Skip to main content

Advertisement

Log in

Diversity of fungi isolated from three temperate ascidians

  • Short Communication
  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

Ascidians are known to harbor diverse and host-specific bacterial and archaeal communities in their tunic. However, to date, only one ascidian species has been investigated to assess symbiotic relationships with fungi and the extent of their diversity. In this study, we isolated and identified 37 strains of fungi in association with three common ascidian species in the NW Mediterranean Sea: Cystodytes dellechiajei, Didemnum fulgens, and Pycnoclavella communis, and 15 additional strains from concentrated seawater samples collected around the animals. Most of the isolated fungi were classified within four orders: Eurotiales (predominantly Penicillium spp.), Pleosporales, Hypocreales (predominantly Trichoderma spp.), and Capnodiales (Cladosporium spp.). Three additional fungal isolates from C. dellechiajei and D. fulgens belonged to the orders Helotiales, Phylachorales and Microascales, and matched to well-known plant and human pathogens (Botrytis cinerea, Plectosphaerella cucumerina and Scopulariopsis brevicaulis). Host-specificity of ascidian-associated fungi was not apparent and thus the significance of ascidian-fungal associations for ascidian wellbeing and their possible ecological roles remain unknown.

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

References

  • Ainsworth TD, Thurber RV, Gates RD (2010) The future of coral reefs: a microbial perspective. Trends Ecol Evol 25:233–240

    Article  PubMed  Google Scholar 

  • Ainsworth TD, Krause L, Bridge T, Torda G, Raina J-B, Zakrzewski M, Gates RD, Padilla-Gamino JL, Spalding HL, Smith C, Woolsey ES, Bourne DG, Bongaerts P, Hoegh-Guldberg O, Leggat W (2015) The coral core microbiome identifies rare bacterial taxa as ubiquitous endosymbionts. ISME J in press

  • Alker AP, Smith GW, Kim K (2001) Characterization of Aspergillus sydowii (Thom et Church), a fungal pathogen of Caribbean sea fan corals. Hydrobiologia 460:105–111

    Article  Google Scholar 

  • Amend AS, Barshis DJ, Oliver TA (2012) Coral-associated marine fungi form novel lineages and heterogenous assemblages. ISME J 6:1291–1301

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Appleton DR, Copp BR (2003) Kottamide E, the first example of a natural product bearing the amino acid 4-amino-1, 2-dithiolane-4-carboxylic acid (Adt). Tetrahedron Lett 44:8963–8965

    Article  CAS  Google Scholar 

  • Appleton DR, Page MJ, Lambert G, Berridge MV, Copp BR (2002) Kottamides A–D: novel bioactive imidazolone-containing alkaloids from the New Zea- land ascidian Pycnoclavella kottae. J Org Chem 67:5402–5404

    Article  CAS  PubMed  Google Scholar 

  • Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR (2014) Marine natural products. Nat Prod Rep 31:160–258

    Article  CAS  PubMed  Google Scholar 

  • Blunt JW, Copp BR, Keyzers RA, Munro MHG, Prinsep MR (2015) Marine natural products. Nat Prod Rep 32:116–211

    Article  CAS  PubMed  Google Scholar 

  • Bontemps N, Bry D, López-Legentil S, Simon-Levert A, Long C, Banaigs B (2010) Structures and antimicrobial activities of pyridoacridine alkaloids isolated from different chromotypes of the ascidian Cystodytes dellechiajei. J Nat Prod 73:1044–1048

    Article  CAS  PubMed  Google Scholar 

  • Bourne DG, Garren M, Work TM, Rosenberg E, Smith GW, Harvell CD (2009) Microbial disease and the coral holobiont. Trends Microbiol 17:554–562

    Article  CAS  PubMed  Google Scholar 

  • Bry D, Banaigs B, Long C, Bontemps N (2011) New pyridoacridine alkaloids from the purple morph of the ascidian Cystodytes dellechiajei. Tetrahedron Lett 52:3041–3044

    Article  CAS  Google Scholar 

  • Carlucci A, Raimondo ML, Santos JC, Phillips AJL (2012) Plectosphaerella species associated with root and collar rots of horticultural crops in southern Italy. Persoonia 28:34–48

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Carman MR, Morris JA, Karney RC, Grunden DW (2010) An initial assessment of native and invasive tunicates in shellfish aquaculture of the North American east coast. J Appl Ichthyol 26:8–11

    Article  Google Scholar 

  • Carr G, Tay W, Bottriell H, Andersen SK, Mauk AG, Andersen RJ (2009) Plectosphaeroic acids A, B, and C, Indoleamine 2,3-Dioxygenase inhibitors produced in culture by a marine isolate of the fungus Plectosphaerella cucumerina. Org Lett 11:2996–2999

    Article  CAS  PubMed  Google Scholar 

  • Cuenca-Estrella M, Gomez-Lopez A, Mellado E, Buitrago MJ, Monzón A, Rodriguez-Tudela JL (2003) Scopulariopsis brevicaulis, a fungal pathogen resistant to broad-spectrum antifungal agents. Antimicrob Agents Chemother 47:2339–2341

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Dhar J, Carey PB (1993) Scopulariopsis brevicaulis skin lesions in an AIDS patient. AIDS 7:1283–1284

    Article  CAS  PubMed  Google Scholar 

  • Easson CG, Thacker RW (2014) Phylogenetic signal in the community structure of host-specific microbiomes of tropical marine sponges. Front Microbiol 5:Article 532

    Article  PubMed  Google Scholar 

  • Ein-Gil N, Ilan M, Carmeli S, Smith GW, Pawlik JR, Yarden O (2009) Presence of Aspergillus sydowii, a pathogen of gorgonian sea fans in the marine sponge Spongia obscura. ISME J 3:752–755

    Article  PubMed  Google Scholar 

  • Elad Y, Williamson B, Tudzynski P, Delen N (2007) Botrytis spp. and diseases they cause in agricultural systems—an Introduction. In: Elad Y, Williamson B, Tudzynski P, Delen N (eds) Botrytis: biology, pathology and control. Springer, The Netherlands

    Chapter  Google Scholar 

  • Erwin PM, López-Legentil S, Schuhmann PW (2010) The pharmaceutical value of marine biodiversity for anti-cancer drug discovery. Ecol Econ 70:445–451

    Article  Google Scholar 

  • Erwin PM, Pita L, López-Legentil S, Turon X (2012) Stability of sponge-associated bacteria over large seasonal shifts in temperature and irradiance. Appl Environ Microbiol 78:7358–7360

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Erwin PM, Pineda MC, Webster N, Turon X, López-Legentil S (2013) Small core communities and high variability in bacteria associated with the introduced ascidian Styela plicata. Symbiosis 59:35–46

    Article  Google Scholar 

  • Erwin PM, Pineda MC, Webster NS, Turon X, López-Legentil S (2014) Down under the tunic: bacterial biodiversity hotspots and widespread ammonia-oxidizing archaea in coral reef ascidians. ISME J 8:575–588

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Article  Google Scholar 

  • Geiser DM, Taylor JW, Ritchie KB, Smith GW (1998) Cause of sea fan death in the West Indies. Nature 394:137–138

    Article  CAS  Google Scholar 

  • Höller U, Wright AD, Matthée GF, Konig GM, Draeger S, Aust H-J, Schulz B (2000) Fungi from marine sponges: diversity, biological activity and secondary metabolites. Mycol Res 104:1354–1365

    Article  Google Scholar 

  • Imhoff JF, Kajahn I, Lang G, Wiese J, Peters A (2010) Production and use of antimumoral, antibiotic and insecticidal cyclodepsipeptides. Patent WO 2010/142258

  • Jiao J-Y, Zhu T-J, Zhu W-M, Du L, Wang C-Y, Guan H-S, Gu QQ (2009) Isolation of sponge-associated fungi and screening of their antitumor activity. J Ocean Univ China 39:42–46

    Google Scholar 

  • Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Mentjies P, Drummond AJ (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649

    Article  PubMed Central  PubMed  Google Scholar 

  • Koch L, Lodin A, Herold I, Ilan M, Carmeli S, Yarden O (2014) Sensitivity of Neurospora crassa to a marine-derived Aspergillus tubingensis anhydride exhibiting antifungal activity that is mediated by the MAS1 protein. Marine Drugs 12:4713–4731

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lambert G (2001) A global overview of ascidian introductions and their possible impact on the endemic fauna. In: Sawada H, Tokosawa H, Lambert CC (eds) The biology of ascidians. Springer, Tokyo, Japan

    Google Scholar 

  • Lambert G (2005) Ecology and natural history of the protochordates. Can J Zool 83:34–50

    Article  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) ClustalW and ClustalX version 2. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Li Q, Wang G (2009) Diversity of fungal isolates from three Hawaiian marine sponges. Microbiol Res 164:233–241

    Article  CAS  PubMed  Google Scholar 

  • López-Legentil S, Turon X (2005) How do morphotypes and chemotypes relate to genotypes? The colonial ascidian Cystodytes (Polycitoridae). Zool Scr 34:3–14

    Article  Google Scholar 

  • López-Legentil S, Dieckmann R, Bontemps-Subielos N, Turon X, Banaigs B (2005) Qualitative variation of alkaloids in color morphs of Cystodytes (Ascidiacea). Biochem Syst Ecol 33:1107–1119

    Article  Google Scholar 

  • López-Legentil S, Bontemps-Subielos N, Turon X, Banaigs B (2006a) Temporal variation in the production of four secondary metabolites in a colonial ascidian. J Chem Ecol 32:2079–2084

    Article  PubMed  Google Scholar 

  • López-Legentil S, Turon X, Schupp P (2006b) Chemical and physical defenses against predators in Cystodytes (Ascidiacea). J Exp Mar Biol Ecol 332:27–36

    Article  Google Scholar 

  • López-Legentil S, Erwin PM, Velasco M, Turon X (2013) Growing or reproducing in a temperate sea: optimization of resource allocation in a colonial ascidian. Invertebr Biol 132:69–80

    Article  Google Scholar 

  • López-Legentil S, Turon X, Espluga R, Erwin PM (2015) Temporal stability of bacterial symbionts in a temperate ascidian. Front Microbiol. doi:10.3389/fmicb.2015.01022

  • Martínez-García M, Díaz-Valdés M, Ramos-Esplà A, Salvador N, Lopez P, Larriba E, Antón J (2007a) Cytotoxicity of the ascidian Cystodytes dellechiajei against tumor cells and study of the involvement of associated microbiota in the production of cytotoxic compounds. Marine Drugs 5:52–70

    Article  PubMed Central  PubMed  Google Scholar 

  • Martínez-García M, Díaz-Valdés M, Wanner G, Ramos-Esplà A, Antón J (2007b) Microbial community associated with the colonial ascidian Cystodytes dellechiajei. Environ Microbiol 9:521–534

    Article  PubMed  Google Scholar 

  • Martínez-García M, Koblízek M, López-Legentil S, Antón J (2011) Epibiosis of oxygenic phototrophs containing chlorophylls a, b, c, and d on the colonial ascidian Cystodytes dellechiajei. Microb Ecol 61:13–19

    Article  PubMed  Google Scholar 

  • Menezes CB, Bonugli-Santosa RC, Miquelettoa PB, Passarinia MR, Silvaa CH, Justoa MR, Leala RR, Fantinatti-Garbogginia F, Oliveiraa VM, Berlinckb RG, Sette LD (2010) Microbial diversity associated with algae, ascidians and sponges from the north coast of São Paulo state, Brazil. Microbiol Res 165:466–482

    Article  PubMed  Google Scholar 

  • Montenegro TGC, Rodrigues FAR, Jimenez PC, Angelim AL, Melo VMM, Rodrigues Filho E, de Oliveira MCF, Costa-Lotufo LV (2012) Cytotoxic activity of fungal strains isolated from the ascidian Eudistoma vannamei. Chem Biodivers 9:2203–2209

    Article  CAS  PubMed  Google Scholar 

  • Morrison-Gardiner S (2002) Dominant fungi from Australia coral reefs. Fungal Divers 9:105–121

    Google Scholar 

  • Mouchka ME, Hewson I, Harvell CD (2010) Coral-associated bacterial asemblages: current knowledge and the potential for climate-driven impacts. Integr Comp Biol 50:662–674

    Article  PubMed  Google Scholar 

  • Park MS, Fong JJ, Oh S-Y, Kwon KK, Sohn JH, Lim YW (2014) Marine-derived Penicillium in Korea: diversity, enzyme activity, and antifungal properties. Antonie Van Leeuwenhoek 106:331–345

    Article  CAS  PubMed  Google Scholar 

  • Paul VJ, Ritson-Williams R, Sharp K (2011) Marine chemical ecology in benthic environments. Nat Prod Rev 28:345–387

    Article  CAS  Google Scholar 

  • Paz Z, Komon-Zelazowska M, Druzhinina IS, Aveskamp MM, Shnaiderman A, Aluma Y, Carmeli S, Ilan M, Yarden O (2010) Diversity and potential antifungal properties of fungi associated with a Mediterranean sponge. Fungal Divers 42:17–26

    Article  Google Scholar 

  • Pérez-Portela R, Turon X (2007) Prey preferences of the polyclad flatworm Prostheceraeus roseus among Mediterranean species of the ascidian genus Pycnoclavella. Hydrobiologia 592:535–539

    Article  Google Scholar 

  • Pérez-Portela R, Duran S, Palacin C, Turon X (2007) The genus Pycnoclavella (Ascidiacea) in the Atlanto- Mediterranean region: a combined molecular and morphological approach. Invertebr Syst 21:187–205

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Rowan R (1998) Diversity and ecology of zooxanthellae on coral reefs. J Phycol 34:407–417

    Article  Google Scholar 

  • Schmitt S, Tsai P, Bell J, Fromont J, Ilan M, Lindquist N, Perez T, Rodrigo A, Schupp PJ, Vacelet J, Webster NS, Hentschel U, Taylor MW (2012) Assessing the complex sponge microbiota: core, variable and species-specific bacterial communities in marine sponges. ISME J 6:564–576

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shenkar N, Swalla BJ (2011) Global diversity of Ascidiacea. PLoS ONE 6:e20657

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sun H-H, Mao W-J, Jiao J-Y, Xu J-C, Li H-Y, Chen Y, Qi X-H, Chen Y-L, Xu J, Zhao C-Q, Hou Y-J, Yang Y-P (2011) Structural characterization of extracellular polysaccharides produced by the marine fungus Epicoccum nigrum JJY-40 and their antioxidant activities. Mar Biotechnol 13:1048–1055

    Article  CAS  PubMed  Google Scholar 

  • Suryanarayanan TS (2012) The diversity and importance of fungi associated with marine sponges. Bot Mar 55:553–564

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Tarjuelo I, López-Legentil S, Codina M, Turon X (2002) Defence mechanisms of adults and larvae of colonial ascidians: patterns of palatability and toxicity. Mar Ecol Prog Ser 235:103–115

    Article  Google Scholar 

  • Taylor MW, Schupp P, Dahllof I, Kjelleberg S, Steinberg PD (2004) Host specificity in marine sponge-associated bacteria, and potential implications for marine microbial diversity. Environ Microbiol 6:121–130

    Article  PubMed  Google Scholar 

  • Thacker RW, Freeman CJ (2012) Sponge-microbe symbioses: recent advances and new directions. Adv Mar Biol 62:57–111

    Article  PubMed  Google Scholar 

  • Tianero MDB, Kwan JC, Wyche TP, Presson AP, Koch M, Barrows LR, Bugni TS, Schmidt EW (2015) Species specificity of symbiosis and secondary metabolism in ascidians. ISME J 9:615–628

    Article  PubMed  Google Scholar 

  • Van Bressem M-F, Raga JA, Di Guardo G, Jepson PD, Duignan PJ, Siebert U, Barrett T, de Oliveira Santos MC, Moreno IB, Siciliano S, Aguilar A, Van Waerebeek K (2009) Emerging infectious diseases in cetaceans worldwide and the possible role of environmental stressors. Dis Aquat Org 86:143–157

    Article  PubMed  Google Scholar 

  • Webster NS (2007) Sponge disease: a global threat? Environ Microbiol 9:1363–1375

    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 

  • Wheat LJ, Bartlett M, Ciccarelli M, Smith JW (1984) Opportunistic Scopulariopsis pneumonia in an immunocompromised host. South Med J 77:1608–1609

    Article  CAS  PubMed  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Aplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR protocols: a guide to methods and applications. Academic, New York

    Google Scholar 

  • Wiese J, Ohlendorf B, Blümel M, Schmaljohann R, Imhoff J (2011) Phylogenetic identification of fungi isolated from the marine sponge Tethya aurantium and identification of their secondary metabolites. Marine Drugs 9:561–585

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Williamson B, Tudzynski B, Tudzynski P, Van Kan JA (2007) Botrytis cinerea: the cause of grey mould disease. Mol Plant Pathol 8:561–580

    Article  CAS  PubMed  Google Scholar 

  • Xin ZH, Tian L, Zhu TJ, Wang WL, Du L, Fang YC, Gu QQ, Zhu WM (2007) Isocoumarin derivatives from the sea squirt-derived fungus Penicillium stoloniferum QY2-10 and the halotolerant fungus Penicillium notatum B-52. Arch Pharm Res 30:816–819

    Article  CAS  PubMed  Google Scholar 

  • Yarden O (2014) Fungal association with sessile marine invertebrates. Front Microbiol 5:228

    Article  PubMed Central  PubMed  Google Scholar 

  • Yarden O, Ainsworth TD, Roff G, Leggat W, Fine M, Hoegh-Guldberg O (2007) Increased prevalence of ubiquitous ascomycetes in an acropoid coral (Acropora formosa) exhibiting symptoms of brown band syndrome and skeletal eroding band. Appl Environ Microbiol 73:2755–2757

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Yu ZG, Lang G, Kajahn I, Schmaljohann R, Imhoff JF (2008) Scopularides A and B, cyclodepsipeptides from a marine sponge-derived fungus, Scopulariopsis brevicaulis. J Nat Prod 71:1052–1054

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was funded by the Spanish Government project MARSYMBIOMICS CTM2013-43287-P, and the Catalan Government grant 2014SGR-336 for Consolidated Research Groups.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Susanna López-Legentil.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

López-Legentil, S., Erwin, P.M., Turon, M. et al. Diversity of fungi isolated from three temperate ascidians. Symbiosis 66, 99–106 (2015). https://doi.org/10.1007/s13199-015-0339-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-015-0339-x

Keywords

Navigation