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.
Similar content being viewed by others
References
Agardh CA (1820) Icones algarum ineditae. Fasc. 1. Lundae (Lund]) [4] pp., pls. I–X
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 12:4550–4573
Armisen R (1995) World-wide use and importance of Gracilaria. J Appl Phycol 7:231–243
Ballard WO, Whitlock MC (2004) The incomplete natural history of mitochondria. Mol Ecol 13:729–744
Bezerra AF, Marinho-Soriano E (2010) Cultivation of the red seaweed Gracilaria birdiae (Gracilariales, Rhodophyta) in tropical waters of Northeast Brazil. Biomass Bioenergy 34:1813–1817
Bird CJ (1995) A review of recent taxonomic concepts and developments in the Gracilariaceae (Rhodophyta). J Appl Phycol 7:255–267
Bird CJ, McLachlan J (1982) Some underutilized taxonomic criteria in Gracilaria (Rhodophyta, Gigartinales). Bot Mar 25:557–562
Buschmann AH, Correa JA, Westermeier R, Hernández-González MC, Norambuena R (2001) Red algal farming in Chile: a review. Aquaculture 194:203–220
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):173–182
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 53:109–116
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:e77662
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 161:785–795
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 30:83–91
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1669
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 24:1643–1653
Dawson EY (1954) Notes on tropical Pacific marine algae. Bull Soc Calif Acad Sci 53:1–7
Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376
Fredericq S, Hommersand MH (1990) Diagnoses and key to the genera of the Gracilariaceae (Gracilariales, Rhodophyta). Hydrobiologia 204/205:173–178
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 456:78–86
Gurgel CFD, Fredericq S (2004) Systematics of the Gracilariaceae (Gracilariales, Rhodophyta): a critical assessment based on rbcL sequence analyses. J Phycol 40:138–159
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):13
Hashim MA, Chu KH (2004) Biosorption of cadmium by brown, green and red seaweed. Chem Eng J 97:249–255
Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc Royal Society B Biol Sci 270:313–322
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 22:4673–4680
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 62–69
Iyer R, Tronchin EM, Bolton JJ, Coyne VE (2005) Molecular systematics of the Gracilariaceae (Gracilariales, Rhodophyta) with emphasis on southern Africa. J Phycol 41:672–684
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 133:866–874
Kim MS, Yang MY, Cho GY (2010a) Applying DNA barcoding to Korean Gracilariaceae (Rhodophyta). Cryptogam Algol 31:387–401
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 46:1346–1349
Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
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 70–78
Liao LM, Hommersand MH (2003) A morphological study and taxonomic assessment of the generitype species in the Gracilariaceae. J Phycol 39:1207–1232
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452
Lim P, Thong K, Phang S (2001) Molecular differentiation of two morphological variants of Gracilaria salicornia. J Appl Phycol 13:335–342
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 51:356–366
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 38:649–658
McIvor L, Maggs CA, Provan J, Stanhope MJ (2001) rbcL sequences reveal multiple cryptic introductions of the Japanese red alga Polysiphonia harveyi. Mol Ecol 10:911–919
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 22:623–627
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 63:383–396
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 58:175–187
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:e0182176
Oliveira EC, Plastino EM (1994) Gracilariaceae. In: Akatsuka I (ed) Biology of economic algae. SPB Academic Publishing, The Hague, pp 185–226
Oyieke HA (1993) The yield, physical and chemical properties of agar gel from Gracilaria species (Gracilariales, Rhodophyta) of the Kenya coast. Hydrobiologia 260/261:613–620
Oyieke HA (1994) The effect of phenotypic plasticity on agar from Gracilaria salicornia (J. ag.) Dawson (Gracilariales, Rhodophyta) in Kenya. Bioresour Technol 49:267–271
Oyieke HA, Kokwaro JO (1993) Seasonality of some species of Gracilaria (Gracilariales, Rhodophyta) from Kenya. J Appl Phycol 5:123–124
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 162:64–74
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 40:13–59
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 19:795–801
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 53:232–241
Santelices B, Doty MS (1989) A review of Gracilaria farming. Aquaculture 78:95–133
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 360:1879–1888
Saunders GW (2009) Routine barcoding of Canadian Gracilariales (Rhodophyta) reveals the invasive species Gracilaria vermiculophylla in British Columbia. Mol Ecol Resources 9:140–150
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 10:258
Silva PC, Meñez EG, Moe RL (1987) Catalog of the benthic marine algae of the Philippines. Smithsonian Institution Press, Washington
Silva PC, Basson PW, Moe RL (1996) Catalogue of the benthic marine algae of the Indian Ocean. Univ Calif Publ Bot 79:1–1259
Smith JE, Hunter CL, Smith CM (2002) Distribution and reproductive characteristics of nonindigenous and invasive marine algae in the Hawaiian islands. Pac Sci 56:299–315
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 58:325–343
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 31:16–23
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 55:371–377
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 101:1030–11035
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol (12):2725–2729
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 34:129–134
Trono GC Jr, Ganzon-Fortes ET (1988) Philippine seaweeds. National Book Store, Manila 330 pp
Tungpalan AY (1984) Ethnobotanical study of the seaweeds of Ilocos Norte. Ilocos Fish J 1:134–146
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 310:139–149
Xia B (1986) On Gracilaria salicornia (C. Agardh) Dawson. Chin J Oceanol Limnol 4:100–106
Yamamoto H (1978) Systematic and anatomical study of the genus Gracilaria in Japan. Mem Fac Fish Hokkaido Univ 25:97–152
Yang MY, Kim MS (2015) Molecular analyses for identification of the Gracilariaceae (Rhodophyta) from the Asia–Pacific region. Genes Genom 37:775–787
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 20:161–168
Yang MY, Geraldino PJL, Kim MS (2013) DNA barcode assessment of Gracilaria salicornia (Gracilariaceae, Rhodophyta) from Southeast Asia. Bot Stud 54:27
Yoshida T (1998) Marine algae of Japan. Uchida Rokakuho Publishing Co., Ltd., Tokyo 1222 pp
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 23:219–226
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 25:831–838
Zemke-White WL, Ohno M (1999) World seaweed utilization: an end-century summary. J Appl Phycol 11:369–376
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.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
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.
Rights and permissions
About this article
Cite this article
Ferrer, M.S.R., Gomez, R.N., Nacido, C.B. et al. Genetic diversity of Philippine Gracilaria salicornia (Gracilariaceae, Rhodophyta) based on mitochondrial COI-5P sequences. Biologia 74, 599–607 (2019). https://doi.org/10.2478/s11756-018-00179-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11756-018-00179-7