DOI QR코드

DOI QR Code

Cryptic species diversity of ochtodenes-producing Portieria species (Gigartinales, Rhodophyta) from the northwest Pacific

  • Received : 2018.04.16
  • Accepted : 2018.07.30
  • Published : 2018.09.15

Abstract

Red algae in the genus Portieria produce secondary halogenated monoterpenes, which are effective deterrents against herbivores, as secondary metabolites. Portieria hornemannii samples from various sites contain different concentrations of these metabolites, suggesting the existence of genetic diversity and cryptic species. To evaluate the genetic diversity and species distribution of Portieria in the northwest Pacific, we analyzed rbcL sequences of samples collected from Korea, Japan, and Taiwan. The phylogenetic analysis revealed five distinct lineages at the species level. One was recognized as Portieria japonica and the others were cryptic lineages in P. hornemannii. The rbcL haplotypes of P. japonica were genetically fragmented into two subgroups of geographic origin; Korean and Japanese. The four cryptic lineages within P. hornemannii were also geographically structured at a much finer scale. These results suggest that different genetic lineages in Portieria evolved from variable microhabitats, consequently influencing secondary metabolites. Further study is required to resolve the relationships between genetic and secondary metabolite variations in Portieria.

Keywords

References

  1. Athukorala, Y., Lee, K. -W., Kim, S. -K. & Jeon, Y. -J. 2006. Anticoagulant activity of marine green and brown algae collected from Jeju Island in Korea. Bioresour. Technol. 98:1711-1716.
  2. Clement, M., Posada, D. & Crandall, K. A. 2000. TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9:1657-1659. https://doi.org/10.1046/j.1365-294x.2000.01020.x
  3. Excoffier, L., Laval, G. & Schneider, S. 2005. Arlequin (version 3.0): an integrated software package for population genetics data analysis. Evol. Bioinform. Online 1:47-50.
  4. Fatima, M. R., Dinesh, S., Mekata, T., Itami, T. & Sudhakaran, R. 2016. Therapeutic efficiency of Portieria hornemannii (Rhodophyta) against Vibrio parahaemolyticus in experimentally infected Oreochromis mossambius. Aquaculture 450:369-374. https://doi.org/10.1016/j.aquaculture.2015.08.010
  5. Faulkner, D. J. 2001. Marine natural products. Nat. Prod. Rep. 18:1R-49R. https://doi.org/10.1039/b006897g
  6. Fernando, I. P. S., Sanjeewa, K. K. A., Samarakoon, K. W., Lee, W. W., Kim, H. -S., Kim, E. -A., Gunasekara, U. K. D. S. S., Abeytunga, D. T. U., Nanayakkara, C., de Silva, E. D., Lee, H. -S. & Jeon, Y. -J. 2017. FTIR characterization and antioxidant activity of water soluble crude polysaccharides of Sri Lankan marine algae. Algae 32:75-86. https://doi.org/10.4490/algae.2017.32.12.1
  7. Freshwater, D. W. & Rueness, J. 1994. Phylogenetic relationships of some European Gelidium (Gelidiales, Rhodophyta) species based upon rbcL nucleotide sequence analysis. Phycologia 33:187-194. https://doi.org/10.2216/i0031-8884-33-3-187.1
  8. Fuller, R. W., Cardellina, J. H. 2nd, Jurek, J., Scheuer, P. J., Alvarado-Lindner, B., McGuire, M., Gray, G. N., Steiner, J. R., Clardy, J., Menez, E., Shoemaker, R. H., Newman, D. J., Snader, K. M. & Boyd, M. R. 1994. Isolation and structure/activity features of halomon-related antitumor monoterpenes from the red alga Portieria hornemannii. J. Med. Chem. 37:4407-4411. https://doi.org/10.1021/jm00051a019
  9. Fuller, R. W., Cardellina, J. H., Kato, Y., Brinen, L. S., Clardy, J., Snader, K. M. & Boyd, M. R. 1992. A pentahalogenated monoterpene from the red alga Portieria hornemannii produces a novel cytotoxicity profile against a diverse panel of human tumor cell lines. J. Med. Chem. 35:3007-3011. https://doi.org/10.1021/jm00094a012
  10. Guiry, M. D. & Guiry, G. M. 2018. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Available from: http://www.algaebase.org. Accessed Apr 5, 2018.
  11. Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95-98.
  12. Harvey, W. H. 1860. Characters of new algae, chiefly from Japan and adjacent regions, collected by Charles Wright in the North Pacific Exploring Expedition under Captain James Rodgers. Proc. Am. Acad. Arts Sci. 4:327-335.
  13. Hu, Z. -M., Li, J. -J., Sun, Z. -M., Oak, J. -H., Zhang, J., Fresia, P., Grant, W. S. & Duan, D. -L. 2015. Phylogeographic structure and deep lineage diversification of the red alga Chondrus ocellatus Holmes in the Northwest Pacific. Mol. Ecol. 24:5020-5033. https://doi.org/10.1111/mec.13367
  14. Hu, Z. -M., Uwai, S., Yu, S. -H., Komatsu, T., Ajisaka, T. & Duan, D. -L. 2011. Phylogeographic heterogeneity of the brown macroalga Sargassum horneri (Fucaceae) in the northwestern Pacific in relation to late Pleistocene glaciation and tectonic configurations. Mol. Ecol. 20:3894-3909. https://doi.org/10.1111/j.1365-294X.2011.05220.x
  15. Kang, J. W. 1966. On the geographical distribution of marine algae in Korea. Bull. Pusan Fish. Coll. 7:1-125.
  16. Kim, K. M., Hoarau, G. G. & Boo, S. M. 2012. Genetic structure and distribution of Gelidium elegans (Gelidiales, Rhodophyta) in Korea based on mitochondrial cox1 sequence data. Aquat. Bot. 98:27-33. https://doi.org/10.1016/j.aquabot.2011.12.005
  17. Kim, M. S., Kim, S. Y. & Nelson, W. 2010. Symphyocladia lithophila sp. nov. (Rhodomelaceae, Ceramiales), a new Korean red algal species based on morphology and rbcL sequences. Bot. Mar. 53:233-241.
  18. Knowlton, N. 1993. Sibling species in the sea. Annu. Rev. Ecol. Syst. 24:189-216. https://doi.org/10.1146/annurev.es.24.110193.001201
  19. Lee, H. W., Yang, M. Y. & Kim, M. S. 2016. Verifying a new distribution of the genus Amalthea (Halymeniales, Rhodophyta) with description of A. rubida sp. nov. from Korea. Algae 31:341-349. https://doi.org/10.4490/algae.2016.31.12.8
  20. Lee, K. M., Yang, E. C., Coyer, J. A., Zuccarello, G. C., Wang, W. -L., Choi, C. G. & Boo, S. M. 2012. Phylogeography of the seaweed Ishige okamurae (Phaeophyceae): evidence for glacial refugia in the northwest Pacific region. Mar. Biol. 159:1021-1028. https://doi.org/10.1007/s00227-012-1882-0
  21. Lee, Y. P. 2008. Marine algae of Jeju. Academy Publishing Co., Seoul, 477 pp.
  22. Lee, Y. P. & Kang, S. Y. 2002. A catalogue of the seaweeds in Korea. Jeju National University Press, Jeju, 662 pp..
  23. 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. 33:196-208. https://doi.org/10.1111/j.0022-3646.1997.00196.x
  24. Matlock, D. B., Ginsburg, D. W. & Paul, V. J. 1999. Spatial variability in secondary metabolite production by the tropical red alga Portieria hornemannii. Hydrobiologia 398/399:263-273. https://doi.org/10.1023/A:1017003522096
  25. Mendoza-Gonzalez, A. C., Senties, A., Mateo-Cid, L. E., Diaz-Larrea, J., Pedroche, F. F. & Villanueva, R. A. 2011. Ochtodes searlesii sp. nov. (Gigartinales, Rhodophyta), from the Pacific tropical coast of Mexico, based on morphological and molecular evidence. Phycol. Res. 59:250-258. https://doi.org/10.1111/j.1440-1835.2011.00623.x
  26. Noda, T. 2009. Metacommunity-level coexistence mechanisms in rocky intertidal sessile assemblages based on a new empirical synthesis. Popul. Ecol. 51:41-55. https://doi.org/10.1007/s10144-008-0117-1
  27. Oh, J. -Y., Fernando, I. P. S. & Jeon, Y. -J. 2016. Potential applications of radioprotective phytochemicals from marine algae. Algae 31:403-414. https://doi.org/10.4490/algae.2016.31.12.1
  28. Okamura, K. 1922. Icones of Japanese algae. Vol. IV. Tokyo, pp. 151-184, CLXXXVI-CXCV.
  29. Okamura, K. 1936. Nippon kaiso shi [Descriptions of Japanese algae]. Tokyo, pp. [4], [1]-964, [1]-11, frontispiece portrait, 1-427 figs.
  30. Oliveira, A. S., Sudatti, D. B., Fujii, M. T., Rodrigues, S. V. & Pereira, R. C. 2013. Inter- and intrapopulation variation in the defensive chemistry of the red seaweed Laurencia dendroidea (Ceramiales, Rhodophyta). Phycologia 52:130-136. https://doi.org/10.2216/12-058.1
  31. Park, H. -J., Lee, M. -S., Shim, H. S., Lee, G. -R., Chung, S. Y., Kang, Y. M., Lee, B. -J., Seo, Y. B., Kim, K. S. & Shim, I. 2016. Fermented Saccharina japonica (Phaeophyta) improves neuritogenic activity and TMT-induced cognitive deficits in rats. Algae 31:73-84. https://doi.org/10.4490/algae.2016.31.11.10
  32. Paul, V. J., Meyer, K. D., Nelson, S. G. & Sanger, H. R. 1992. Deterrent effects of seaweed extracts and secondary metabolites on feeding by the rabbitfish Siganus spinus. Proc. 7th Int. Coral Reef Symp. 2:867-874.
  33. Paul, V. J., Nelson, S. G. & Sanger, H. R. 1990. Feeding preference of adult and juvenile rabbitfish Siganus argenteus in relation to chemical defenses of tropical seaweeds. Mar. Ecol. Prog. Ser. 60:23-34. https://doi.org/10.3354/meps060023
  34. Payo, D. A., Calumpong, H. & De Clerck, O. 2011. Morphology, vegetative and reproductive development of the red alga Portieria hornemannii (Gigartinales: Rhizophyllidaceae). Aquat. Bot. 95:94-102. https://doi.org/10.1016/j.aquabot.2011.03.011
  35. Payo, D. A., Leliaert, F., Verbruggen, H., D'hondt, S., Calumpong, H. P. & De Clerck, O. 2013. Extensive cryptic species diversity and fine-scale endemism in the marine red alga Portieria in the Philippines. Proc. Biol. Sci. 280:20122660. https://doi.org/10.1098/rspb.2012.2660
  36. Puglisi, M. P. & Paul, V. J. 1997. Intraspecific variation in the red alga Portieria hornemannii: monoterpene concentrations are not influenced by nitrogen or phosphorus enrichment. Mar. Biol. 128:161-170. https://doi.org/10.1007/s002270050079
  37. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M. A. & Huelsenbeck, J. P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61:539-542. https://doi.org/10.1093/sysbio/sys029
  38. Silva, P. C., Menez, E. G. & Moe, R. L. 1987. Catalog of the benthic marine algae of the Philippines. Smithson. Contrib. Mar. Sci. 27:1-179. https://doi.org/10.5479/si.1943667X.27.1
  39. Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihoodbased phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. https://doi.org/10.1093/bioinformatics/btl446
  40. Tronholm, A., Sanson, M., Afonso-Carrillo, J., Verbruggen, H. & De Clerk, O. 2010. Niche partitioning and the coexistence of two cryptic Dictyota (Dictyotales, Phaeophyceae) species from the Canary Islands. J. Phycol. 46:1075-1087. https://doi.org/10.1111/j.1529-8817.2010.00912.x
  41. Vairappan, C. S., Zanil, I. I. & Kamada, T. 2014. 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. J. Appl. Phycol. 26:1189-1198. https://doi.org/10.1007/s10811-013-0161-x
  42. Wellenreuther, M., Barrett, P. T. & Clements, K. D. 2007. Ecological diversification in habitat use by subtidal triplefin fishes (Tripterygiidae). Mar. Ecol. Prog. Ser. 330:235-246. https://doi.org/10.3354/meps330235
  43. Yang, M. Y. & Kim, M. S. 2016. Molecular phylogeny of the genus Chondracanthus (Rhodophyta), focusing on the resurrection of C. okamurae and the description of C. cincinnus sp. nov. Ocean. Sci. J. 51:517-529. https://doi.org/10.1007/s12601-016-0046-4
  44. Yang, M. Y. & Kim, M. S. 2018. DNA barcoding of the funoranproducing red algal genus Gloiopeltis (Gigartinales) and description of a new species, Gloiopeltis frutex sp. nov. J. Appl. Phycol. 30:1381-1392. https://doi.org/10.1007/s10811-017-1330-0
  45. Yoshida, T. 1998. Marine algae of Japan. Uchida Rokakuho Publishing Co., Ltd., Tokyo, 1222 pp.
  46. Zuccarello, G. C. & West, J. A. 2003. Multiple cryptic species: molecular diversity and reproductive isolation in the Bostrychia radicans/B. moritziana complex (Rhodomelaceae, Rhodophyta) with focus on North American isolates. J. Phycol. 39:948-959. https://doi.org/10.1046/j.1529-8817.2003.02171.x
  47. Zuccarello, G. C., Yeates, P. H., Wright, J. T. & Bartlett, J. 2001. Population structure and physiological differentiation of haplotypes of Caloglossa leprieurii (Rhodophyta) in a mangrove intertidal zone. J. Phycol. 37:235-244. https://doi.org/10.1046/j.1529-8817.2001.037002235.x

Cited by

  1. Fissidens eremicus (Fissidentaceae), a new pseudocryptic African-European species with dimorphic stems vol.43, pp.3, 2018, https://doi.org/10.1080/03736687.2021.1910435
  2. Hidden Diversity in an Antarctic Algal Forest: Metabolomic Profiling Linked to Patterns of Genetic Diversification in the Antarctic Red Alga Plocamium sp. vol.19, pp.11, 2018, https://doi.org/10.3390/md19110607