Morphological and molecular characterization of the free-living Symbiodinium natans-clade A (Dinophyceae) from Bahía de La Paz, Gulf of California

Main Article Content

Ana E Ramos-Santiago
https://orcid.org/0009-0000-3652-3565
Ignacio Leyva-Valencia
https://orcid.org/0000-0001-9904-1512
Yuri B Okolodkov
https://orcid.org/0000-0003-3421-3429
Christine J Band-Schmidt
https://orcid.org/0000-0002-8251-9820

Abstract

The genus Symbiodinium is a group of mostly endosymbiotic dinoflagellates, commonly known as zooxanthellae, which live in association with marine invertebrates and protists. The objective of the present study was the morphological and molecular identification of 2 strains of Symbiodiniales (SNCETMAR-1 and SNCETMAR-2) isolated from the anemone Actinostella sp. from Bahía de La Paz, Gulf of California. Culture identification was conducted via photomicroscopy, including epifluorescence and scanning electron microscopy. A sequence of the SNCETMAR-2 strain was obtained from the 28S rDNA region. The combination of methods allowed the strains to be identified as Symbiodinium natans-clade A. This taxon is a group of endosymbiotic and free-living organisms, which facilitated the cultivation of the strains in the laboratory. The life cycle of this group presented 2 phases, a motile and a non-motile phase in the coccoid state, the last stage where both sexual and asexual division occur. This study extends the reports of clade A of the family Symbiodiniaceae in the Gulf of California and provides valuable information for its culture, identification, and phylogenetic analysis.

Downloads

Download data is not yet available.

Article Details

How to Cite
Ramos-Santiago, A. E., Leyva-Valencia, I., Okolodkov, Y. B., & Band-Schmidt, C. J. (2025). Morphological and molecular characterization of the free-living Symbiodinium natans-clade A (Dinophyceae) from Bahía de La Paz, Gulf of California. Ciencias Marinas, 51. https://doi.org/10.7773/cm.y2025.3498
Section
Research Article

Metrics

References

Baker AC. 2003. Flexibility and specificity in coral-algal symbiosis: diversity, ecology, and biogeography of Symbiodinium. Annu Rev Ecol Evol Syst. 34(1):661-689. https://doi.org/10.1146/ANNUREV.ECOLSYS.34.011802.132417

Bigham-Soostani S, Yousefzadi M, Zarei-Darki B, Ranjbar MS. 2021. Evaluation of cytotoxic and antibacterial properties of Symbiodinium sp. isolated and purified from Stichodactyla haddoni in the Persian Gulf and Gulf of Oman. Aquat Physiol Biotechnol. 9(2):125-144. https://doi.org/10.22124/JAPB.2021.18141.1401

Bustillos-Guzmán J, Band-Schmidt CJ, Durán-Riveroll LM, Hernández-Sandoval FE, López-Cortés DJ, Núñez-Vázquez EJ, Cembella A, Krock B. 2015. Paralytic toxin profile of the marine dinoflagellate Gymnodinium catenatum Graham from the Mexican Pacific as revealed by LC-MS/MS. Food Addit Contam. 32A(3):1-14. https://doi.org/10.1080/19440049.2014.1000978

Carlos AA, Baillie BK, Kawachi M, Maruyama T. 1999. Phylogenetic position of Symbiodinium (Dinophyceae) isolates from tridacnids (Bivalvia), cardiids (Bivalvia), a sponge (Porifera), a soft coral (Anthozoa), and a free‐living strain. J Phycol. 35(5):1054-1062. https://doi.org/10.1046/j.1529-8817.1999.3551054.x

De Palmas S, Denis V, Ribas-Deulofeu L, Loubeyres M, Woo S, Hwang SJ, Song JI, Chen CA. 2015. Symbiodinium spp. associated with high-latitude scleractinian corals from Jeju Island, South Korea. Coral Reefs. 34:919-925. https://doi.org/10.1007/s00338-015-1286-y

Figueroa RI, Howe-Kerr LI, Correa AMS. 2021. Direct evidence of sex and a hypothesis about meiosis in Symbiodiniaceae. Sci Rep. 11:18838. https://doi.org/10.1038/s41598-021-98148-9

Graham ER, Parekh A, Devassy RK, Sanders RW. 2015. Carbonic anhydrase activity changes in response to increased temperature and pCO2 in Symbiodinium-zoanthid associations. J Exp Mar Biol Ecol. 473:218-226. https://doi.org/10.1016/j.jembe.2015.08.017

Granados-Cifuentes C, Neigel J, Leberg P, Rodriguez-Lanetty M. 2015. Genetic diversity of free-living Symbiodinium in the Caribbean: the importance of habitats and seasons. Coral Reefs. 34(3):927-939. https://doi.org/10.1007/s00338-015-1291-1

Guiry MD, Andersen RA. 2018. Validation of the generic name Symbiodinium (Dinophyceae, Suessiaceae) revisited and the reinstatement of Zooxanthella K. Brandt. Notulae Algarum. 58:1-5.

Guiry MD, Guiry GM. 2024. AlgaeBase. World-wide electronic publication. Galway (Ireland): National University of Ireland; [accessed Feb 2024]. https://www.algaebase.org/search/genus/detail/?genus_id=44695

Hansen G, Daugbjerg N. 2009. Symbiodinium natans sp. nov.: a “free-living” dinoflagellate from Tenerife (Northeast-Atlantic Ocean). J Phycol. 45(1):251-263. https://doi.org/10.1111/j.1529-8817.2008.00621.x

Hirose M, Reimer JD, Hidaka M, Suda S. 2008. Phylogenetic analyses of potentially free-living Symbiodinium spp. isolated from coral reef sand in Okinawa, Japan. Mar Biol. 155:105-112. https://doi.org/10.1007/s00227-008-1011-2

Hoppenrath M, Chomerat N, Horiguchi T, Murray SA, Rhodes L. 2023. Marine benthic dinoflagellates - their relevance for science and society. 2nd ed. Stuttgart (Germany): E. Schweizerbart’sche Verlagsbuchhandlung (Nägele u. Obermiller) and Senckenberg Geselschaft für Naturforschung. 376 p.

Hosoi-Tanabe S, Otake I, Sako Y. 2006. Phylogenetic analysis of noxious red tide flagellates Chattonella antiqua, C. marina, C. ovata, and C. verruculosa (Raphidophyceae) based on the rRNA gene family. Fish Sci. 72:1200-1208. https://doi.org/10.1111/j.1444-2906.2006.01277.x

Iglesias-Prieto R, Beltrán VH, LaJeunesse TC, Reyes-Bonilla H, Thomé PE. 2004. Different algal symbionts explain the vertical distribution of dominant reef corals in the eastern Pacific. Proc R Soc Lond B Biol Sci. 271:1757-1763. https://doi.org/10.1098/rspb.2004.2757

Iglesias-Prieto R, Matta JL, Robins WA, Trench RK. 1992. Photosynthetic response to elevated temperature in the symbiotic dinoflagellate Symbiodinium microadriaticum in culture. Proc Natl Acad Sci. 89(21):10302-10305. https://doi.org/10.1073/pnas.89.21.10302

Iglesias-Prieto R, Trench RK. 1994. Acclimation and adaptation to irradiance in symbiotic dinoflagellates. I. Responses of the photosynthetic unit to changes in photon flux density. Mar Ecol Prog Ser. 113:163-175. https://doi.org/10.3354/meps113163

Iglesias-Prieto R, Trench RK. 1997. Acclimation and adaptation to irradiance in symbiotic dinoflagellates. II. Response of chlorophyll-protein complexes to different photon-flux densities. Mar Biol. 130(1):23-33. https://doi.org/10.1007/s002270050221

Jeong HJ, Lee SY, Kang NS, Yoo YD, Lim AS, Lee MJ, Kim HS, Yih W, Yamashita H, LaJeunesse TC. 2014. Genetics and morphology characterize the dinoflagellate Symbiodinium voratum, n. sp., (Dinophyceae) as the sole representative of Symbiodinium Clade E. J Eukaryot Microbiol. 61(1):75-94. https://doi.org/10.1111/jeu.12088

Keller MD, Selvin RC, Claus W, Guillard RRL. 1987. Media for the culture of oceanic ultraplankton. J Phycol. 23(4):633-638. https://doi.org/10.1111/j.1529-8817.1987.tb04217.x

Kemp DW, Hernandez-Pech X, Iglesias-Prieto R, Fitt WK, Schmidt GW. 2014. Community dynamics and physiology of Symbiodinium spp. before, during, and after a coral bleaching event. Limnol Oceanogr. 59(3):788-797. https://doi.org/10.4319/lo.2014.59.3.0788

LaJeunesse TC, Lee SY, Gil-Agudelo DL, Knowlton N, Jeong HJ. 2015. Symbiodinium necroappetens sp. nov. (Dinophyceae): an opportunist ‘zooxanthella’ found in bleached and diseased tissues of Caribbean reef corals. Eur J Phycol. 50(2):223-238. https://doi.org/10.1080/09670262.2015.1025857

LaJeunesse TC, Parkinson JE, Gabrielson PW, Jeong HJ, Reimer JD, Voolstra CR, Santos SR. 2018. Systematic revision of Symbiodiniaceae highlights the antiquity and diversity of coral endosymbionts. Curr Biol. 28(16):2570-2580.e6. https://doi.org/10.1016/j.cub.2018.07.008

Lee SY, Jeong HJ, Kang NS, Jang TY, Jang SH, Lajeunesse TC. 2015. Symbiodinium tridacnidorum sp. nov., a dinoflagellate common to Indo-Pacific giant clams, and a revised morphological description of Symbiodinium microadriaticum Freudenthal, emended Trench & Blank. Eur J Phycol. 50(2):155-172. https://doi.org/10.1080/09670262.2015.1018336

Méndez-Méndez SM. 2020. Expresión diferencial de genes en Cladocopium sp. de dos especies de coral en el Golfo de California [dissertation]. [Mexico]: CIBNOR. 80 p.

Mordret S, Romac S, Henry N, Colin S, Carmichael M, Berney C, Audic S, Richter DJ, Pochon X, de Vargas C, et al. 2016. The symbiotic life of Symbiodinium in the open ocean within a new species of calcifying ciliate (Tiarina sp.) The ISME J. 10(6):1424-1436. https://doi.org/10.1038/ismej.2015.211

Parkinson JE, Coffroth MA, LaJeunesse TC. 2015. New species of Clade B Symbiodinium (Dinophyceae) from the greater Caribbean belong to different functional guilds: S. aenigmaticum sp. nov., S. antillogorgium sp. nov., S. endomadracis sp. nov., and S. pseudominutum sp. nov. J Phycol. 51(5):850-858. https://doi.org/10.1111/jpy.12340

Pawlowski J, Holzmann M, Fahrni JF, Pochon X, Lee JJ. 2001. Molecular identification of algal endosymbionts in large miliolid Foraminifera: 2. Dinoflagellates. J Eukaryot Microbiol. 48(3):368-373. https://doi.org/10.1111/j.1550-7408.2001.tb00326.x

Pochon X, Gates RD. 2010. A new Symbiodinium clade (Dinophyceae) from soritid foraminifera in Hawai’i. Mol Phylogenet Evol. 56(1):492-497. https://doi.org/10.1016/j.ympev.2010.03.040

Ramos-Santiago AE. 2023. Taxonomía morfológica y molecular de dinoflagelados epibentónicos del Golfo de California [dissertation]. [Mexico]: CICIMAR-IPN. 203 p.

Sampayo EM, Dove S, LaJeunesse TC. 2009. Cohesive molecular genetic data delineate species diversity in the dinoflagellate genus Symbiodinium. Mol Ecol. 18(3):500-519. https://doi.org/10.1111/j.1365-294X.2008.04037.x

Santos SR, Taylor DJ, Coffroth MA. 2001. Genetic comparisons of freshly isolated versus cultured symbiotic dinoflagellates: Implications for extrapolating to the intact symbiosis. J Phycol. 37(5):900-912. https://doi.org/10.1046/j.1529-8817.2001.00194.x

Sea temperature. 2024. Water temperature in La Paz (BCS); [accessed Feb 2024]. https://seatemperature.info/august/mexico/la-paz-water-temperature.html

Takabayashi M, Adams LM, Pochon X, Gates RD. 2012. Genetic diversity of free-living Symbiodinium in surface water and sediment of Hawai̔i and Florida. Coral Reefs. 31(1):157-167. http://doi.org/10.1007/s00338-011-0832-5

Takahashi S, Whitney SM, Badger MR. 2009. Different thermal sensitivity of the repair of photodamaged photosynthetic machinery in cultured Symbiodinium species. Proc Natl Acad Sci. 106:3237-3242. https://doi.org/10.1073/pnas.0808363106

Taylor FJR, Harrison PJ. 1983. Ecological aspects of intracellular symbiosis. In: Schenk HEA, Schwemmler W, Intracellular Space as Oligogenetic Ecosystem. Berlin (Germany): De Gruyter. p. 828-842. https://doi.org/10.1515/9783110841237-086

Wilcox TP. 1998. Large-subunit ribosomal RNA systematics of symbiotic dinoflagellates: morphology does not recapitulate phylogeny. Mol Phylogenet Evol. 10(3):436-448.

Yamashita H, Koike K. 2013. Genetic identity of free-living Symbiodinium obtained over a broad latitudinal range in the Japanese coast. Phycol Res. 61(1):68-80. https://doi.org/10.1111/pre.12004

Yorifuji M, Takeshima H, Mabuchi K, Watanabe T, Nishida M. 2015. Comparison of Symbiodinium dinoflagellate flora in sea slug populations of the Pteraeolidia ianthina complex. Mar Ecol Prog Ser. 521:91-104. https://doi.org/10.3354/meps11155