado R (2012) Trends in the discovery of new marine natural products from invertebrates over the last two decades—where and what are we bioprospecting? PLoS One 7:e30580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lebar MD, Heimbegner JL, Baker BJ (2007) Cold-water marine natural products. Nat Prod Rep 24:774–797

    Article  CAS  PubMed  Google Scholar 

  • Li B, Stribley JA, Ticu A, Xie W, Schopfer LM, Hammond P, Brimijoin S, Hinrichs SH, Lockridge O (2000) Abundant tissue butyrylcholinesterase and its possible function in the acetylcholinesterase knock-out mouse. J Neurochem 75:1320–1331

    Article  CAS  PubMed  Google Scholar 

  • Lippert H, Brinkmeyer R, Mülhaupt T, Iken K (2003) Antimicrobial activity in sub-Arctic marine invertebrates. Polar Biol 26:591–600

    Article  Google Scholar 

  • McClintock JB, Gauthier JJ (1992) Antimicrobial activities of Antarctic sponges. Antarctic Sci 4:179–183

    Article  Google Scholar 

  • McClintock JB, Amsler CD, Baker BJ, Van Soest RWM (2005) Ecology of Antarctic marine sponges: an overview. Integr Comp Biol 45:359–368

    Article  PubMed  Google Scholar 

  • Miceli HM, Diaz AJ, Lee AS (2011) Emerging opportunistic yeast infections. Lancet Infect Dis 11:142–151

    Article  PubMed  Google Scholar 

  • Molinski TF, Dalisay DS, Lievens SL, Saludes JP (2009) Drug development from marine natural products. Nat Rev Drug Discov 9:69–85

    Article  Google Scholar 

  • Munoz-Torrero D (2008) Acetylcholinesterase inhibitors as disease-modifying therapies for Alzheimer’s disease. Curr Med Chem 15:2433–2455

    Article  CAS  PubMed  Google Scholar 

  • Munro M, Blunt J, Dumdei E, Hickford S, Lill R, Li S, Battershill CN, Duckworth AR (1999) The discovery and development of marine compounds with pharmaceutical potential. J Biotechnol 70:15–25

    Article  CAS  PubMed  Google Scholar 

  • Muricy G, Hajdu E, Araujo F V., Hagler AN (1993) Antimicrobial activity of Southwestern Atlantic shallow-water marine sponges (Porifera). In: Uriz MJ, Rützler K (eds) Recent advances in ecology and systematics of sponges, Scientia Marina. pp 427–432

  • Neofytos D, Horn D, De Simone JAJ (2007) Rhodotorula mucilaginosa catheter-related fungemia in a patient with sickle cell disease: case presentation and literature review. South Med J 100:198–200

    Article  PubMed  Google Scholar 

  • Neumann K (ed) (2008) Marine-derived fungi: a source for structurally new and bioactive secondary metabolites. Dissertation, University of Bonn, Bonn

    Google Scholar 

  • Novak Babič M, Zalar P, Ženko B et al (2015) Candida and Fusarium species known as opportunistic human pathogens from customer-accessible parts of residential washing machines. Fungal Biol 119:95–113

    Article  Google Scholar 

  • O’Donnell K, Sutton AD, Rinaldi GM et al (2010) Internet-accessible DNA sequence database for identifying Fusaria from human and animal infections. J Clin Microbiol 48:3708–3718

    Article  PubMed  PubMed Central  Google Scholar 

  • OECD (2011) Test no. 201: freshwater alga and cyanobacteria, growth inhibition test, OECD Guidelines for the testing of chemicals, section 2. OECD Publishing, Paris

    Google Scholar 

  • Orhan IE (2013) Nature: a substantial source of auspicious substances with acetylcholinesterase inhibitory action. Curr Neuropharmacol 11:379–387

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Page M, West L, Northcote P et al (2005) Spatial and temporal variability of cytotoxic metabolites in populations of the New Zealand sponge Mycale hentscheli. J Chem Ecol 31:1161–1174

    Article  CAS  PubMed  Google Scholar 

  • Papaleo MC, Romoli R, Bartolucci G et al (2013) Bioactive volatile organic compounds from Antarctic (sponges) bacteria. New Biotechnol 30:824–838

    Article  CAS  Google Scholar 

  • Perry NB, Ettouati K, Litaudon M, Blunt JW, Munro MHG, Parkin S, Hope H (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 

  • Pezzementi L, Chatonnet A (2010) Evolution of cholinesterases in the animal kingdom. Chem Biol Interact 187:27–33

    Article  CAS  PubMed  Google Scholar 

  • Pfaller MA, Diekema DJ, Gibbs DL, Newell VA, Meis JF, Gould IM, Fu W, Colombo AL, Rodriguez-Noriega E (2007) Results from the ARTEMIS DISK global antifungal surveillance study, 1997–2005: an 8.5-year analysis of susceptibilities of Candida species and other yeast species to fluconazole and voriconazole determined by CLSI standardized disk diffusion testing. J Clin Microbiol 45:1735–1745

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pohanka M (2011) Cholinesterases, a target of pharmacology and toxicology. Biomed Pap 155:219–223

    Article  CAS  Google Scholar 

  • Sacristán-Soriano O, Banaigs B, Becerro MA (2012) Temporal trends in the secondary metabolite production of the sponge Aplysina aerophoba. Mar Drugs 10:677–693

    Article  PubMed  PubMed Central  Google Scholar 

  • Sagar S, Kaur M, Radovanovic A, Bajic VB (2013) Dragon exploration system on marine s ponge compounds interactions. J Cheminform 5:11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sales PM, Souza PM, Simeoni LA, Silveira D (2012) α-Amylase inhibitors: a review of raw material and isolated compounds from plant sources. J Pharm Pharm Sci 15:141–183

    PubMed  Google Scholar 

  • Scannapieco FA, Torres G, Levine MJ (1993) Salivary α-amylase: role in dental plaque and caries formation. Crit Rev Oral Biol Med 4:301–307

    CAS  PubMed  Google Scholar 

  • Schlitzer R (2015) Ocean data view. http://odv.awi.de. Accessed 2 Nov 2015

  • Schmitz FJ, Gunasekera SP, Yalamanchili G, Hossain MB, Van der Helm D (1984) Tedanolide: a potent cytotoxic macrolide from the Caribbean sponge Tedania ignis. J Am Chem Soc 106:7251–7252

    Article  CAS  Google Scholar 

  • Sepčić K, Kauferstein S, Mebs D, Turk T (2010) Biological activities of aqueous and organic extracts from tropical marine sponges. Mar Drugs 8:1550–1566

    Article  PubMed  PubMed Central  Google Scholar 

  • Shaaban M, Abd-Alla HI, Hassan AZ, Aly HF, Ghani MA (2012) Chemical characterization, antioxidant and inhibitory effects of some marine sponges against carbohydrate metabolizing enzymes. Org Med Chem Lett 16:30

    Article  Google Scholar 

  • Simone M, Erba E, Damia G, Vikhanskaya F et al (2005) Variolin B and its derivate deoxy-variolin B: new marine natural compounds with cyclin-dependent kinase inhibitor activity. Eur J Cancer 41:2366–2377

    Article  CAS  PubMed  Google Scholar 

  • Singh AJ, Xu CX, Xu X, West LM, Wilmes A, Chan A, Hamel E, Miller JH, Northcote PT, Ghosh AK (2010) Peloruside B, a potent antitumor macrolide from the New Zealand marine sponge Mycale hentscheli: isolation, structure, total synthesis, and bioactivity. J Org Chem 75:2–10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sutton DA, Brandt ME (2011) Fusarium and other opportunistic hyaline fungi. In: Versalovic J, Jorgensen JH, Funke G, et al. (eds) Manual of clinical microbiology, 10th Edition. American Society of Microbiology, pp 1853–1879

  • Taboada S, García-Fernández LF, Bueno S, Vázquez J, Cuevas C (2010) Antitumoral activity in Antarctic and sub-Antarctic benthic organisms. Antarctic Sci 22:494–507

    Article  Google Scholar 

  • Thakur NL, Anil AC (2000) Antibacterial activity of the sponge Ircinia ramosa: importance of its surface-associated bacteria. J Chem Ecol 26:57–71

    Article  CAS  Google Scholar 

  • Thompson JE, Murphy PT, Berquist PR, Evans EA (1987) Environmentally induced variation in diterpene composition of the marine sponge Rhopaloeides odorabile. Biochem Syst Ecol 15:595–606

    Article  CAS  Google Scholar 

  • Timm C, Mordhorst T, Kock M (2010) Synthesis of 3-alkyl pyridinium alkaloids from the arctic sponge Haliclona viscosa. Mar Drugs 8:483–497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turk T, Ambrožič Avguštin J, Batista U et al (2013) Biological activities of ethanolic extracts from deep-sea antarctic marine sponges. Mar Drugs 11:1126–1139

    Article  PubMed  PubMed Central  Google Scholar 

  • van Asbeck EC, Clemons KV, Stevens DA (2009) Candida parapsilosis: a review of its epidemiology, clinical aspects, typing and antimicrobial susceptibility. Crit Rev Microbiol 35:283–309

    Article  PubMed  Google Scholar 

  • Xin Y, Kanagasabhapathy M, Janussen D, Xue S, Zhang W (2011) Phylogenetic diversity of Gram-positive bacteria cultured from Antarctic deep-sea sponges. Polar Biol 34:1501–1512

    Article  Google Scholar 

  • Zalar P, Novak M, de Hoog GS, Gunde-Cimerman N (2011) Dishwashers—a man-made ecological niche accommodating human opportunistic fungal pathogens. Fungal Biol 115:997–1007

    Article  CAS  PubMed  Google Scholar 

  • Zhen Z, Jing Z, Caihuan KE, Dexiang W (2013) Antimicrobial activities of novel cultivable bacteria isolated from marine sponge Tedania anhelans. Chin J Oceanol Limnol 31:581–590

    Article  Google Scholar 

Download references

Acknowledgments

The authors gratefully acknowledge the Slovenian Research Agency (Research Programmes P1-0207, P4-0127, P1-0055, and P1-0198), the ERASMUS Student Mobility Programme for financial support to MK, LS and ML, and Deutsche Forschungsgemeinschaft for financial support for the Antarctic sponge research project by DJ (JA-1063/17-1). We acknowledge the financial support received from the Ministry of Education, Science and Sport and the University of Ljubljana via the “Innovative scheme for co-financing of doctoral studies,” the Slovenian Research Agency through the Infrastructural Centre Mycosmo, MRIC UL, and the Centre of Excellence for Integrated Approaches in Chemistry and Biology of Proteins (CIPKeBiP). Dr. Chris Berrie is greatly acknowledged for editing and appraisal of the manuscript.

Author information

Authors and Affiliations

  1. Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia

    Sabina Berne, Martina Kalauz, Marko Lapat, Lora Savin, Jerneja Ambrožič Avguštin, Nina Gunde-Cimerman, Tom Turk & Kristina Sepčić

  2. Department of Biotechnology, University of Rijeka, Rijeka, Croatia

    Martina Kalauz, Marko Lapat & Lora Savin

  3. Senckenberg Research Institute and Nature Museum, Frankfurt am Main, Germany

    Dorte Janussen & Daniel Kersken

  4. Faculty of Medicine, Institute of Biophysics, University of Ljubljana, Ljubljana, Slovenia

    Špela Zemljič Jokhadar

  5. Medex d.o.o., Ljubljana, Slovenia

    Domen Jaklič

  6. Centre of Excellence for Integrated Approaches in Chemistry and Biology of Proteins (CIPKeBiP), Jamova 39, 1000, Ljubljana, Slovenia

    Nina Gunde-Cimerman

  7. Chair of Pharmaceutical Biology, Faculty of Pharmacy, University of Ljubljana, Ljubljana, Slovenia

    Mojca Lunder & Irena Roškar

  8. National Institute of Biology, Ljubljana, Slovenia

    Tina Eleršek

Authors
  1. Sabina Berne
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Martina Kalauz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marko Lapat
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Lora Savin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Dorte Janussen
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Daniel Kersken
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jerneja Ambrožič Avguštin
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Špela Zemljič Jokhadar
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Domen Jaklič
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Nina Gunde-Cimerman
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Mojca Lunder
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Irena Roškar
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Tina Eleršek
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Tom Turk
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Kristina Sepčić
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kristina Sepčić.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 17 kb)

Supplementary material 2 (DOCX 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Berne, S., Kalauz, M., Lapat, M. et al. Screening of the Antarctic marine sponges (Porifera) as a source of bioactive compounds. Polar Biol 39, 947–959 (2016). https://doi.org/10.1007/s00300-015-1835-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-015-1835-4

Keywords

Search

Navigation