Planta Med 2016; 82(09/10): 767-774
DOI: 10.1055/s-0042-105652
Mini Reviews
Georg Thieme Verlag KG Stuttgart · New York

Ecological and Pharmacological Activities of Antarctic Marine Natural Products

Conxita Avila
Further Information

Publication History

received 23 December 2015
revised 17 March 2016

accepted 22 March 2016

Publication Date:
24 May 2016 (online)

Abstract

Antarctic benthic communities are regulated by abundant interactions of different types among organisms, such as predation, competition, etc. Predators are usually sea stars, with omnivorous habits, as well as other invertebrates. Against this strong predation pressure, many organisms have developed all sorts of defensive strategies, including chemical defenses. Natural products are thus quite common in Antarctic organisms with an important ecological and pharmacological potential. In this paper, the chemical defenses of the Antarctic organisms studied during the ECOQUIM and ACTIQUIM projects, as well as their pharmacological potential, are reviewed. For the ecological defenses, predation against the sea star Odontaster validus is analyzed and evaluated along depth gradients as well as considering the lifestyle of the organisms. For the pharmacological activity, the anticancer, anti-inflammatory, and antibacterial activities tested are evaluated here. Very often, only crude extracts or fractions have been tested so far, and therefore, the natural products responsible for such activities remain yet to be identified. Even if the sampling efforts are not uniform along depth, most ecologically active organisms are found between 200 and 500 m depth. Also, from the samples studied, about four times more sessile organisms possess chemical defenses against the sea star than the vagile ones; these represent 50 % of sessile organisms and 35 % of the vagile ones, out of the total tested, being active. Pharmacological activity has not been tested uniformly in all groups, but the results show that relevant activity is found in different phyla, especially in Porifera, Cnidaria, Bryozoa, and Tunicata, but also in others. No relationship between depth and pharmacological activity can be established with the samples tested so far. More studies are needed in order to better understand the ecological relationships among Antarctic invertebrates mediated by natural products and to fully explore their pharmacological potential.

 
  • References

  • 1 Dayton PK, Robilliard GA, Paine RT, Dayton LB. Biological accommodation in the benthic community at McMurdo Sound, Antarctica. Ecol Monogr 1974; 44: 105-128
  • 2 Arntz WE, Brey T, Gallardo VA. Antarctic zoobenthos. Oceanogr Mar Biol Ann Rev 1994; 32: 241-304
  • 3 Clarke A, Aronson RB, Crame JA, Gili JM, Blake DB. Evolution and diversity of the benthic fauna of the Southern Ocean continental shelf. Antarct Sci 2004; 16: 559-568
  • 4 Avila C, Taboada S, Núñez-Pons L. Antarctic marine chemical ecology: what is next?. Mar Ecol 2008; 29: 1-71
  • 5 Taboada S, Núñez-Pons L, Avila C. Feeding repellence of Antarctic and sub-Antarctic benthic invertebrates against the omnivorous seastar Odontaster validus . Polar Biol 2013; 36: 13-25
  • 6 Kijjoa A, Sawangwong P. Drugs and cosmetics from the sea. Mar Drugs 2004; 2: 73-82
  • 7 Albericio F, Álvarez M, Cuevas C, Francesch A, Pla D, Tulla-Puche J. The sea as a source of new drugs. In: Tamaki N, Kuge Y, editors Molecular imaging for integrated medical therapy and drug development. Tokyo: Springer Japan; 2010: 237-249
  • 8 Newman DJ, Cragg GM. Natural products as sources of new drugs over the 30 years from 1981 to 2010. J Nat Prod 2012; 75: 311-335
  • 9 Jha RK, Zi-rong X. Biomedical compounds from marine organisms. Mar Drugs 2004; 2: 123-146
  • 10 Mayer AMS, Rodríguez AD, Berlinck RGS, Fusetani N. Marine pharmacology in 2007–8: marine compounds with antibacterial, anticoagulant, antifungal, anti-inflammatory, antimalarial, antiprotozoal, antituberculosis, and antiviral activities; affecting the immune and nervous system, and other miscellaneous mechanisms of action. Comp Biochem Physiol C Toxicol Pharmacol 2011; 153: 191-222
  • 11 Lebar MD, Heimbegner JL, Baker BJ. Cold-water marine natural products. Nat Prod Rep 2007; 24: 774-797
  • 12 Blunt JW, Copp BR, Keyzers R, Munro MHG, Prinsep MR. Marine natural products. Nat Prod Rep 2014; 31: 160-258
  • 13 Avila C, Iken K, Fontana A, Cimino G. Chemical ecology of the Antarctic nudibranch Bathydoris hodgsoni Eliot, 1907: defensive role and origin of its natural products. J Exp Mar Bio Ecol 2000; 252: 27-44
  • 14 Iken K, Avila C, Fontana A, Gavagnin M. Chemical ecology and origin of defensive compounds in the Antarctic nudibranch Austrodoris kerguelenensis (Opisthobranchia: Gastropoda). Mar Biol 2002; 141: 101-109
  • 15 Figuerola B, Núñez-Pons L, Vázquez J, Taboada S, Cristobo FJ, Ballesteros M, Avila C. Chemical interactions in Antarctic marine benthic ecosystems. In: Cruzado A, editor Marine ecosystems. Rijeka, Croatia: In-Tech; 2012: 105-126
  • 16 Figuerola B, Núñez-Pons L, Moles J, Avila C. Feeding repellence in Antarctic bryozoans. Naturwissenschaften 2013; 100: 1069-1081
  • 17 Figuerola B, Núñez-Pons L, Monleón-Getino T, Avila C. Chemo-ecological interactions in Antarctic bryozoans. Polar Biol 2014; 37: 1017-1030
  • 18 Moles J, Núñez-Pons L, Taboada S, Figuerola B, Cristobo J, Avila C. Anti-predatory chemical defences of Antarctic benthic fauna. Mar Biol 2015; 162: 1813-1821
  • 19 Núnez-Pons L, Forestieri R, Nieto RM, Varela M, Nappo M, Rodríguez J, Jiménez C, Castelluccio F, Carbone M, Ramos-Esplá A, Gavagnin M, Avila C. Chemical defenses of tunicates of the genus Aplidium from the Weddell Sea (Antarctica). Polar Biol 2010; 33: 1319-1329
  • 20 Núñez-Pons L, Carbone M, Paris D, Melck D, Ríos P, Cristobo J, Castelluccio F, Gavagnin M, Avila C. Chemo-ecological studies on Hexactinellid sponges from the Southern Ocean. Naturwissenschaften 2012; 99: 353-368
  • 21 Núñez-Pons L, Carbone M, Vázquez J, Rodríguez J, Nieto RM, Varela MM, Gavagnin M, Avila C. Natural products from Antarctic colonial ascidians of the genera Aplidium and Synoicum: variability and defensive role. Mar Drugs 2012; 10: 1741-1764
  • 22 Reyes F, Fernández R, Rodríguez A, Francesch A, Taboada S, Avila C, Cuevas C. Aplicyanins A–F, new cytotoxic bromoindole derivatives from the marine tunicate Aplidium cyaneum . Tetrahedron 2008; 64: 5119-5123
  • 23 Taboada S, García-Fernández LF, Bueno S, Vázquez J, Cuevas C, Avila C. Antitumoural activity in Antarctic and sub-Antarctic benthic organisms. Ant Sci 2010; 22: 494-507
  • 24 Moles J, Torrent A, Alcaraz MJ, Ruhí R, Avila C. Anti-inflammatory activity in selected Antarctic benthic organisms. Front Mar Sci 2014; 1
  • 25 Figuerola B, Sala-Comorera L, Angulo-Preckler C, Vázquez J, Montes MJ, García-Aljaro C, Mercadé E, Blanch AR, Avila C. Antimicrobial activity of Antarctic bryozoans: an ecological perspective with potential for clinical applications. Mar Environ Res 2014; 101: 52-59
  • 26 Núñez-Pons L, Carbone M, Vázquez J, Gavagnin M, Avila C. Lipophilic defenses from Alcyonium soft corals of Antarctica. J Chem Ecol 2013; 39: 675-685
  • 27 Núnez-Pons L, Avila C. Deterrent activities in the crude lipophilic fractions of Antarctic benthic organisms: chemical defences against keystone predators. Polar Res 2014; 33: 21624
  • 28 Clarke A, Johnston NM. Antarctic marine benthic diversity. Oceanogr Mar Biol Ann Rev 2003; 41: 47-114
  • 29 Griffiths HJ. Antarctic marine biodiversity – what do we know about the distribution of life in the Southern Ocean?. PLoS One 2010; 5: e11683
  • 30 Barnes DK, Conlan KE. Disturbance, colonization and development of Antarctic benthic communities. Philos Trans R Soc Lond B Biol Sci 2007; 362: 11-38
  • 31 Gutt J, Sirenko BI, Arntz WE, Smirnov IS, De Broyer C. Biodiversity of the Weddell Sea: macrozoobenthic species (demersal fish included) sampled during the expedition ANT XIII3 (EASIZ I) with RV ‘Polarstern’. Ber Polarforsch/Rep Polar Res 2000; 372: 1-118
  • 32 Núñez-Pons L, Avila C. Natural products mediating ecological interactions in Antarctic benthic communities: a mini-review of the known molecules. Nat Prod Rep 2015; 32: 1114-1130
  • 33 Núñez-Pons L, Rodríguez-Arias M, Gómez-Garreta A, Ribera-Siguán A, Avila C. Feeding deterrency in Antarctic marine organisms: bioassays with the omnivore amphipod Cheirimedon femoratus . Mar Ecol Prog Ser 2012; 462: 163-174
  • 34 Angulo-Preckler C, Cid C, Oliva F, Avila C. Antifouling activity in some benthic Antarctic invertebrates by in situ experiments at Deception Island, Antarctica. Mar Environ Res 2015; 105: 30-38
  • 35 Figuerola B, Taboada S, Monleón-Getino T, Vázquez J, Avila C. Cytotoxic activity of Antarctic benthic organisms against the common sea urchin Sterechinus neumayeri . Oceanography 2013; 1: 1-9
  • 36 Núnez-Pons L, Avila C. Defensive metabolites from Antarctic invertebrates: does energetic content interfere with feeding repellence?. Mar Drugs 2014; 12: 3770-3791
  • 37 Carbone M, Núñez-Pons L, Castelluccio F, Avila C, Gavagnin M. Illudalane sesquiterpenoids of the alcyopterosin series from the Antarctic marine soft coral Alcyonium grandis . J Nat Prod 2009; 72: 1357-1360
  • 38 Amsler CD, McClintock JB, Baker BJ. Chemical defenses of Antarctic marine organisms: a reevaluation of the latitudinal hypothesis. In: Davidson W, Howard-Williams C, Broady P, editors Antarctic ecosystems: models for wider ecological understanding. Christchurch: New Zealand Natural Sciences; 2000: 158-164
  • 39 McClintock JB, Amsler CD, Baker B. Overview of the chemical ecology of benthic marine invertebrates along the Western Antarctic Peninsula. Integr Comp Biol 2010; 50: 967-980
  • 40 De Broyer C, Koubbi P, Griffiths HJ, Raymond B, Udekem dʼAcoz C, Van de Putte AP, Danis B, David B, Grant S, Gutt J, Held C, Hosie G, Huettmann F, Post A, Ropert-Coudert Y. Biogeographic atlas of the Southern Oceans. Cambridge, UK: Scientific Committee on Antarctic Research; 2014
  • 41 Antonov AS, Avilov SA, Kalinovsky AI, Anastyuk SD, Dmitrenok PS, Evtushenko EV, Kalinin VI, Smirnov AV, Taboada S, Ballesteros M, Avila C, Stonik VA. Triterpene glycosides from Antarctic sea cucumbers. 1. Structure of liouvillosides A1, A2, A3, B1, and B2 from the sea cucumber Staurocucumis liouvillei: new procedure for separation of highly polar glycoside fractions and taxonomic revision. J Nat Prod 2008; 71: 1677-1685
  • 42 Antonov AS, Avilov SA, Kalinovsky AI, Anastyuk SD, Dmitrenok PD, Kalinin VI, Taboada S, Bosch A, Avila C, Stonik VA. Triterpene glycosides from Antarctic sea cucumbers. 2. Structure of Achlioniceosides A1, A2, and A3 from the Sea Cucumber Achlionice violaecuspidata (= Rhipidothuria racowitzai). J Nat Prod 2009; 72: 33-38
  • 43 Antonov AS, Avilov SA, Kalinovsky AI, Dmitrenok PS, Kalinin VI, Taboada S, Ballesteros M, Avila C. Triterpene glycosides from Antarctic sea cucumbers III. Structures of liouvillosides A(4) and A(5), two minor disulfated tetraosides containing 3-O-methylquinovose as terminal monosacharide units from the sea cucumber Staurocucumis liouvillei (Vaney). Nat Prod Res 2011; 25: 1324-1333
  • 44 Carbone M, Núñez-Pons L, Paone M, Castelluccio F, Avila C, Gavagnin M. Rossinone-related meroterpenes from the Antarctic tunicate Aplidium fuegiense . Tetrahedron 2012; 68: 3541-3544
  • 45 Carbone M, Núñez-Pons L, Ciavatta ML, Castelluccio F, Avila C, Gavagnin M. Occurrence of a taurine derivative in an Antarctic glass sponge. Nat Prod Commun 2014; 9: 469-470
  • 46 Cutignano A, Zhang W, Avila C, Cimino G, Fontana A. Intrapopulation variability in the terpene metabolism of the Antarctic opisthobranch mollusc Austrodoris kerguelenensis . Eur J Org Chem 2011; 27: 5383-5389
  • 47 Cutignano A, Moles J, Avila C, Fontana A. Granuloside, a unique linear homosesterterpene from the Antarctic nudibranch Charcotia granulosa . J Nat Prod 2015; 78: 1761-1764
  • 48 Iken K, Avila C, Ciavatta ML, Fontana A, Cimino G. Hodgsonal, a new drimane sesquiterpene from the mantle of the Antarctic nudibranch Bathydoris hodgsoni . Tetrahedron Lett 1998; 39: 5635-5638
  • 49 Núñez-Pons L, Nieto RM, Avila C, Jiménez C, Rodríguez J. Mass spectrometry detection of minor new meridianins from the Antarctic colonial ascidians Aplidium falklandicum and Aplidium meridianum . J Mass Spectrom 2015; 50: 103-111
  • 50 Silchenko AS, Kalinovsky AI, Avilov SA, Andryjashchenko PV, Dmitrenok PS, Kalinin VI, Taboada S, Avila C. Triterpene glycosides from Antarctic sea cucumbers IV. Turquetoside A, a 3-O-methylquinovose containing disulfated tetraoside from the sea cucumber Staurocucumis turqueti (Vaney, 1906) (= Cucumaria spatha). Biochem Syst Ecol 2013; 51: 45-49