ALGAE

The Korean Society of Phycology (한국조류학회(藻類))
권호 표지
DOI QR코드

DOI QR Code

Insight into the species identification and distribution of Grateloupiaceae (Halymeniales, Rhodophyta) having Grateloupia filicina-like morphology in the Northwest Pacific

  • Su Yeon Kim (Korea Inter-University Institute of Ocean Science, Pukyong National University) ;
  • Sung Min Boo (Department of Biology, Chungnam National University) ;
  • Hawn Su Yoon (Department of Biological Sciences, Sungkyunkwan University) ;
  • Myung Sook Kim (Department of Biology and Research Institute for Basic Sciences, Jeju National University)
  • Received : 2023.01.16
  • Accepted : 2023.03.14
  • Published : 2023.03.15
Download PDF
⟨ Previous Next ⟩

Abstract

Accurately identifying species is the basis of all biological studies. There has been much confusion in the identification of Grateloupiacean species, which have finely pinnate gross morphology similar to Grateloupia filicina (the type species of the family). The objective of this study was to comprehensively investigate species identification and distribution of G. filicina-like species in the Northwest Pacific, based on the rbcL sequences. A total of 118 specimens from 78 sites in Korea and Japan were collected from 2001 to 2021 and analyzed for their rbcL sequences. Additional 341 sequences downloaded from the GenBank were included in our comprehensive dataset. Based on these sequences, we documented the nomenclatural history and geographical distribution of the species, and commented on the application of species name. G. asiatica was the most abundant G. filicina-like species in the Northwest Pacific, and its high degree of morphological variation caused many misidentifications. In particular, G. dalianensis, G. serra, and G. variata require reconsideration of their conspecificity with G. asiatica using more specimens from China. By contrast, G. oligoclora was presumed to be a heterotypic synonym of G. subpectinata. The occurrence of G. acuminata, G. ramosissima, and G. livida in Korea resulted from misidentifications with other species.

Keywords

Acknowledgement

We thank Drs. Eun Chan Yang and Hyung Woo Lee for collecting precious algal samples and allowing their use for this study. This work was partly supported by the National Research Foundation of Korea (NRF), NRF-2022R1C1C2004043 to SYK and NRF-2020R1I1A2069706 to MSK.

References

  1. Ang, P. O. Jr., Leung, S. M. & Choi, M. M. 2014. A verification of reports of marine algal species from the Philippines. Philipp. J. Sci. 142:5-49. 
  2. Bolton, J. J., De Clerck, O., Francis, C. M., Siyanga-Tembo, F. & Anderson, R. J. 2016. Two newly discovered Grateloupia (Halymeniaceae, Rhodophyta) species on aquaculture rafts on the west coast of South Africa, including the widely introduced Grateloupia turuturu. Phycologia 55:659-664.  https://doi.org/10.2216/15-104.1
  3. Calderon, M. S., Boo, G. H. & Boo, S. M. 2014. Morphology and phylogeny of Ramirezia osornoensis gen. and sp. nov. and Phyllymenia acletoi sp. nov. (Halymeniales, Rhodophyta) from South America. Phycologia 53:23-36.  https://doi.org/10.2216/13-158.1
  4. Cao, C. C., Li, Y. Z. & Wang, H. W. 2016. Morphological observation, life history and rbcL gene sequence analysis of a new species, Grateloupia variata sp. nov. (Halymeniaceae, Rhodophyta) from Qingdao, China. Mar. Biol. Res. 12:443-453.  https://doi.org/10.1080/17451000.2015.1104416
  5. Chellamanimegalai, P., Pavan-Kumar, A., Balange, A. K., Dwivedi, A. & Deshmukhe, G. 2020. New record of marine red algal species Grateloupia orientalis Showe M. Lin & H. Y. Liang and G. catenata Yendo (Halymeniaceae, Rhodophyta) from the east coast of India. Curr. Sci. 119:849-854.  https://doi.org/10.18520/cs/v119/i5/849-854
  6. Dawson, E. Y. 1958. A new gigartinoid Grateloupia (red alga) from Hawaii. Pac. Nat. 1:3-5. 
  7. De Clerck, O., Gavio, B., Fredericq, S., Barbara, I. & Coppejans, E. 2005. Systematics of Grateloupia filicina (Halymeniaceae, Rhodophyta), based on rbcL sequence analyses and morphological evidence, including the reinstatement of G. minima and the description of G. capensis sp. nov. J. Phycol. 41:391-410.  https://doi.org/10.1111/j.1529-8817.2005.04189.x
  8. Duan, X., Bian, Y., Wang, H. & Wang, H. 2022. Grateloupia oligoclora (Halymeniaceae, Rhodophyta): a new species from China based on morphological observation, life history and rbcL gene sequence analysis. Mar. Biol. Res. 17:994-1004.  https://doi.org/10.1080/17451000.2022.2046279
  9. Faye, E. J., Wang, H. W., Kawaguchi, S., Shimada, S. & Masuda, M. 2004. Reinstatement of Grateloupia subpectinata (Rhodophyta, Halymeniaceae) based on morphology and rbcL sequences. Phycol. Res. 52:59-67.  https://doi.org/10.1111/j.1440-1835.2004.tb00316.x
  10. Freshwater, D. W. & Rueness, J. 1994. Phylogenetic relationships of some European Gelidium (Gelidiales, Rhodophyta) species based on rbcL nucleotide sequence analysis. Phycologia 33:187-194.  https://doi.org/10.2216/i0031-8884-33-3-187.1
  11. Gargiulo, G. M., Morabito, M. & Manghisi, A. 2013. A re-assessment of reproductive anatomy and postfertilization development in the systematics of Grateloupia (Halymeniales, Rhodophyta). Cryptogam. Algol. 34:3-35.  https://doi.org/10.7872/crya.v34.iss1.2013.3
  12. Gavio, B. & Fredericq, S. 2002. Grateloupia turuturu (Halymeniaceae, Rhodophyta) is the correct name of the non-native species in the Atlantic known as Grateloupia doryphora. Eur. J. Phycol. 37:349-359.  https://doi.org/10.1017/S0967026202003839
  13. Guiry, M. D. & Guiry, G. M. 2022. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway. Available from: http://www.algaebase.org. Accessed Oct 1, 2022. 
  14. Iima, M., Kinoshita, T., Kawaguchi, S. & Migita, S. 1995. Cultivation of Grateloupia acuminata (Halymeniaceae, Rhodophyta) by regeneration from cut fragments of basal crust and upright thalli. J. Appl. Phycol. 7:583-588.  https://doi.org/10.1007/BF00003946
  15. Jung, S. -M., Park, J. S., Shim, H. J., Kwon, Y. S., Kim, H. G. & Shin, H. S. 2016. Antioxidative effect of phycoerythrin derived from Grateloupia filicina on rat primary astrocytes. Biotechnol. Bioprocess. Eng. 21:676-682.  https://doi.org/10.1007/s12257-016-0369-0
  16. Kawaguchi, S. 1991. Taxonomic notes on the Halymeniaceae (Rhodophyta) from Japan. I. Halymenia acuminata (Holmes) J. Agardh. Jpn. J. Phycol. 39:329-336. 
  17. Kawaguchi, S., Wang, H. W., Horiguchi, T., Sartoni, G. & Masuda, M. 2001. A comparative study of the red alga Grateloupia filicina (Halymeniaceae) from the northwestern Pacific and Mediterranean with the description of Grateloupia asiatica sp. nov. J. Phycol. 37:433-442.  https://doi.org/10.1046/j.1529-8817.2001.037003433.x
  18. 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., Meintjes, P. & Drummond, A. 2012. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647-1649.  https://doi.org/10.1093/bioinformatics/bts199
  19. Kim, H. G. & Park, J. G. 2006. Tissue culture of Grateloupia acuminata (Rhodophyta) from the eastern coast of Korea. J. Aquac. 19:216-221. 
  20. Kim, M. -K. & Kim, K. -T. 2000. Studies on the seaweeds in the islands of Ullungdo and Dokdo: I. Decrease of algal species compositions and changes of marine algal flora. Algae 15:119-124. 
  21. 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.  https://doi.org/10.1515/BOT.2010.031
  22. Kim, S. Y., Han, E. G., Kim, M. S., Park, J. K. & Boo, S. M. 2013. Grateloupia jejuensis (Halymeniales, Rhodophyta): a new species previously confused with G. elata and G. cornea in Korea. Algae 28:233-240.  https://doi.org/10.4490/algae.2013.28.3.233
  23. Kim, S. Y., Lee, H. W., Yang, E. C., Boo, S. M., Lopez-Bautista, J., Fredericq, S., D'Archino, R., Yoon, H. S. & Kim, M. S. 2021. Resurrection of the family Grateloupiaceae Emend. (Halymeniales, Rhodophyta) based on a multigene phylogeny and comparative reproductive morphology. Front. Ecol. Evol. 9:775627. 
  24. Kim, S. Y., Manghisi, A., Morabito, M., Yang, E. C., Yoon, H. S., Miller, K. A. & Boo, S. M. 2014. Genetic diversity and haplotype distribution of Pachymeniopsis gargiuli sp. nov. and P. lanceolata (Halymeniales, Rhodophyta) in Korea, with notes on their non-native distributions. J. Phycol. 50:885-896.  https://doi.org/10.1111/jpy.12218
  25. Lee, H. B. 1987. A systematic study of Halymeniaceae (Rhodophyta, Cryptonemiales) in Korea. Ph.D. dissertation, Seoul National University, Seoul, Korea, 390 
  26. Lee, H. W. & Kim, M. S. 2019. Female reproductive structures define the novel genus, Nesoia (Halymeniaceae, Rhodophyta). Eur. J. Phycol. 54:66-77.  https://doi.org/10.1080/09670262.2018.1513166
  27. Lee, I. K. & Kang, J. W. 1986. A check list of marine algae in Korea. Korean J. Phycol. 1: 311-325. 
  28. Lee, J. I., Kim, H. G., Geraldino, P. J. L., Hwang, I. K. & Boo, S. M. 2009. Molecular classification of the genus Grateloupia (Halymeniaceae, Rhodophyta) in Korea. Algae 24:231-238.  https://doi.org/10.4490/ALGAE.2009.24.4.231
  29. Li, F., Jiang, P., Zhao, S. & Wang, H. W. 2016. Research on the revision of Grateloupia fastigiata Li et Ding (Rhodophyta, Halymeniaceae) based on morphological observations and rbcL sequence analyses. Acta Hydrobiol. Sin. 40:1249-1256. 
  30. Lin, S. -M., Liang, H. -Y. & Hommersand, M. H. 2008. Two types of auxiliary cell ampullae in Grateloupia (Halymeniaceae, Rhodophyta), including G. taiwanensis sp. nov. and G. orientalis sp. nov. from Taiwan based on rbcL gene sequence analysis and cystocarp development. J. Phycol. 44:196-214.  https://doi.org/10.1111/j.1529-8817.2007.00443.x
  31. Liu, F., Tian, Y. -L. & Wang, H. -W. 2017. Research on the revision of Grateloupia didymecladia Li et Ding based on morphological observations and molecular analyses. Acta Hydrobiol. Sin. 41:1273-1281. 
  32. Liu, H., Chen, X., Song, L., Li, K., Zhang, X., Liu, S., Qin, Y. & Li, P. 2019. Polysaccharides from Grateloupia filicina enhance tolerance of rice seeds (Oryza sativa L.) under salt stress. Int. J. Biol. Macromol. 124:1197-1204.  https://doi.org/10.1016/j.ijbiomac.2018.11.270
  33. Liu, J., Li, J., Bian, Y., Ding, Y., Wang, H. & Wang, H. 2020. The morphological, developmental and molecular landscape of Grateloupia qingdaoensis Li et Ding. J. Appl. Phycol. 32:2093-2103.  https://doi.org/10.1007/s10811-020-02046-y
  34. Lou, Y., Yi, P., Song, X. W. & Wang, H. W. 2019. Grateloupia serra sp. nov. H. W. Wang & Y. Lou (Halymeniaceae, Rhodophyta): a new species previously confused with Grateloupia asiatica in China. Mar. Biol. Res. 15:1-12.  https://doi.org/10.1080/17451000.2019.1593461
  35. Mateo-Cid, L. E., Mendoza-Gonzalez, A. C., Gavio, B. & Fredericq, S. 2005. Grateloupia huertana sp. nov. (Halymeniaceae, Rhodophyta), a peculiar new prostrate species from tropical Pacific Mexico. Phycologia 44:4-16.  https://doi.org/10.2216/0031-8884(2005)44[4:GHSNHR]2.0.CO;2
  36. Nam, K. W. & Kang, P. J. 2013. Algal flora of Korea. Vol. 4, No. 9. Marine red algae. Rhodophyta: Florideophyceae: Halymeniales: Halymeniaceae, Tsengiaceae. National Institute of Biological Resources, Incheon, pp. 21-22. 
  37. Nelson, W. A., Kim, S. Y., D'Archino, R. & Boo, S. M. 2013. The first record of Grateloupia subpectinata from the New Zealand region and comparison with G. prolifera, a species endemic to the Chatham Islands. Bot. Mar. 56:507-513.  https://doi.org/10.1515/bot-2013-0059
  38. Nguyen, T. V., Le, N. H., Lin, S. -M., Steen, F. & De Clerck, O. 2013. Checklist of the marine macroalgae of Vietnam. Bot. Mar. 56:207-227.  https://doi.org/10.1515/bot-2013-0010
  39. Okamura, K. 1936. Descriptions of Japanese algae. Uchidarokakuho, Tokyo, 964
  40. Peng, C., Ding, H., Tang, Z., Guo, L. & Yang, G. 2018. Molecular grouping of Grateloupia tissues collected along Chinese coast and microsatellite diversity analysis of G. asiatica. J. Ocean. Univ. China 17:925-931.  https://doi.org/10.1007/s11802-018-3496-8
  41. Rodriguez-Prieto, C., De Clerck, O., Guiry, M. D. & Lin, S. -M. 2022. Revisiting the systematics of the genera Grateloupia, Phyllymenia, and Prionitis (Halymeniaceae, Rhodophyta) with a description of a new species: Prionitis taiwani-borealis. J. Phycol. 58:234-250.  https://doi.org/10.1111/jpy.13226
  42. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Daring, A., Hohna, S., Larget, B., Liu, L., Suchard, M. A. & Huelsenbeck, J. P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice a cross a large model space. Syst. Biol. 61:539-542.  https://doi.org/10.1093/sysbio/sys029
  43. Sheng, Y. -W., Zhang, W., Zhao, D. & Wang, H. -W. 2012. A morphological and molecular assessment of the genus Sinotubimorpha (Halymeniaceae, Rhodophyta). J. Syst. Evol. 50:146-152.  https://doi.org/10.1111/j.1759-6831.2011.00174.x
  44. Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690.  https://doi.org/10.1093/bioinformatics/btl446
  45. Sumikawa, K., Takei, K., Kumagai, Y., Shimizu, T., Yasui, H. & Kishimura, H. 2020. In silico analysis of ACE inhibitory peptides from chloroplast proteins of red alga Grateloupia asiatica. Mar. Biotechnol. 22:391-402.  https://doi.org/10.1007/s10126-020-09959-2
  46. Sun, Y., Chen, X., Cheng, Z., Liu, S., Yu, H., Wang, X. & Li, P. 2017. Degradation of polysaccharides from Grateloupia filicina and their antiviral activity to avian leucosis virus subgroup J. Mar. Drugs 15:345. 
  47. Verlaque, M., Brannock, P. M., Komatsu, T., Villalard-Bohnsack, M. & Marston, M. 2005. The genus Grateloupia C. Agardh (Halymeniaceae, Rhodophyta) in the Thau Lagoon (France, Mediterranean): a case study of marine plurispecific introductions. Phycologia 44:477-496.  https://doi.org/10.2216/0031-8884(2005)44[477:TGGCAH]2.0.CO;2
  48. Wang, H., Guo, S., Zhang, X., Zhao, D., Zhang, W. & Luan, R. 2014. Re-identifying Grateloupia yangjiangensis (Rhodophyta, Halymeniaceae) based on morphological observations, life history and rbcL sequence analyses. Acta Hydrobiol. Sin. 33:77-84. 
  49. Wang, H. W., Guan, Y., Zhao, F. Q. & Zhao, D. 2015. Grateloupia huanghaiensis sp. nov. (Halymeniaceae, Rhodophyta), a peculiar new species from China. Mar. Biol. Res. 11:396-404.  https://doi.org/10.1080/17451000.2014.932913
  50. Wang, H. W., Kawaguchi, S., Horiguchi, T. & Masuda, M. 2000. Reinstatement of Grateloupia catenata (Rhodophyta, Halymeniaceae) on the basis of morphology and rbcL sequences. Phycologia 39:228-237.  https://doi.org/10.2216/i0031-8884-39-3-228.1
  51. Wang, H. W., Kawaguchi, S., Horiguchi, T. & Masuda, M. 2001. A morphological and molecular assessment of the genus Prionitis J. Agardh (Halymeniaceae, Rhodophyta). Phycol. Res. 49:251-261.  https://doi.org/10.1111/j.1440-1835.2001.tb00255.x
  52. Wolf, M. A., Sfriso, A. & Moro, I. 2014. Thermal pollution and settlement of new tropical alien species: the case of Grateloupia yinggehaiensis (Rhodophyta) in the Venice lagoon. Estuar. Coast. Shelf Sci. 147:11-16.  https://doi.org/10.1016/j.ecss.2014.05.020
  53. Xia, B. 2004. Flora algarum marinarum sinicarum Tomus II Rhodophyta No. III Gelidiales Cryptonemiales Hildenbrandiales. Science Press, Beijing, 203 pp. 
  54. Yang, E. C., Boo, S. M., Bhattacharya, D., Saunders, G. W., Knoll, A. H., Fredericq, S., Graf, L. & Yoon, H. S. 2016. Divergence time estimates and the evolution of major lineages in the florideophyte red algae. Sci. Rep. 6:21361. 
  55. Yang, M. Y. & Kim, M. S. 2015. Taxonomy of Grateloupia (Halymeniales, Rhodophyta) by DNA barcode marker analysis and a description of Pachymeniopsis volvita sp. nov. J. Appl. Phycol. 27:1373-1384.  https://doi.org/10.1007/s10811-014-0432-1
  56. Yang, M. Y., Kim, S. Y. & Kim, M. S. 2021. Verification of hotspots of genetic diversity in Korean population of Grateloupia asiatica and G. jejuensis (Rhodophyta) show low genetic diversity and similar geographic distribution. Genes Genomics 43:1463-1469.  https://doi.org/10.1007/s13258-021-01168-y
  57. Zhang, J., Tang, X., Chen, W. Z., Liu, T. & Li, Y. 2018. The complete plastid genome of Grateloupia filicina (Rhodophyta) and phylogenetic analysis. Mitochondrial DNA B Resour. 3:1172-1173.  https://doi.org/10.1080/23802359.2018.1524279
  58. Zhao, D., Wang, H., Sheng, Y., Lu, J. & Luan, R. 2012. Morphological observation and rbcL gene sequences studies of two new species, Grateloupia dalianensis H. W. Wang et D. Zhao, sp. nov. and G. yinggehaiensis, H. W. Wang et R. X. Luan, sp. nov. Halymeniaceae, Rhodophyta) from China. Acta Oceanol. Sin. 31:109-120.