Skip to main content

Who Produces Ianthelline? The Arctic Sponge Stryphnus fortis or its Sponge Epibiont Hexadella dedritifera: a Probable Case of Sponge-Sponge Contamination

Journal of Chemical Ecology volume 42, pages 339–347 (2016)Cite this article

Abstract

The bromotyrosine derivative ianthelline was isolated recently from the Atlantic boreo-arctic deep-sea sponge Stryphnus fortis, and shown to have clear antitumor and antifouling effects. However, chemosystematics, field observations, and targeted metabolic analyses (using UPLC-MS) suggest that ianthelline is not produced by S. fortis but by Hexadella dedritifera, a sponge that commonly grows on S. fortis. This case highlights the importance of combining taxonomic and ecological knowledge to the field of sponge natural products research.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Albrizio S, Ciminiello P, Fattorusso E, Magno S, Pansini M (1994) Chemistry of Verongida sponges. I constituents of the Caribbean sponge Pseudoceratina crassa Tetrahedron 50:783–788

  • Alcolado PM (1984) Nuevas especies de esponjas encontradas en Cuba. Poeyana, 271, 1–22

  • Assmann M, Wray V, van Soest Rob WM, Proksch P (1998) A new bromotyrosine alkaloid from the Caribbean sponge Aiolochroia crassa. Zeitschrift für Naturforschung C 53:398

    CAS  Google Scholar 

  • Cárdenas P. (2010). Phylogeny, taxonomy and evolution of the astrophorida (Porifera, Demospongiae) [PhD thesis, available at http://hdl.handle.net/1956/4020]. Bergen: University of Bergen. 290 p.

  • Cárdenas P, Rapp HT (2015) Demosponges from the northern mid-Atlantic Ridge shed more light on the diversity and biogeography of North Atlantic deep-sea sponges. J Mar Biol Assoc UK 95:1475–1516

    Article  Google Scholar 

  • Cárdenas P, Rapp HT, Klitgaard AB, Best M, Thollesson M, Tendal OS (2013) Taxonomy, biogeography and DNA barcodes of Geodia species (Porifera, Demospongiae, Tetractinellida) in the Atlantic boreo-arctic region. Zool J Linnean Soc 169:251–311

    Article  Google Scholar 

  • Cárdenas P, Xavier J, Tendal OS, Schander C, Rapp HT (2007) Redescription and resurrection of Pachymatisma normani (Demospongiae, Geodiidae), with remarks on the genus Pachymatisma. J Mar Biol Assoc UK 87:1511–1525

    Article  Google Scholar 

  • Cárdenas P, Xavier JR, Reveillaud J, Schander C, Rapp HT (2011) Molecular phylogeny of the Astrophorida (Porifera, Demospongiae) reveals an unexpected high level of spicule homoplasy. PLoS One 6:e18318

    Article  PubMed  PubMed Central  Google Scholar 

  • Cárdenas P Rapp HT (2012) A review of Norwegian streptaster-bearing Astrophorida (Porifera: Demospongiae: Tetractinellida), new records and a new species. Zootaxa, 3253, 1–53

  • Carter HJ (1876) Descriptions and Figures of Deep-Sea Sponges and their Spicules, from the Atlantic Ocean, dredged up on board H.M.S.‘Porcupine’, chiefly in 1869 (concluded). Annals and Magazine of Natural History, 4, (105): 226-240; (106): 307-324; (107):388–410; (108):458–479, pls XII-XVI

  • Ciminiello P, Fattorusso E, Magno S, Pansini M (1995) Chemistry of Verongida sponges, IV comparison of the secondary metabolite composition of several specimens of Pseudoceratina crassa. J Nat Prod 58:689–696

    CAS  Article  Google Scholar 

  • Erpenbeck D, van Soest RM (2007) Status and perspective of sponge chemosystematics. Mar Biotechnol 9:2–19

    CAS  Article  PubMed  Google Scholar 

  • Erpenbeck D, van Soest RWM (2005) A survey for biochemical synapomorphies to reveal phylogenetic relationships of halichondrid demosponges (Metazoa: Porifera). Biochem Syst Ecol 33:585–616

    CAS  Article  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3:294–299

    CAS  PubMed  Google Scholar 

  • Gao H, Kelly M, Hamann MT (1999) Bromotyrosine-derived metabolites from the sponge Aiolochroia crassa. Tetrahedron 55:9717–9726

    CAS  Article  Google Scholar 

  • Gotsbacher M, Karuso P (2015) New antimicrobial bromotyrosine analogues from the sponge Pseudoceratina purpurea and its predator Tylodina corticalis. Marine Drugs 13:1389–1409

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Hanssen KØ, Andersen JH, S T, RA E, Svenson J, A-M G, Hansen E (2012) Antitumoral and mechanistic studies of ianthelline isolated from the Arctic sponge Stryphnus fortis. Anticancer Res 32:4287–4297

    CAS  PubMed  Google Scholar 

  • Hanssen KØ, Cervin G, Trepos R, Petitbois J, Haug T, Hansen E, Andersen JH, Pavia H, Hellio C, Svenson J (2014) The bromotyrosine derivative ianthelline isolated from the Arctic marine sponge Stryphnus fortis inhibits marine micro- and Macrobiofouling. Mar Biotechnol 16:684–694

    CAS  Article  PubMed  Google Scholar 

  • Hansen GA (1885) Spongiadae. The Norwegian North-Atlantic Expedition 1876-1878. Zoologi, 13:1–26, pls I-VII, 21 map

  • Hentschel E (1929) Die Kiesel- und Hornschwämme des Nördlichen Eismeers. In: F. Römer, F. Schaudinn, A. Brauer & W. Arndt (ed), Fauna Arctica. Eine Zusammenstellung der arktischen Tierformen mitbesonderer Berücksichtigung des Spitzbergen-Gebietes auf Grund der Ergebnisse der Deutschen Expedition in das Nördliche Eismeer im Jahre 1898. G. Fischer, Jena, pp. 857–1042, pls XII-XIV

  • Hyatt A (1875) Revision of the North American Poriferae; with Remarks upon Foreign Species. Part I. Memoirs of the Boston Society of Natural History, 2:399–408, pl. XIII

  • Kelly SR, Garo E, Jensen PR, Fenical W, Pawlik JR (2005) Effects of Caribbean sponge secondary metabolites on bacterial surface colonization. Aquat Microb Ecol 40:191–203

    Article  Google Scholar 

  • Lira NS, Montes RC, Tavares JF, MSd S, EVLd C, PFd A-F, LC R, CdS D, JM B-F (2011) Brominated compounds from marine sponges of the genus Aplysina and a compilation of their 13C NMR spectral data. Marine Drugs 9:2316–2368

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Litaudon M, Guyot M (1986) Ianthelline, un nouveau dérivé de la dibromo-3,5 tyrosine, isolé de l'éponge Ianthella ardis (Bahamas). Tetrahedron Lett 27:4455–4456

    CAS  Article  Google Scholar 

  • Makarieva TN, Stonik VA, Alcolado P, Elyakov YB (1981) Comparative study of the halogenated tyrosine derivatives from Demospongiae (Porifera). Compar Biochem Physiol Part B: Compar Biochem 68:481–484

    Article  Google Scholar 

  • Matsunaga S, Kobayashi H, van Soest RWM, Fusetani N (2005) Novel bromotyrosine derivatives that inhibit growth of the fish pathogenic bacterium Aeromonas hydrophila, from a marine sponge Hexadella sp.1. J Org Chem 70:1893–1896

    CAS  Article  PubMed  Google Scholar 

  • Morris SA, Andersen RJ (1989) Nitrogenous metabolites from the deep water sponge Hexadella sp. Can J Chem 67:677–681

    CAS  Article  Google Scholar 

  • Morrow C, Cárdenas P (2015) Proposal for a revised classification of the Demospongiae (Porifera). Front Zool 12:1–27

    Article  Google Scholar 

  • Peng J, Li J, Hamann MT. 2005. The marine bromotyrosine derivatives. In: Cordell GA, editor. The alkaloids: Chemistry and biology: Academic Press. p 59–262.

  • Redmond NE, Morrow CC, Thacker RW, Diaz MC, Boury-Esnault N, Cárdenas P, Hajdu E, Lôbo-Hajdu G, Picton BE, Pomponi SA and others. 2013. Phylogeny and systematics of Demospongiae in light of new small subunit ribosomal DNA (18S) sequences. Integr Comp Biol 53:388–415.

  • Reveillaud J, Allewaert C, Pérez T, Vacelet J, Banaigs B, Vanreusel A (2012) Relevance of an integrative approach for taxonomic revision in sponge taxa: case study of the shallow-water Atlanto-Mediterranean Hexadella species (Porifera: Ianthellidae: Verongida). Invert System 26:230–248

    Article  Google Scholar 

  • Reveillaud J, Maignien L, Eren AM, Huber JA, Apprill A, Sogin ML, Vanreusel A (2014) Host-specificity among abundant and rare taxa in the sponge microbiome. ISME J 8:1198–1209

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Reveillaud J, Remerie T, van Soest RWM, Erpenbeck D, Cárdenas P, Derycke S, Xavier J, Rigaux A, Vanreusel A (2010) Species boundaries and phylogenetic relationships between Atlanto-Mediterranean shallow-water and deep-sea coral associated Hexadella species (Porifera, Ianthellidae). Mol Phylogenet Evol 56:104–114

    Article  PubMed  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  • Schulze FE (1878) Untersuchungen über den Bau und die Entwicklung der Spongien. Vierte Mittheilung. Die Familie der Aplysinidae. Zeitschrift für wissenschaftliche Zoologie, 30:379–420, pls. XXI-XXIV

  • Siiri AO. 2011. Biological and chemical characterization of ianthelline isolated from a marine sponge, http://munin.uit.no/handle/10037/5216 [Master Thesis]: University of Tromsø. 80 p.

  • Sollas WJ (1880) The sponge-fauna of Norway; a Report on the Rev. A.M. Norman’s Collection of Sponges from the Norwegian Coast. Annals and Magazine of Natural History, 5:130–144, pls VI-VII; 241-259, pls X-XII

  • Topsent E (1913) Spongiaires provenant des campagnes scientifiques de la ‘Princesse Alice’ dans les Mers du Nord (1898-1899 - 1906-1907). Résultats des campagnes scientifiques accomplies par le Prince Albert I. Monaco, 45:1–67, pls I-V

  • Trepos R, Cervin G, Hellio C, Pavia H, Stensen W, Stensvåg K, Svendsen J-S, Haug T, Svenson J (2014) Antifouling compounds from the sub-Arctic ascidian Synoicum pulmonaria: Synoxazolidinones a and C, Pulmonarins a and B, and synthetic analogues. J Nat Prod 77:2105–2113

    CAS  Article  PubMed  Google Scholar 

  • van Soest RWM, Braekman JC (1999) Chemosystematics of Porifera: a review. Memoirs of the Queensland Museum 44:569–589

    Google Scholar 

  • Varmedal I. 2009. Bioactive molecules extracted from the marine sponge Aplysilla sulfurea and the marine phytoplankton Porosira glacialis, http://munin.uit.no/handle/10037/3561 [Master Thesis]: University of Tromsø. 64 p.

  • Vosmaer GCJ (1885) The Sponges of the ‘Willem Barents’ Expedition 1880 and 1881. Bijdragen tot de Dierkunde, 12:1–47, pls I-V

  • Zea S, Henkel TP, Pawlik JR. 2014. The sponge guide: A picture guide to Caribbean sponges. 3rd Edition. Available online at http://www.spongeguide.org. Accessed on: 2015–09-01.

Download references

Acknowledgments

I am grateful to Prof. Ulf Göransson (Uppsala University, Div. of Pharmacognosy) for providing the secondary metabolites extraction protocol and for commenting on an earlier version of this manuscript. I warmly thank Dr. Mikael Thollesson (Uppsala University, Div. of Systematic Biology) for collecting and sharing his Bahamian Aplysinidae samples for this study. Johan Svenson and Kine Østnes Hanssen (UiT The Arctic University of Norway, Tromsø) are acknowledged for providing an ianthelline extract. Alfred Svan and Erik Jacobsson (both at Uppsala University, Dept. of Medicinal Chemistry) are thanked for their help with the LC-MS2 experiments. I also thank Alexander Plotkin (University of Bergen, Norway) for collecting S. fortis and S. normani in Svalbard (AB321 Marine Benthic Fauna of Svalbard on board the RV Helmer Hanssen), and Dr. Christine Morrow (Queen’s University, Belfast) for collecting S. fortis during the CE13008 campaign (June 2013, RV Celtic Explorer using the ROV Holland I, chief scientist: Louise Allcock). I acknowledge the staff involved in the NEREIDA Project for providing the Flemish Cap specimens obtained during the NEREIDA surveys carried out on board the Spanish RV Miguel Oliver. Finally, I am grateful to the anonymous reviewers and the editor for their helpful comments and suggestions, which greatly improved this study. This study was funded by the European Union’s Seventh Framework Programme (FP7) under grant agreement No. 311848 (Bluegenics KBBE-2012-6).

Author information

Authors and Affiliations

  1. Department of Medicinal Chemistry, Division of Pharmacognosy, BioMedical Centre, Uppsala University, Husargatan 3, 751 23, Uppsala, Sweden

    Paco Cárdenas

Authors
  1. Paco Cárdenas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Paco Cárdenas.

Ethics declarations

Conflict of Interest

The author declares no conflict of interest.

Electronic supplementary material

Online Resource 1

LC-MS2 experiments to compare m/z, retention time (Rt) and fragment ions of an authentic ianthelline from Hanssen et al. (2012) and a putative ianthelline extracted from Stelletta normani (ZMBN 89728). (DOCX 124 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Cárdenas, P. Who Produces Ianthelline? The Arctic Sponge Stryphnus fortis or its Sponge Epibiont Hexadella dedritifera: a Probable Case of Sponge-Sponge Contamination. J Chem Ecol 42, 339–347 (2016). https://doi.org/10.1007/s10886-016-0693-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10886-016-0693-z

Keywords

  • Porifera
  • Bromotyrosine
  • Ianthelline
  • Verongiida
  • Tetractinellida
  • Aiolochroia
  • Chemosystematics