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Biologia

, Volume 74, Issue 6, pp 599–607 | Cite as

Genetic diversity of Philippine Gracilaria salicornia (Gracilariaceae, Rhodophyta) based on mitochondrial COI-5P sequences

  • Ma. Salvacion R. Ferrer
  • Rosalie N. Gomez
  • Christi B. Nacido
  • Minerva T. Moises
  • Richard V. DumilagEmail author
Original Article
  • 51 Downloads

Abstract

Gracilaria salicornia is an agar-producing marine rhodophyte endemically distributed across into the Indo-Pacific region. Despite previous study that examined patterns of genetic diversity of this species from the Southeast Asian region, samples representing conspecific populations from the Philippines are few. In this study, we performed phylogenetic and haplotype network analyses comprising 95 isolates of G. salicornia from the Philippines using the mitochondrial 5′ end of the cytochrome c oxidase subunit I (COI-5P) gene sequences. Contrary to what was previously known, our results showed that the Philippine populations of G. salicornia are genetically heterogenous. In addition to eight haplotypes previously recognized for G. salicornia, eight novel haplotypes were detected from the Philippines, which collectively represented by three distinct genetic lineages. The degree of variation in COI-5P sequences, however, did not allow recognition between the two G. salicornia morphotypes (i.e., “G. salicornia” type and “G. crassa” type). In general, this study emphasized the significance of wide-scale sampling in order to estimate the extent of distribution and level of heterogeneity among the populations of G. salicornia in the Philippines.

Keywords

Agarophyte COI-5P Genetic diversity Gracilaria salicornia Haplotype 

Notes

Acknowledgments

This study was funded by the National Fisheries Research and Development Institute (NFRDI) under the Department of Agriculture (DA) and the Bureau of Fisheries and Aquatic Resources (BFAR). We are grateful for the support given to us by the NFRDI Management, the BFAR Regional Offices, the concerned Local Government Units (LGUs) and the fisher folks/seaweed gatherers. We would also like to give credit to Carlos C. Jacela Jr. and Josefino S. Mondragon for their substantial contribution in this study and to other NFRDI researchers who shared their equipment and facilities during laboratory work. Special thanks to Dr. Arturo O. Lluisma of The Marine Science Institute, University of the Philippines, Diliman (UP-MSI) for his guidance and valuable comments and suggestions every time he was consulted about this study.

Compliance with ethical standards

Ethical approval

All sampling in this study was conducted in accordance with the Philippine Republic Act No. 9147. (Wildlife Resources Conservation and Protection Act).

Conflict of interest

No potential conflict of interest was reported by the authors.

References

  1. Agardh CA (1820) Icones algarum ineditae. Fasc. 1. Lundae (Lund]) [4] pp., pls. I–XGoogle Scholar
  2. Almeida CLF, Falcão HS, Lima GRM, Montenegro CA, Lira NS, Athayde-Filho PF, Rodrigues LC, Souza MFV, Barbosa-Filho JM, Batista LM (2011) Bioactivities from marine algae of the genus Gracilaria. Int J Mol Sci 12:4550–4573CrossRefGoogle Scholar
  3. Armisen R (1995) World-wide use and importance of Gracilaria. J Appl Phycol 7:231–243CrossRefGoogle Scholar
  4. Ballard WO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744CrossRefGoogle Scholar
  5. Bezerra AF, Marinho-Soriano E (2010) Cultivation of the red seaweed Gracilaria birdiae (Gracilariales, Rhodophyta) in tropical waters of Northeast Brazil. Biomass Bioenergy 34:1813–1817CrossRefGoogle Scholar
  6. Bird CJ (1995) A review of recent taxonomic concepts and developments in the Gracilariaceae (Rhodophyta). J Appl Phycol 7:255–267CrossRefGoogle Scholar
  7. Bird CJ, McLachlan J (1982) Some underutilized taxonomic criteria in Gracilaria (Rhodophyta, Gigartinales). Bot Mar 25:557–562CrossRefGoogle Scholar
  8. Buschmann AH, Correa JA, Westermeier R, Hernández-González MC, Norambuena R (2001) Red algal farming in Chile: a review. Aquaculture 194:203–220CrossRefGoogle Scholar
  9. Calumpong HP, Maypa A, Magbanua M, Suarez P (1999) Biomass and agar assessment of three species of Gracilaria from Negros Island, Central Philippines. Hydrobiologia 398(399):173–182CrossRefGoogle Scholar
  10. Campbell MA, Presting G, Bennett MS, Sherwood AR (2014) Highly conserved organellar genomes in the Gracilariales as inferred using new data from the Hawaiian invasive alga Gracilaria salicornia (Rhodophyta). Phycologia 53:109–116CrossRefGoogle Scholar
  11. Chan SW, Cheang CC, Chirapart A, Gerung G, Tharith C, Ang P (2013) Homogeneous population of the brown alga Sargassum polycystum in Southeast Asia: possible role of recent expansion and asexual propagation. PLoS One 8:e77662CrossRefGoogle Scholar
  12. Chan SW, Cheang CC, Yeung CW, Chirapart A, Gerung G, Ang P (2014) Recent expansion led to the lack of genetic structure of Sargassum aquifolium populations in Southeast Asia. Mar Biol 161:785–795Google Scholar
  13. Chung K, Soo S, Teo S, Phang S (2011) Analysis of native and alkali-treated agar from species of Gracilaria (Gracilariaceae, Rhodophyta) collected from Morib, Malaysia. Malaysian J Sci 30:83–91CrossRefGoogle Scholar
  14. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1669CrossRefGoogle Scholar
  15. Costa ES, Plastino EM, Petti R, Oliveira EC, Oliveira MC (2012) The Gracilariaceae germplasm Bank of the University of Sao Paulo, Brazil – a DNA barcoding approach. J Appl Phycol 24:1643–1653CrossRefGoogle Scholar
  16. Dawson EY (1954) Notes on tropical Pacific marine algae. Bull Soc Calif Acad Sci 53:1–7Google Scholar
  17. Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376CrossRefGoogle Scholar
  18. Fredericq S, Hommersand MH (1990) Diagnoses and key to the genera of the Gracilariaceae (Gracilariales, Rhodophyta). Hydrobiologia 204/205:173–178CrossRefGoogle Scholar
  19. Fukunaga A, Peyton KA, Thomas FIM (2014) Epifaunal community structure and ammonium uptake compared for the invasive algae, Gracilaria salicornia and Acanthophora specifera, and the native alga, Padina thivyi. J Exp Mar Biol Ecol 456:78–86CrossRefGoogle Scholar
  20. Gurgel CFD, Fredericq S (2004) Systematics of the Gracilariaceae (Gracilariales, Rhodophyta): a critical assessment based on rbcL sequence analyses. J Phycol 40:138–159CrossRefGoogle Scholar
  21. Gurgel CF, Terada R, Abbott IA, Fredericq S, Norris JN (2006) Towards a global phylogeography of Gracilaria salicornia (Gracilariaceae, Rhodophyta), an invasive species in Hawaii, based on chloroplast and mitochondrial markers. J Phycol 42(s1):13CrossRefGoogle Scholar
  22. Hashim MA, Chu KH (2004) Biosorption of cadmium by brown, green and red seaweed. Chem Eng J 97:249–255CrossRefGoogle Scholar
  23. Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc Royal Society B Biol Sci 270:313–322CrossRefGoogle Scholar
  24. Higgins D, Thompson J, Gibson T, Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680CrossRefGoogle Scholar
  25. Huynh QN Nguyen HD (1998) the seaweed resources of Vietnam. In: (AT Critchley, M Ohno, DB largo, RD Gillespie) seaweeds resources of the world. Japan International Cooperation Agency. Yokosuka, Japan, pp 62–69Google Scholar
  26. Iyer R, Tronchin EM, Bolton JJ, Coyne VE (2005) Molecular systematics of the Gracilariaceae (Gracilariales, Rhodophyta) with emphasis on southern Africa. J Phycol 41:672–684CrossRefGoogle Scholar
  27. Kazɫowski B, Chiu Y, Kazɫowska K, Pan C, Wu C (2012) Prevention of Japanese encephalitis virus infections by low-degree-polymerisation sulfated saccharides from Gracilaria sp. and Monostroma nitidum. Food Chem 133:866–874CrossRefGoogle Scholar
  28. Kim MS, Yang MY, Cho GY (2010a) Applying DNA barcoding to Korean Gracilariaceae (Rhodophyta). Cryptogam Algol 31:387–401Google Scholar
  29. Kim SY, Weinberger F, Boo SB (2010b) Genetic data hint at a common donor region for invasive Atlantic and Pacific populations for Gracilaria vermiculophylla (Gracilariales, Rhodophyta). J Phycol 46:1346–1349CrossRefGoogle Scholar
  30. Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefGoogle Scholar
  31. Lewmanomont K (1998) The seaweeds resources of Thailand. In: (AT Critchley, M Ohno, DB largo, RD Gillespie) seaweeds resources of the world. Japan International Cooperation Agency. Yokosuka, Japan, pp 70–78Google Scholar
  32. Liao LM, Hommersand MH (2003) A morphological study and taxonomic assessment of the generitype species in the Gracilariaceae. J Phycol 39:1207–1232CrossRefGoogle Scholar
  33. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452CrossRefGoogle Scholar
  34. Lim P, Thong K, Phang S (2001) Molecular differentiation of two morphological variants of Gracilaria salicornia. J Appl Phycol 13:335–342CrossRefGoogle Scholar
  35. Lyra GM, Costa ES, De Jesus PB, De Matos JCG, Caires TA, Oliveira MC, Oliveira EC, Xi Z, Nunes JMC, Davis CC (2015) Phylogeny of Gracilariaceae (Rhodophyta): evidence from plastid and mitochondrial nucleotide sequences. J Phycol 51:356–366Google Scholar
  36. Marston M, Villalard-Bohnsack M (2002) Genetic variability and potentiel sources of Grateloupia doryphora (Halymeniaceae, Rhodophyta), an invasive species in Rhode Island waters (USA). J Phycol 38:649–658CrossRefGoogle Scholar
  37. McIvor L, Maggs CA, Provan J, Stanhope MJ (2001) rbcL sequences reveal multiple cryptic introductions of the Japanese red alga Polysiphonia harveyi. Mol Ecol 10:911–919CrossRefGoogle Scholar
  38. Mehta GK, Meena R, Prasad K, Genesan M, Siddhanta AK (2010) Preparation of galactans from Gracilaria debilis and Gracilaria salicornia (Gracilariales, Rhodophyta) of Indian waters. J Appl Phycol 22:623–627CrossRefGoogle Scholar
  39. Nelson SG, Glenn EP, Moore D, Ambrose B (2009) Growth and distribution of the macroalgae Gracilaria salicornia and G. parvispora (Rhodophyta) established from aquaculture introductions at Moloka‘i, Hawai‘i. Pac Sci 63:383–396CrossRefGoogle Scholar
  40. Ng P, Lim P, Phang S (2015) Small-scale genetic structure of Gracilaria salicornia and its red algal parasite, G. babae (Gracilariaceae, Rhodophyta), in Malaysia. Bot Mar 58:175–187CrossRefGoogle Scholar
  41. Ng P, Lin S, Lim P, Hurtado AQ, Phang S, Yow Y, Sun Z (2017) Genetic and morphological analyses of Gracilaria firma and G. changii (Gracilariaceae, Rhodophyta), the commercially important agarophytes in western Pacific. PLoS One 12:e0182176CrossRefGoogle Scholar
  42. Oliveira EC, Plastino EM (1994) Gracilariaceae. In: Akatsuka I (ed) Biology of economic algae. SPB Academic Publishing, The Hague, pp 185–226Google Scholar
  43. Oyieke HA (1993) The yield, physical and chemical properties of agar gel from Gracilaria species (Gracilariales, Rhodophyta) of the Kenya coast. Hydrobiologia 260/261:613–620CrossRefGoogle Scholar
  44. Oyieke HA (1994) The effect of phenotypic plasticity on agar from Gracilaria salicornia (J. ag.) Dawson (Gracilariales, Rhodophyta) in Kenya. Bioresour Technol 49:267–271CrossRefGoogle Scholar
  45. Oyieke HA, Kokwaro JO (1993) Seasonality of some species of Gracilaria (Gracilariales, Rhodophyta) from Kenya. J Appl Phycol 5:123–124CrossRefGoogle Scholar
  46. Pedrosa-Gerasmio IR, Agmata AB, Santos MD (2015) Genetic diversity, population genetic structure, and demographichistory of Auxis thazard (Perciformes), Selar crumenophthalmus (Perciformes), Rastrelliger kanagurta (Perciformes) and Sardinella lemuru (Clupeiformes) in Sulu-Celebes Sea inferred by mitochondrial DNA sequences. Fish Res 162:64–74CrossRefGoogle Scholar
  47. Phang S, Yeong H, Ganzon-Fortes ET, Lewmanomont K, Prathep A, Hau LN, Gerung GS, Tan KS (2016) Marine algae of the South China Sea bordered by Indonesia, Malaysia, Philippines, Singapore, Thailand and Vietnam. Raffles Bull Zool Suppl 40:13–59Google Scholar
  48. Phooprong S, Ogawa H, Hayashizaki K (2007) Photosynthetic and respiratory responses of Gracilaria salicornia (C. ag.) Dawson (Gracilariales, Rhodophyta) from Thailand and Japan. J Appl Phycol 19:795–801CrossRefGoogle Scholar
  49. Rodgers SK, Cox EF (1999) Rate of spread of introduced rhodophytes Kappaphycus alvarezii, Kappaphycus striatum, and Gracilaria salicornia and their current distributions in Kāne‘ohe bay, O‘ahu, Hawai‘i. Pac Sci 53:232–241Google Scholar
  50. Santelices B, Doty MS (1989) A review of Gracilaria farming. Aquaculture 78:95–133CrossRefGoogle Scholar
  51. Saunders GW (2005) Applying DNA barcoding to red macroalgae: a preliminary appraisal holds promise for future applications. Philos Trans R Soc Lond Ser B Biol Sci 360:1879–1888CrossRefGoogle Scholar
  52. Saunders GW (2009) Routine barcoding of Canadian Gracilariales (Rhodophyta) reveals the invasive species Gracilaria vermiculophylla in British Columbia. Mol Ecol Resources 9:140–150CrossRefGoogle Scholar
  53. Sherwood AR, Kurihara A, Conklin KY, Sauvage T, Presting GG (2010) The Hawaiian Rhodophyta biodiversity survey (2006-2010): a summary of principal findings. BMC Plant Biol 10:258CrossRefGoogle Scholar
  54. Silva PC, Meñez EG, Moe RL (1987) Catalog of the benthic marine algae of the Philippines. Smithsonian Institution Press, WashingtonCrossRefGoogle Scholar
  55. Silva PC, Basson PW, Moe RL (1996) Catalogue of the benthic marine algae of the Indian Ocean. Univ Calif Publ Bot 79:1–1259Google Scholar
  56. Smith JE, Hunter CL, Smith CM (2002) Distribution and reproductive characteristics of nonindigenous and invasive marine algae in the Hawaiian islands. Pac Sci 56:299–315CrossRefGoogle Scholar
  57. Smith JE, Hunter CL, Conklin EJ, Most R, Sauvage T, Squair C, Smith CM (2004) Ecology of the invasive red alga Gracilaria salicornia (Rhodophyta) on O‘ahu, Hawai‘i. Pac Sci 58:325–343CrossRefGoogle Scholar
  58. Song S, Lim P, Poong S, Phang S (2015) Genetic variation in Gracilaria tenuistipitata (Rhodophyta) from northern Singapore and neighbouring countries. Raffles Bull Zool Suppl 31:16–23Google Scholar
  59. Song S, Yong H, Lim P, Ng P, Phang S (2016) Complete mitochondrial genome, genetic diversity and molecular phylogeny of Gracilaria salicornia (Rhodophyta: Gracilariaceae). Phycologia 55:371–377CrossRefGoogle Scholar
  60. Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 101:1030–11035Google Scholar
  61. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol (12):2725–2729Google Scholar
  62. Terada R, Abe T, Kawaguchi S (2010) Reproductive phenology of three species of Gracilaria: G. blodgettii Harvey, G. vermiculophylla (Ohmi) Papenfuss and G. salicornia (C. Agardh) Dawson (Gracilariales, Rhodophyta) from Okinawa, Ryukyu Islands, Japan coast. Mar Sci 34:129–134Google Scholar
  63. Trono GC Jr, Ganzon-Fortes ET (1988) Philippine seaweeds. National Book Store, Manila 330 ppGoogle Scholar
  64. Tungpalan AY (1984) Ethnobotanical study of the seaweeds of Ilocos Norte. Ilocos Fish J 1:134–146Google Scholar
  65. Williams I, Walsh W, Miyasaki A, Friedlander A (2006) Effects of rotational closure on coral reef fishes in the Waikiki diamond head fishery management area, O‘ahu, Hawai. i Mar Ecol Prog Ser 310:139–149CrossRefGoogle Scholar
  66. Xia B (1986) On Gracilaria salicornia (C. Agardh) Dawson. Chin J Oceanol Limnol 4:100–106CrossRefGoogle Scholar
  67. Yamamoto H (1978) Systematic and anatomical study of the genus Gracilaria in Japan. Mem Fac Fish Hokkaido Univ 25:97–152Google Scholar
  68. Yang MY, Kim MS (2015) Molecular analyses for identification of the Gracilariaceae (Rhodophyta) from the Asia–Pacific region. Genes Genom 37:775–787CrossRefGoogle Scholar
  69. Yang EC, Kim KS, Geraldino PGL, Sahoo D, Shin J, Boo SM (2008) Mitochondrial cox1 and plastid rbcL genes of Gracilaria vermiculophylla (Gracilariaceae, Rhodophyta). J Appl Phycol 20:161–168CrossRefGoogle Scholar
  70. Yang MY, Geraldino PJL, Kim MS (2013) DNA barcode assessment of Gracilaria salicornia (Gracilariaceae, Rhodophyta) from Southeast Asia. Bot Stud 54:27CrossRefGoogle Scholar
  71. Yoshida T (1998) Marine algae of Japan. Uchida Rokakuho Publishing Co., Ltd., Tokyo 1222 ppGoogle Scholar
  72. Yow Y, Lim P, Phang S (2011) Genetic diversity of Gracilaria changii (Gracilariaceae, Rhodophyta) from west coast, peninsular Malaysia based on mitochondrial cox1 gene analysis. Appl Phycol 23:219–226CrossRefGoogle Scholar
  73. Yow Y, Lim P, Phang S (2013) Assessing the use of mitochondrial cox1 gene and cox2-3 spacer for genetic diversity study of Malaysian Gracilaria changii (Gracilariaceae, Rhodophyta) from peninsular Malaysia. Appl Phycol 25:831–838CrossRefGoogle Scholar
  74. Zemke-White WL, Ohno M (1999) World seaweed utilization: an end-century summary. J Appl Phycol 11:369–376CrossRefGoogle Scholar

Copyright information

© Plant Science and Biodiversity Centre, Slovak Academy of Sciences 2018

Authors and Affiliations

  1. 1.Marine Plants Section, National Fisheries Research and Development InstituteQuezon CityPhilippines
  2. 2.Department of Biological Sciences, Institute of Arts and SciencesFar Eastern UniversityManilaPhilippines

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