Skip to main content
Log in

A comprehensive evaluation of the potential chemical defenses of antarctic ascidians against sympatric fouling microorganisms

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

Abstract

The present study analyzed the bioactivity of whole body extracts from six solitary and eight colonial ascidian taxa against 20 sympatric bacterial isolates and one sympatric diatom species from the Western Antarctic Peninsula. Ascidians had crude lipophilic and hydrophilic extracts assayed against 20 bacterial strains. The lipophilic extract of one ascidian caused growth inhibition in all bacterial isolates at 3× tissue-level concentrations. The lipophilic and hydrophilic extracts were fractionated into seawater-soluble and insoluble fractions and assayed at three concentrations against a sympatric diatom species. Significant diatom mortality was detected at 3× and 1× concentrations in all but one ascidian taxon. Lipophilic fractions caused higher diatom mortality than hydrophilic extracts. The specificity of secondary metabolites against diatom fouling and the lack of activity against bacteria suggest high selective pressure for chemical defenses against diatom fouling or the potential that bacterial pathogens are controlled by the ascidian immune system.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Amsler CD, Moeller CB, McClintock JB, Iken KB, Baker BJ (2000) Chemical defenses against diatom fouling in Antarctic marine sponges. Biofouling 16(1):29–45

    Article  CAS  Google Scholar 

  • Amsler CD, Okogbue IN, Landry DM, Amsler MO, McClintock JB, Baker BJ (2005) Potential chemical defenses against diatom fouling in Antarctic macroalgae. Bot Mar 48(4):318–322. doi:10.1515/bot.2005.041

    Article  Google Scholar 

  • Azumi K, Yokosawa H, Ishii S (1990a) Halocyamines—Novel antimicrobial tetrapeptide-like substances isolated from the hemocytes of the solitary ascidian Halocynthia roretzi. Biochemistry 29(1):159–165

    Article  CAS  Google Scholar 

  • Azumi K, Yoshimizu M, Suzuki S, Ezura Y, Yokosawa H (1990b) Inhibitory effect of halocyamine, an antimicrobial substance from ascidian hemocytes, on the growth of fish viruses and marine bacteria. Cell Mol Life Sci 46(10):1066–1068. doi:10.1007/bf01940675

    Article  CAS  Google Scholar 

  • Ballarin L, Franchini A, Ottaviani E, Sabbadin A (2001) Morula cells as the major immunomodulatory hemocytes in ascidians: evidences from the colonial species Botryllus schlosseri. Biol Bull 201(1):59–64

    Article  CAS  Google Scholar 

  • Bandurraga MM, Fenical W (1985) Isolation of the muricins: evidence of a chemical adaptation against fouling in the marine octocoral Muricea fruticosa (gorgonacea). Tetrahedron 41(6):1057–1065. doi:10.1016/s0040-4020(01)96473-7

    Article  CAS  Google Scholar 

  • Barthel D, Wolfrath B (1989) Tissue sloughing in the sponge Halichondria panicea a fouling organism prevents being fouled. Oecologia 78(3):357–360. doi:10.1007/bf00379109

    Article  Google Scholar 

  • Bavestrello G, Arillo A, Calcinai B, Cattaneo-Vietti R, Cerrano C, Gaino E, Penna A, Sara M (2000) Parasitic diatoms inside antarctic sponges. Biol Bull 198(1):29–33

    Article  CAS  Google Scholar 

  • Bernan VS (2001) Metabolites of free-living, commensal, and symbiotic benthic marine microorganisms. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton, pp 567–591

    Chapter  Google Scholar 

  • Bryan PJ, McClintock JB, Slattery M, Rittschof DP (2003) A comparative study of the non-acidic chemically mediated antifoulant properties of three sympatric species of ascidians associated with seagrass habitats. Biofouling 19(4):235–245

    Article  CAS  Google Scholar 

  • Caldwell GS, Olive PJW, Bentley MG (2002) Inhibition of embryonic development and fertilization in broadcast spawning marine invertebrates by water soluble diatom extracts and the diatom toxin 2-trans, 4-trans decadienal. Aquatic Toxicol 60(1–2):123–137. doi:10.1016/s0166-445x(01)00277-6

    Article  CAS  Google Scholar 

  • Cerrano C, Arillo A, Bavestrello G, Calcinai B, Cattaneo-Vietti R, Penna A, Sarà M, Totti C (2000) Diatom invasion in the antarctic hexactinellid sponge Scolymastra joubini. Polar Biol 23(6):441–444. doi:10.1007/s003000050466

    Article  Google Scholar 

  • Cerrano C, Calcinai B, Cucchiari E, Camillo C, Totti C, Bavestrello G (2004) The diversity of relationships between Antarctic sponges and diatoms: the case of Mycale acerata Kirkpatrick, 1907 (Porifera, Demospongiae). Polar Biol 27(4):231–237. doi:10.1007/s00300-003-0581-1

    Article  Google Scholar 

  • Cooper ELP, Nicolò (2001) Immunodefense in tunicates: cells and molecules. In: Sawada H, Yokosawa H, Lambert CC (eds) The biology of ascidians. Springer, Tokyo, pp 381–394

    Google Scholar 

  • Cox G (1986) Comparison of Prochloron from different hosts. I. Structural and ultrastructural characteristics. New Phytol 104(3):429–445

    Google Scholar 

  • Davis AR, Wright AE (1989) Interspecific differences in fouling of two congeneric ascidians (Eudistoma olivaceum and E. capsulatum): is surface acidity an effective defense? Mar Biol V102(4):491–497

    Google Scholar 

  • Davis AR, Targett NM, McConnell OJ, Young CM (1989) Epibiosis of marine algae and benthic invertebrates: natural products chemistry and other mechanisms inhibiting settlement and overgrowth. In: Scheuer PJ (ed) Bioorganic marine chemistry, vol 3. Springer, Berlin, pp 86–114

    Chapter  Google Scholar 

  • Dobretsov S, Dahms H-U, Qian P-Y (2006) Inhibition of biofouling by marine microorganisms and their metabolites. Biofouling 22(1):43–54

    Article  CAS  Google Scholar 

  • Donia MS, Hathaway BJ, Sudek S, Haygood MG, Rosovitz MJ, Ravel J, Schmidt EW (2006) Natural combinatorial peptide libraries in cyanobacterial symbionts of marine ascidians. Nat Chem Biol 2(12):729–735. http://www.nature.com/nchembio/journal/v2/n12/suppinfo/nchembio829_S1.html

    Google Scholar 

  • Ducklow H, Carlson C, Church M, Kirchman D, Smith D, Steward G (2001) The seasonal development of the bacterioplankton bloom in the Ross Sea, Antarctica, 1994–1997. Deep Sea Res Part II Topical Stud Oceanogr 48(19–20):4199–4221. doi:10.1016/s0967-0645(01)00086-8

    Article  CAS  Google Scholar 

  • El-Sayed SZ, Fryxell GA (1993) Phytoplankton. In: Friedman IE (ed) Antarctic microbiology. Wiley, New York, pp 65–122

    Google Scholar 

  • Engel S, Jensen PR, Fenical W (2002) Chemical ecology of marine microbial defense. J Chem Ecol 28(10):1971–1985. doi:10.1023/a:1020793726898

    Article  CAS  Google Scholar 

  • Findlay C, Smith VJ (1995) Antibacterial activity in the blood cells of the solitary ascidian, Ciona intestinalis, in vitro. J Exp Zool 273(5):434–444. doi:10.1002/jez.1402730507

    Article  Google Scholar 

  • Franks A, Haywood P, Holmstrom C, Egan S, Kjelleberg S, Kumar N (2005) Isolation and structure elucidation of a novel yellow pigment from the marine bacterium Pseudoalteromonas tunicata. Molecules 10(10):1286–1291

    Article  CAS  Google Scholar 

  • Fujita T, Matsushita M, Endo Y (2004) The lectin-complement pathway—its role in innate immunity and evolution. Immunol Rev 198(1):185–202. doi:10.1111/j.0105-2896.2004.0123.x

    Article  CAS  Google Scholar 

  • Hirose E (2005) Phylogeny of ascidian-Prochloron symbiosis. Zool Sci 22(12):1417

    Google Scholar 

  • Hirose E (2009) Ascidian tunic cells: morphology and functional diversity of free cells outside the epidermis. Invertebr Biol 128(1):83–96. doi:10.1111/j.1744-7410.2008.00153.x

    Article  Google Scholar 

  • Holmström C, Egan S, Franks A, McCloy S, Kjelleberg S (2002) Antifouling activities expressed by marine surface associated Pseudoalteromonas species. FEMS Microbiol Ecol 41(1):47–58. doi:10.1111/j.1574-6941.2002.tb00965.x

    Article  Google Scholar 

  • Hoyle G (1953) Spontaneous squirting of an ascidian, Phallusia mammillata (Cuvier). J Mar Biol Assoc UK 31:541–562

    Article  Google Scholar 

  • Ianora A, Miralto A, Poulet SA, Carotenuto Y, Buttino I, Romano G, Casotti R, Pohnert G, Wichard T, Colucci-D’Amato L, Terrazzano G, Smetacek V (2004) Aldehyde suppression of copepod recruitment in blooms of a ubiquitous planktonic diatom. Nature 429(6990):403–407. http://www.nature.com/nature/journal/v429/n6990/suppinfo/nature02526_S1.html

    Google Scholar 

  • Koplovitz G, McClintock J, Amsler C, Baker B (2009) Palatability and chemical anti-predatory defenses in common ascidians from the Antarctic Peninsula. Aquatic Biol 7(1–2):81–92. doi:10.3354/ab00188

    Article  Google Scholar 

  • Kowalke J (1999) Filtration in antarctic ascidians—striking a balance. J Exp Mar Biol Ecol 242:233–244

    Article  Google Scholar 

  • Lambert G (1968) The general ecology and growth of a solitary ascidian, Corella willmeriana. Biol Bull 135(2):296–307

    Article  Google Scholar 

  • Lambert G, Lambert CC, Waaland JR (1996) Algal symbionts in the tunics of six New Zealand ascidians (Chordata, Ascidiacea). Invertebr Biol 115(1):67–78

    Article  Google Scholar 

  • Lebar M, Luttenton L, McClintock J, Amsler C, Baker B (2011) Accumulation of vanadium, manganese, and nickel in Antarctic tunicates. Polar Biol 34(4):587–590. doi:10.1007/s00300-010-0902-0

    Article  Google Scholar 

  • McClintock JB, Baker BJ (1997) A review of the chemical ecology of Antarctic marine invertebrates. Am Zool 37(4):329–342. doi:10.1093/icb/37.4.329

    CAS  Google Scholar 

  • McClintock JB, Amsler MO, Amsler CD, Southworth KJ, Petrie C, Baker BJ (2004) Biochemical composition, energy content and chemical antifeedant and antifoulant defenses of the colonial antarctic ascidian Distaplia cylindrica. Mar Biol 145(6):885–894

    Article  CAS  Google Scholar 

  • McLachlan J (1973) Growth media, marine. In: Stein JR (ed) Handbook of phycological methods. Cambridge University Press, Cambridge, pp 25–51

    Google Scholar 

  • Miralto A, Barone G, Romano G, Poulet SA, Ianora A, Russo GL, Buttino I, Mazzarella G, Laabir M, Cabrini M, Giacobbe MG (1999) The insidious effect of diatoms on copepod reproduction. Nature 402(6758):173–176. http://www.nature.com/nature/journal/v402/n6758/suppinfo/402173a0_S1.html

    Google Scholar 

  • Monteiro SM, Chapman MG, Underwood AJ (2002) Patches of the ascidian Pyura stolonifera (Heller, 1878): structure of habitat and associated intertidal assemblages. J Exp Mar Biol Ecol 270(2):171–189

    Article  Google Scholar 

  • Moss C, Green DH, Pérez B, Velasco A, Henríquez R, McKenzie JD (2003) Intracellular bacteria associated with the ascidian Ecteinascidia turbinata phylogenetic and in situ hybridisation analysis. Mar Biol 143(1):99–110. doi:10.1007/s00227-003-1060-5

    Article  CAS  Google Scholar 

  • Murray AE, Preston CM, Massana R, Taylor LT, Blakis A, Wu K, DeLong EF (1998) Seasonal and spatial variability of bacterial and archaeal assemblages in the coastal waters near Anvers Island, Antarctica. Appl Environ Microbiol 64(7):2585–2595

    CAS  Google Scholar 

  • Murugan A, Ramasamy MS (2003) Biofouling deterrent activity of the natural product from ascidian, Distaplia nathensis [Chordata]. Indian J Mar Sci 32(2):162–164

    Google Scholar 

  • Parry DL (1984) Chemical properties of the test of ascidians in relation to predation. Mar Ecol Prog Ser 17(3):279–282

    Article  CAS  Google Scholar 

  • Peters K, Amsler C, McClintock J, Baker B (2009) Potential chemical defenses of Antarctic sponges against sympatric microorganisms. Polar Biol 33(5):649–658

    Article  Google Scholar 

  • Pisut DP, Pawlik JR (2002) Anti-predatory chemical defenses of ascidians: secondary metabolites or inorganic acids? J Exp Mar Biol Ecol 270(2):203–214

    Article  CAS  Google Scholar 

  • Ramasamy MS, Murugan A (2003) Chemical defense in ascidians Eudistoma viride and Didemnum psammathodes in Tuticorin, southeast coast of India: bacterial epibiosis and fouling deterrent activity. Indian J Mar Sci 32(4):337–339

    CAS  Google Scholar 

  • Ramos-Esplá AA, Carcel JA, Varela M (2005) Zoogeographical relationships of the littoral ascidiofauna around the Antarctic Peninsula, in the Scotia Arc and in the Magellan region. Sci Mar 69:215–223

    Google Scholar 

  • Raub MF, Cardellina JH, Spande TF (1992) The Piclavines, antimicrobial indolizidines from the tunicate Clavelina Picta. Tetrahedron Lett 33(17):2257–2260

    Article  CAS  Google Scholar 

  • Rhoades DF (1979) Evolution of plant chemical defense against herbivores. In: Rosenthal G, Janzen D (eds) Herbivores: their interaction with secondary plant metabolites. Academic Press, New York, pp 3–54

    Google Scholar 

  • Sahade R, Tatián M, Kowalke J, Kühne S, Esnal GB (1998) Benthic faunal associations on soft substrates at Potter Cove, King George Island, Antarctica. Polar Biol 19(2):85–91

    Article  Google Scholar 

  • Salomon CE, Faulkner DJ (2002) Localization studies of bioactive cyclic peptides in the ascidian Lissoclinum patella. J Nat Prod 65(5):689–692. doi:10.1021/np010556f

    Article  CAS  Google Scholar 

  • Schmidt EW, Nelson JT, Rasko DA, Sudek S, Eisen JA, Haygood MG, Ravel J (2005) Patellamide A and C biosynthesis by a microcin-like pathway in Prochloron didemni, the cyanobacterial symbiont of Lissoclinum patella. Proc Natl Acad Sci USA 102(20):7315–7320. doi:10.1073/pnas.0501424102

    Article  CAS  Google Scholar 

  • Schuett C, Doepke H, Groepler W, Wichels A (2005) Diversity of intratunical bacteria in the tunic matrix of the colonial ascidian Diplosoma migrans. Helgol Mar Res 59(2):136–140. doi:10.1007/s10152-004-0212-4

    Article  Google Scholar 

  • Seleghim M, de Lira S, Campana P, Berlinck R, Custódio M (2007) Localization of granulatimide alkaloids in the tissues of the ascidian Didemnum granulatum. Mar Biol 150(5):967–975

    Article  CAS  Google Scholar 

  • Simmons TL, Coates RC, Clark BR, Engene N, Gonzalez D, Esquenazi E, Dorrestein PC, Gerwick WH (2008) Biosynthetic origin of natural products isolated from marine microorganismal invertebrate assemblages. Proc Natl Acad Sci USA 105(12):4587–4594. doi:10.1073/pnas.0709851105

    Article  CAS  Google Scholar 

  • Steinberg PD, De Nys R (2002) Chemical mediation of colonization of seaweed surfaces. J Phycol 38(4):621–629. doi:10.1046/j.1529-8817.2002.02042.x

    Article  CAS  Google Scholar 

  • Steinberg PD, De Nys R, Kjelleberg S (2002) Chemical mediation of surface colonization. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton (FL), pp 355–387

    Google Scholar 

  • Stoecker D (1978) Resistance of a tunicate to fouling. Biol Bull 155(3):615–626

    Article  Google Scholar 

  • Stoecker D (1980) Relationships between chemical defense and ecology in benthic ascidians. Mar Ecol Prog Ser 3:257–265

    Article  CAS  Google Scholar 

  • Tatian M, Sahade RJ, Doucet ME, Esnal GB (1998) Ascidians (Tunicata, ascidiacea) of Potter Cove, South Shetland Islands, Antarctica. Antarct Sci 10(2):147–152

    Article  Google Scholar 

  • Tatian M, Antacli JC, Sahade R (2005) Ascidians (Tunicata, Ascidiacea): species distribution along the Scotia Arc. Sci Mar 69:205–214

    Article  Google Scholar 

  • Teo SLM, Ryland JS (1995) Potential antifouling mechanisms using toxic chemicals in some British ascidians. J Exp Mar Biol Ecol 188(1):49–62

    Article  CAS  Google Scholar 

  • Tsukamoto S, Kato H, Hirota H, Fusetani N (1994) Antibacterial and antifungal sulfated alkane and alkenes from the hepatopancreas of the ascidian Halocynthia roretzi. J Nat Prod 57(11):1606–1609. doi:10.1021/np50113a027

    Article  CAS  Google Scholar 

  • Wahl M (1989) Marine epibiosis. I. Fouling and antifouling: some basic aspects. Mar Ecol Prog Ser 58:175–189

    Article  Google Scholar 

  • Wahl M (1995) Bacterial epibiosis on Bahamian and Pacific ascidians. J Exp Mar Biol Ecol 191(2):239–255

    Article  Google Scholar 

  • Wahl M, Banaigs B (1991) Marine epibiosis. III. Possible antifouling defense adaptations in Polysyncraton lacazei (Giard) (Didemnidae, Ascidiacea). J Exp Mar Biol Ecol 145(1):49–63. doi:10.1016/0022-0981(91)90005-h

  • Wahl M, Jensen PR, Fenical W (1994) Chemical control of bacterial epibiosis on ascidians. Mar Ecol Prog Ser 110(1):45–57

    Article  Google Scholar 

  • Walters LJ, Hadfield MG, Smith CM (1996) Waterborne chemical compounds in tropical macroalgae: positive and negative cues for larval settlement. Mar Biol 126(3):383–393. doi:10.1007/bf00354620

    Article  Google Scholar 

  • Yokobori S, Kurabayashi A, Neilan BA, Maruyama T, Hirose E (2006) Multiple origins of the ascidian-Prochloron symbiosis: molecular phylogeny of photosymbiotic and non-symbiotic colonial ascidians inferred from 18S rDNA sequences. Mol Phylogenet Evol 40(1):8–19. doi:10.1016/j.ympev.2005.11.025

    Article  CAS  Google Scholar 

  • Zar JH (2009) Biostatistical analysis, 5th edn. Prentice Hall, New Jersey

    Google Scholar 

Download references

Acknowledgments

We thank Margaret Amsler, Craig Aumack, Jill Zamzow, and Philip Bucolo for their assistance with field collections. We are very grateful to Linda Cole at the Smithsonian Institution in Washington, DC, for her assistance with ascidian taxonomy. We wish to acknowledge the generous logistical support provided by those individuals employed by Raytheon Polar Services Company. This research was facilitated by NSF awards to CDA and JBM (OPP-0442769) and to BJB (OPP-0442857). JBM acknowledges the support of an Endowed Research Professorship in Polar and Marine Biology through the University of Alabama at Birmingham.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to James B. McClintock.

Additional information

Communicated by F. Bulleri.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Koplovitz, G., McClintock, J.B., Amsler, C.D. et al. A comprehensive evaluation of the potential chemical defenses of antarctic ascidians against sympatric fouling microorganisms. Mar Biol 158, 2661–2671 (2011). https://doi.org/10.1007/s00227-011-1764-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-011-1764-x

Keywords

Navigation