Journal of Applied Phycology

, Volume 26, Issue 2, pp 1189–1198 | Cite as

Structural diversity and geographical distribution of halogenated secondary metabolites in red algae, Laurencia nangii Masuda (Rhodomelaceae, Ceramiales), in the coastal waters of North Borneo Island

  • Charles S. VairappanEmail author
  • Intan Irna Zanil
  • Takashi Kamada


The red algae genus Laurencia (Rhodomelaceae, Ceramiales) is known as a prolific producer of halogenated secondary metabolites with a high level of species diversity and geographical distribution. In North Borneo Island, Malaysia, there are four main Laurencia species: Laurencia snackeyi, Laurencia majuscula, Laurencia similis and L. nangii. Although the chemistry of Laurencia is well studied, the diversity of compounds in L. nangii has not been thoroughly investigated. Therefore, we studied the chemical constituents of seven populations of L. nangii from Tunku Abdul Rahman Marine Park (two populations), Dinawan Island (one population), Tun Mustapha Marine Park (two populations) and Tun Sakaran Marine Park (two populations). Halogenated compounds were isolated and the structures determined via spectroscopic methods. A total of 20 metabolites belonging to the classes of sesquiterpenes, acetylenes, bromoallenes, diterpenes and triterpenes were identified. Populations from Tunku Abdul Rahman Marine Park and Dinawan Island contained non-chamigrane-type sesquiterpenes, acetylenes and diterpenes. Populations from Tun Mustapha Marine Park contained chamigrane-type sesquiterpenes, acetylenes and diterpenes. However, the chemical compositions of populations from Tun Sakaran Marine Park were found to differ significantly, containing chamigrane-type and non-chamigrane-type sesquiterpenes, bromoallenes and triterpenes. This investigation has revealed the presence of interesting chemotaxonomical markers in populations of L. nangii and the existence of chemical races in this species.


Red algae Laurencia nangii North Borneo Island Halogenated metabolites Chemotaxonomical markers Chemical race 



The authors would like to thank the International Foundation for Science (IFS) and Organization for the Prohibition of Chemical Weapons (OCPW) for research grant IFS 4836/2 and Sabah Parks for the research permit and assistance during sample collection.


  1. Abe T, Masuda M (1998) Laurencia japonensis sp. nov. (Ceramiales, Rhodophyta). Eur J Phycol 33:17–24CrossRefGoogle Scholar
  2. Dias DA, Urban S (2011) Phytochemical studies of the southern Australian marine alga, Laurencia elata. Phytochemistry 72:2081–2089PubMedCrossRefGoogle Scholar
  3. de Oliveira LS, Gregoracci GB, Silva GGZ, Salgado LT, Filho GA, Alves-Ferreira M, Pereira RC, Thompson FL (2012) Transcriptomic analysis of the red seaweed Laurencia dendroidea (Florideophyceae, Rhodophyta) and its microbiome. BMC Genomics 13:487–499PubMedCentralPubMedCrossRefGoogle Scholar
  4. Erickson KL (1983) Constituents of Laurencia. In: Scheuer PJ (ed) Marine natural products: chemical and biological perspectives, vol. V. Academic, New York, pp 131–257CrossRefGoogle Scholar
  5. Findlay JA, Li G (2002) Novel terpenoids from the sea hare Aplysia punctata. Can J Chem 80:1697–1707CrossRefGoogle Scholar
  6. González AG, Martin JD, Martin VS, Norte M, Pérez R, Ruano JZ, Drexler SA, Clardy J (1982) Non-terpenoid C-15 metabolites from the red seaweed Laurencia pinnatifida. Tetrahedron 38:1009–1014CrossRefGoogle Scholar
  7. Howard BM, Fenical W (1976) α- and β-Snyderol; new bromo-monocyclic sesquiterpenes from the seaweed Laurencia. Tetrahedron Lett 17:41–44CrossRefGoogle Scholar
  8. Howard BM, Fenical W, Donovan SF, Clardy J (1982) Neoirione, a diterpenoid of a new skeletal class from the red marine alga Laurencia CF irieii. Tetrahedron Lett 23:3847–3850CrossRefGoogle Scholar
  9. Ireland C, Stallard MO, Faulkner DJ, Finer J, Clardy J (1976) Some chemical constituents of the digestive gland of the sea hare Aplysia californica. J Org Chem 41:2461–2465PubMedCrossRefGoogle Scholar
  10. Ji NY, Li XM, Cui CM, Wang BG (2007a) Two new brominated diterpenes from Laurencia decumbens. Chinese Chem Lett 18:957–959CrossRefGoogle Scholar
  11. Ji NY, Li XM, Li K, Ding LP, Gloer JB, Wang BG (2007b) Diterpenes, sesquiterpenes and a C15-acetogenin from the marine red alga Laurencia mariannensis. J Nat Prod 70:1901–1905PubMedCrossRefGoogle Scholar
  12. Kamada T, Vairappan CS (2012) A new bromoallene-producing chemical type of the red alga Laurencia nangii Masuda. Molecules 17:2119–2125PubMedCrossRefGoogle Scholar
  13. Manzo E, Ciavatta ML, Gavanin M, Puliti R, Mollo E, Guo YW, Mattia CA, Mazzarella L, Cimino G (2005) Structure and absolute stereochemistry of novel C15-halogenated acetogenins from the anaspidean mollusc Aplysia dactylomela. Tetrahedron 61:7456–7469CrossRefGoogle Scholar
  14. Masuda M (1997) A taxonomic study of the genus Laurencia (Ceramiales, Rhodophyta) from Vietnam. IV. Laurencia nangii sp. nov. Cryptogamie Algol 18:309–318Google Scholar
  15. Masuda M, Abe T, Kogame K, Kawaguchi S, Phang SM, Daitoh M, Sakai T, Takahashi Y, Suzuki M (2002) Taxonomic notes on marine algae from Malaysia. VIII. Three species of Laurencia (Rhodophyceae). Bot Mar 45:571–579CrossRefGoogle Scholar
  16. Masuda M, Abe T, Suzuki T, Suzuki M (1996) Morphological and chemotaxonomic studies on Laurencia composita and L. okamurae (Ceramiales, Rhodophyta). Phycologia 35:550–562CrossRefGoogle Scholar
  17. Masuda M, Abe T, Sato S, Suzuki T, Suzuki M (1997) Diversity of halogenated secondary metabolites in the red alga Laurencia nipponica (Rhodomelaceae, Ceramiales). J Phycol 33:196–208CrossRefGoogle Scholar
  18. Masuda M, Kogame K, Arisawa S, Suzuki M (1998) Morphology and halogenated secondary metabolites of three Gran Canarian species of Laurencia (Ceramiales, Rhodophyta). Bot Mar 41:265–277Google Scholar
  19. Norte M, Fernández JJ, Cataldo F, González AG (1989) E-dihydrorhodophytin, a C15 acetogenin from the red alga Laurencia pinnatifida. Phytochemistry 28:647–649CrossRefGoogle Scholar
  20. Pettit GR, Herald CL, Einck JJ, Vanell LD, Brown P, Gust D (1978) Isolation and structure of angasiol. J Org Chem 43:4685–4686CrossRefGoogle Scholar
  21. Rhoades DF (1979) Evolution of plant chemical defense against herbivores. In: Rosenthal GA, Janzen DH (ed) Herbivores: their interaction with secondary plant metabolites. Academic, New York, pp 3–54Google Scholar
  22. Schmitz FJ, McDonald FJ, Vanderah DJ (1978) Marine natural products: sesquiterpene alcohols and ethers from the sea hare Aplysia dactylomela. J Org Chem 43:4220–4225CrossRefGoogle Scholar
  23. Sudatti DB, Fujii MT, Rodrigues SV, Turra A, Pereira RC (2011) Effects of abiotic factors on growth and chemical defenses in cultivated clones of Laurencia dendroidea J. Agardh (Ceramiales, Rhodophyta). Mar Biol 158:1439–1446CrossRefGoogle Scholar
  24. Suzuki M, Furusaki A, Kurosawa E (1979) The absolute configurations of halogenated chamigrene derivatives from the marine alga, Laurencia glandulifera Kützing. Tetrahedron 35:823–831CrossRefGoogle Scholar
  25. Suzuki M, Kurosawa E, Furusaki A, Katsuragi S, Matsumoto T (1984) Neolaurallene, a new halogenated C-15 nonterpenoid from the red alga Laurencia okamurai Yamada. Chem Lett 13:1033–1034CrossRefGoogle Scholar
  26. Suzuki M, Matsuo Y, Takeda S, Suzuki T (1993) Intricatetraol, a halogenated triterpene alcohol from the red alga Laurencia intricata. Phytochemistry 33:651–656CrossRefGoogle Scholar
  27. Suzuki M, Takahashi Y, Matsuo Y, Masuda M (1996) Pannosallene, a brominated C15 nonterpenoid from Laurencia pannosa. Phytochemistry 41:1101–1103CrossRefGoogle Scholar
  28. Suzuki M, Takahashi Y, Mitome Y, Itoh T, Abe T, Masuda M (2002) Brominated metabolites from an Okinawan Laurencia intricata. Phytochemistry 60:861–867PubMedCrossRefGoogle Scholar
  29. Suzuki M, Takahashi Y, Nakano S, Abe T, Masuda M, Ohnishi T, Noya Y, Seki K (2009) An experimental approach to study the biosynthesis o brominated metabolites by the red algal genus Laurencia. Phytochemistry 70:1410–1415PubMedCrossRefGoogle Scholar
  30. Suzuki M, Vairappan CS (2005) Halogenated secondary metabolites from Japanese species of the red algal genus Laurencia (Rhodomelaceae, Ceramiales). Curr Topics Phytochem 5:1–38CrossRefGoogle Scholar
  31. Takahashi Y, Daitoh M, Suzuki M, Abe T, Masuda M (2002) Halogenated metabolites from the new Okinawan red alga Laurencia yonaguniensis. J Nat Prod 65:395–398PubMedCrossRefGoogle Scholar
  32. Vairappan CS (2003) Potent antibacterial activity of halogenated metabolites from Malaysian red algae, Laurencia majuscula (Rhodomelaceae, Ceramiales). Biomol Eng 20:255–259PubMedCrossRefGoogle Scholar
  33. Vairappan CS, Ishii T, Tan KL, Suzuki M, Zhan Z (2010) Antibacterial activities of halogenated secondary metabolites from Bornean Laurencia spp. Mar Drugs 8:1743–1749PubMedCentralPubMedCrossRefGoogle Scholar
  34. Vairappan CS, Kamada T, Lee WW, Jeon YJ (2013) Anti-inflammatory activity of halogenated secondary metabolites of Laurencia snackeyi (Weber-van Bosse) Masuda in LPS-stimulated RAW264.7 macrophages. J Appl Phycol. doi: 10.1007/s10811-013-0023-6 Google Scholar
  35. Vairappan CS, Tan KL (2009) C-15 halogenated acetogenin with antibacterial activity against food pathogens. Malays J Sci 28:263–268Google Scholar
  36. Young DN, Howard BM, Fenical W (1980) Subcellular location of brominated secondary metabolites in red alga Laurencia snyderae. J Phycol 16:182–185CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Charles S. Vairappan
    • 1
    Email author
  • Intan Irna Zanil
    • 1
  • Takashi Kamada
    • 1
  1. 1.Laboratory of Natural Products Chemistry, Institute for Tropical Biology and ConservationUniversiti Malaysia SabahKota KinabaluMalaysia

Personalised recommendations