Morphological and molecular analyses of Coolia malayensis (Dinophyceae) and effects of extracts of the macroalga Dictyota dichotoma (Phaeophyceae) on its growth
Morphological and molecular analyses of Coolia malayensis (Dinophyceae) and effects of extracts of the macroalga Dictyota dichotoma (Phaeophyceae) on its growth
DOI:
https://doi.org/10.37543/oceanides.v37i1-2.276Keywords:
epibenthic dinoflagellates, growth curves, molecular taxonomyAbstract
Coolia is a genus that at present includes eight species of epibenthic dinoflagellates of interest due
to the toxins produced (e.g., cooliatoxin) by species of the genus and their associations with other toxic epibenthic
dinoflagellates genera (Ostreopsis, Amphidinium, Prorocentrum and Gambierdiscus). There is limited information
on the diversity and ecology of this genus along the coasts of Mexico. The objectives of this study were to identify
by the use of integrative taxonomy (morphological and molecular) two isolates of Coolia (CMBAPAZ-1 and s/i 72)
from Bahía de la Paz, Gulf of California and to determine the effects of the extracts from the macroalga Dictyota dichotoma on their growth. Both isolates were cultured in GSe medium with and without macroalgal extracts: 1) GSe
medium, 2) GSe with the addition of the crude extract of D. dichotoma, 3) GSe with the addition of the carbohydrate
fraction of D. dichotoma, and 4) GSe with the addition of the non-precipitable fraction of D. dichotoma. Morphological and molecular analyses of the 28S region of rDNA (bootstrap values > 95%) confirmed the identification
of the isolates as Coolia malayensis. There were no significant differences (p < 0.05) in the cell abundances of two
strains in GSe medium compared with the other treatments. The maximum abundances found in strains CMBAPAZ-1 and s/i 72 at 28 days of culture were 40,271 ± 3,018 and 43,428 ± 4,560 cells mL-1, respectively. The growth
rate ranged from 0.129 to 0.139 div day-1 in both strains. The extract and fractions of D. dichotoma neither favored
nor inhibited the growth of C. malayensis; therefore, the possibility that the macroalga may favor the growth of this
dinoflagellate in its natural environment is not excluded
Downloads
References
Accoroni, S., Percopo, I., Cerino, F., Romagnoli, T.,
Pichierri, S., Perrone, C., y Totti, C. (2015). Allelopathic interactions between the HAB dinoflagellate Ostreopsis cf. ovata and macroalgae. Harmful Algae, 49, 147-155. https://doi.org/10.1016/j.
hal.2015.08.007
Almazán-Becerril, A., Rosiles-González, G., Escobar-Morales, S., Rodríguez-Palacios, M., y Hernández-Becerril, D.U. (2012). Dinoflagelados
bentónicos del Arrecife Mesoamericano: Caribe
mexicano. Centro de Investigación Científica de
Yucatán, Mérida, Yucatán, México.
Aquino-Cruz, A., y Okolodkov, Y.B. (2016). Impact of increasing water temperature on growth,
photosynthetic efficiency, nutrient consumption,
and potential toxicity of Amphidinium cf. carterae and Coolia monotis (Dinoflagellata). Revista de Biología Marina y Oceanografía,51(3),
-580. https://doi.org/10.4067/S0718-
Arbelaez, N., Mancera-Pineda, J.E., y Reguera, B.
(2017). Epiphytic dinoflagellates of Thalassia
testudinum in two coastal systems of the Colombian Caribbean. Boletín de Investigaciones
Marinas y Costeras, 46(2), 9-40. https://doi.
org/10.25268/bimc.invemar.2017.46.2.725
Armi, Z., Turki, S., Trabelsi, E., y Ben-Maiz, N.
(2010). First recorded proliferation of Coolia mo- notis (Meunier, 1919) in the North Lake of Tunis
(Tunisia) correlation with environmental factors.
Environmental Monitoring and Assessment, 164, 423-433. https://doi.org/10.1007/s10661-009-
-z
Ataka, T., Funaki, H., Yamaguchi, H., y Adachi, M.
(octubre de 2021). Effect of adding macroalgal
extracts on the growth of Gambierdiscus scabrosus and G. silvae isolated from Japan. En C.J.
Band-Schmidt (Presidencia). Resumen del XIX
International Conference on Harmful Algae, La
Paz, Baja California Sur, México.
Barranguet, C. (1997). The role of microphytoben- thic primary production in a Mediterranean mus- sel culture area. Estuarine Coastal and Shelf
Science, 44, 753-765. https://doi.org/10.1006/
ecss.1996.0153
Ben-Gharbia, H., KeÂfi-Daly, Y.O., Cecchi, P., Masseret, E., Amzil, Z., Herve, F., Laabir, M. (2017).
New insights on the species-specific allelopa- thic interactions between macrophytes and ma- rine HAB dinoflagellates. PLoS ONE, 12(11),
e0187963. https://doi.org/10.1371/journal.
pone.0187963
Bianco, É. M., Rogers, R., Teixeira, V.L., y Pereira,
R. (2008). Antifoulant diterpenes produced by
the brown seaweed Canistrocarpus cervicornis.
Journal of Applied Phycology, 21(3), 341-346.
https://doi.org/10.1007/s10811-008-9374-9
Blanfuné, A., Boudouresque, C.F., Grossel, H., y
Thibaut, T. (2015). Distribution and abundance
of Ostreopsis spp. and associated species (Dinophyceae) in the northwestern Mediterranean:
the region and the macroalgal substrate matter.
Environmental Science and Pollution Research,
(16), 12332-12346. https://doi.org/10.1007/
s11356-015-4525-4
Boisnoir, A., Pascal, P.Y., Cordonnier, S., y Lemée,
R. (2019). Spatio-temporal dynamics and biotic
substrate preferences of benthic dinoflagellates
in the Lesser Antilles, Caribbean Sea. Harmful Algae, 81, 18-29. https://doi.org/10.1016/j.
hal.2018.11.012
Bustillos-Guzmán, J.J., Band-Schmidt, C.J., Durán-Riveroll, L.M., Hernández-Sandoval, F.E.,
López-Cortés, D.J., Núñez-Vázquez, E.J.,…
Krock, B. (2015). Paralytic toxin profile of the
marine dinoflagellate Gymnodinium catenatum
Graham from the Mexican Pacific as revealed by
LC-MS/MS. Food Additives & Contaminants,
(3), 381-394. https://doi.org/10.1080/1944004
2014.1000978
Carnicer, O., Tunin Ley, A., Andree, K.B., Turquet,
J., Diogène, J., y Fernández Tejedor, M. (2015).
Contribution to the genus Ostreopsis in Reunion
Island (Indian Ocean): molecular, morphologic
and toxicity characterization. Cryptogamie, Algologie, 36(1), 101-119. https://doi.org/10.7872/
crya.v36.iss1.2015.101
Chinain, M., Gatti, C.M., Roué, M., y Darius, T.
(2020). Ciguatera-causing dinoflagellates in the
genera Gambierdiscus and Fukuyoa: distribution,
ecophysiology and toxicology. En D.V. Subba
Rao (Ed.), Dinoflagellates: classification, evolu- tion, physiology and ecological significance (pp.
-457). Hauppauge, NY, USA: Nova Science
Publishers.
Cohu, S., Thibaut, T., Mangialajo, L., Labat, J.P.,
Passafiume, O., Blanfuné, A., Simon, N., Cottalorda, J.M., y Lemée, R. (2011). Occurrence of
the toxic dinoflagellate Ostreopsis cf. ovata in
relation with environmental factors in Monaco
(NW Mediterranean). Marine Pollution Bulletin, 62(12), 2681-2691. https://doi.org/10.1016/j.
Efectos de Dictyota dichotoma en el crecimiento de Coolia malayensis 15
marpolbul.2011.09.022
Darriba, D., Taboada, G.L., Doallo, R., y Posada, D.
(2012). jModelTest 2: more models, new heuristics and parallel computing. Nature Methods,
(8), 772. https://doi.org/10.1038/nmeth.2109
David, H., Laza-Martínez, A., Rodríguez, F., Fraga,
S., y Orive, E. (2019). Coolia guanchica sp. nov.
(Dinophyceae) a new epibenthic dinoflagellate
from the Canary Islands (NE Atlantic Ocean).
European Journal of Phycology, 55(1), 1-13.
https://doi.org/10.1080/09670262.2019.1651400
El-Katony, T. M., Deyab, M.A., El-Adl, M.F., y Ward,
F.M.E.N. (2020). The aqueous extract and powder of the brown alga Dictyota dichotoma (Hudson) differentially alleviate the impact of abiotic
stress on rice (Oryza sativa L.). Physiology and
Molecular Biology of Plants, 26(6), 1155-1171.
https://doi.org/10.1007/s12298-020-00805-2
Faust, M.A. (1995). Observation of sand-dwelling
toxic dinoflagellates (Dinophyceae) from widely differing sites, including two new species.
Journal of Phycology, 31, 996-1003. https://doi.
org/10.1111/j.0022-3646.1995.00996.x
Fraga, S., Penna, A., Bianconi, I., Paz, B., y Zapata,
M. (2008). Coolia canariensis sp. nov. (Dinophyceae), a new nontoxic epiphytic benthic dinoflagellate from the Canary Islands. Journal of Phycology, 44, 1060-1070. https://doi.org/10.1111/
j.1529-8817.2008.00555.x
Gémin, M.P., Réveillon, D., Hervé, F., Pavaux, A.S.,
Tharaud, M., Séchet, V.,…Amzil, Z. (2020).
Toxin content of Ostreopsis cf. ovata depends
on bloom phases, depth and macroalgal substrate in the NW Mediterranean Sea. Harmful
Algae, 92(101727). https://doi.org/10.1016/j.
hal.2019.101727
Gómez, F., Qiu, D., Otero-Morales, E., Lopes, R.M., y
Lin, S. (2016). Circumtropical distribution of the
epiphytic dinoflagellate Coolia malayensis (Dinophyceae): morphology and molecular phylogeny from Puerto Rico and Brazil. Phycological
Research, 64, 194-199. https://doi.org/10.1111/
pre.12134
González-Giro, Z., Fuentes-Reyes, M., Batista-Corbal, P., Campos-Castro A., y Vera-Pérez, Y.
(2015). Análisis fitoquímico preliminar de dos
extractos del alga Padina gymnospora. Revista
de Ciencias Biológicas y de la Salud, 17(2), 26-
https://doi.org/10.18633/BT.V17I2.176
Grzebyk, D., Berland, B., Thomassin, B.A., Bosi, C.,
y Arnoux, A. (1994). Ecology of ciguateric din- oflagellates in the coral reef complex of Mayotte
Island (SW Indian Ocean). Journal of Experi- mental Marine Biology and Ecology, 187, 51-66.
https://doi.org/10.1016/0022-0981(94)90224-0
Guillard, R.R.L. (1973). Methods for microflagellates
and nannoplankton. En J.R. Stein. (Ed.), Handbook of phycological methods. Culture methods
and growth measurements (pp. 69-85). Cambrid- ge, UK: Cambridge, University Press.
Guiry, M.D., y Guiry, G.M. (2022). AlgaeBase. National University of Ireland, Galway, Republic
of Ireland. Recuperado de http://www.algaebase.
org
Hernández-Castro, J.E. (2017). Dinoflagelados y toxinas lipofílicas en bancos naturales de bivalvos
al sur de la Bahía de La Paz, B.C.S., México (Tesis de maestría). CICIMAR-IPN, La Paz, Baja
California Sur, México.
Hoppenrath, M., Murray, S. A., Chomérat, N., y Horiguchi, T. (2014). Marine benthic dinoflagellates
dinoflagellates - unveiling their worldwide biodiversity. Stuttgart, Germany: Schweizerbart’sche
Verlagsbuchhandlun (Nägele u. Obermuller).
Hosoi-Tanabe, S., Otake, I., y Sako, Y. (2006). Análisis filogenético de flagelados nocivos de la
marea roja Chattonella antiqua, C. marina, C.
ovata y C. verruculosa (Raphidophyceae) basado
en la familia de genes rRNA. Fisheries Science,
(6), 1200-1208. https://doi.org/10.1111/j.1444-
2006.01277.x
Jeong, H.J., Yih, W., Kang, N.S., Lee, S.Y., Yoon,
E.Y., Yoo, Y.D.,…Kim, J.H. (2012). First report
of the epiphytic benthic dinoflagellates Coolia
canariensis and Coolia malayensis in the waters
off Jeju Island, Korea: morphology and rADN
sequences. Journal of Eukaryotic Microbiolo- gy, 59, 114-133. https://doi.org/10.1111/j.1550-
2012.00610.x
Karafas, S., York, R., y Tomas, C. (2015). Morphological and genetic analysis of the Coolia monotis species complex with the introduction of
two new species, Coolia santacroce sp. nov. and
Coolia palmyrensis sp. nov. (Dinophyceae). Har- mful Algae, 46, 18-33. https://doi.org/10.1016/j.
hal.2015.05.002
Larsson M.E., Smith, K.F., y Doblin, M.A. (2019).
First description of the environmental niche of
the epibenthic dinoflagellate species Coolia palmyrensis, C. malayensis, and C. tropicalis (Dinophyceae) from eastern Australia. Journal of
Phycology, 55, 565-577. https://doi.org/10.1111/
jpy.12833
Laza-Martínez, A., Orive, E., y Miguel, I. (2011).
Morphological and genetic characterization of
benthic dinoflagellates of the genera Coolia, Ostreopsis and Prorocentrum from the south-eastern Bay of Biscay. European Journal of Phyco-
Ramos Santiago et al.
logy, 46(1), 45-65. https://doi.org/10.1080/09670
2010.550387
Leaw, C.P., Po-Teen, L., Kok, Wah, C., Boon-Koon,
N., y Gires, U. (2010). Morphology and molecular characterization of a new species of thecate benthic dinoflagellate, Coolia malayensis
sp. nov. (Dinophyceae). Journal of Phycology,
, 162-171. https://doi.org/10.1111/j.1529-
2009.00778.x
Leaw, C.P., Tan, T.H., Lim, H.C., Teng, S.T., Yong,
H.L., Smith, K.F.,…Lim, P.T. (2016). New
scenario for speciation in the benthic dinoflagellate genus Coolia (Dinophyceae). Harmful
Algae, 55, 137-149. https://doi.org/10.1016/j.
hal.2016.02.010
Leung, P.T.Y., Yan, M., Yiu, S.K.F., Lam, V.T.T., Ip,
J.C.H., Au, M.W.Y.,…Lam, P.K.S. (2017). Molecular phylogeny and toxicity of harmful benthic dinoflagellates Coolia (Ostreopsidaceae,
Dinophyceae) in a sub-tropical marine ecosystem: the first record from Hong Kong. Marine
Pollution Bulletin, 124, 878-889. https://doi.org/10.1016/j.marpolbul.2017.01.017
Li, X., Yan, M., Gu, J., Lam, V.T.T., Wai, T.C., Baker,
D.M.,…Leung, P.T.Y. (2020). The effect of temperature on physiology, toxicity and toxin content of the benthic dinoflagellate Coolia malayensis from a seasonal tropical region. Water
Research, 185, 116264. https://doi.org/0.1016/j.
watres.2020.116264
Marchan-Álvarez, J., Valerio-Gonzáles, L., Troccoli-Ghinaglia, L., y López-Monroy, F. (2017). Dinoflagelados bentónicos asociados con el sedimento arenoso en dos playas de la isla de Margarita,
Venezuela. Revista Biodiversidad Neotropical, 7(3), 156-168. https://doi.org/10.18636/bioneo- tropical.v7i3.539
Mateo-Cid, L.E., Mendoza-González, A.C., Huer- ta-Múzquiz, L., Aguilar-Rosas, R., y Aguilar-Ro- sas, L.E. (2000). La familia Dictyotaceae (Dictyotales, Phaeophyta) en la península de Baja California, México. Anales de la Escuela Nacional
de Ciencias Biológicas, 46(2), 189-270.
Mohammad-Noor, N., Adam, A., Saad, S., Ak- mal-Khodzori, F., y Muhd-Shaleh, S.R. (2019).
Effects of medium and substrate preferences
soil extract on growth of Coolia (Dinophyceae).
Journal of System Management, 14(2), 71-81.
Mohammad-Noor, N., Moestrup, O., Lundholm, N.,
Fraga, S., Adam, A., Holmes, M.J., y Saleh, E.
(2013). Autecology and phylogeny of Coolia tro- picalis and Coolia malayensis (Dinophyceae),
with emphasis on taxonomy of C. tropicalis ba- sed on light microscopy, scanning electron microscopy and LSU rADN. Journal of Phycology,
, 536-545. https://doi.org/10.1111/jpy.12062
Momigliano, P., Sparrow, L., Blair, D., y Heimann, K.
(2013). The diversity of Coolia spp. (Dinophyceae Ostreopsidaceae) in the central Great Barrier
Reef Region. PLoS ONE, 8(10), e79278. https://
doi.org/10.1371/journal.pone.0079278
Nascimento, S.M., da Silva, R.A.F., Oliveira, F., Fraga, S., y Salgueiro, F. (2019). Morphology and
molecular phylogeny of Coolia tropicalis, Coolia
malayensis and a new lineage of the Coolia canariensis species complex (Dinophyceae) isolated
from Brazil. European Journal of Phycology, 54,
-13. https://doi.org/10.1080/09670262.2019.15
Penna, A., Battocchi, C., Capellacci, S., Fraga, S.,
Aligizaki, K., Lemée, R., y Vernesi, C. (2014).
Mitochondrial, but not rADN, genes fail to dis- criminate dinoflagellate species in the genus Os- treopsis. Harmful Algae, 40, 40-50. https://doi.
org/10.1016/j.hal.2014.10.004
Penna, A., Vila, M., Fraga, S., Giacobbe, M.G.,
Andreoni, F., Riobo, P., y Vernesi, C. (2005).
Characterization of Ostreopsis and Coolia (Di- nophyceae) isolates in the western Mediterranean
Sea based on morphology, toxicity and internal
transcribed spacer 5.8s rADN sequences. Journal of Phycology, 41(1), 212-225. https://doi.org/10.1111/j.1529-8817.2005.04011.x
Rahman-Shah, M., Samarakoon, K.W., Ko, J., Chaminda-Lakmal, H.H., Lee, J., An, S.,…J. Lee.
(2014). Potentiality of benthic dinoflagellate
cultures and screening of their bioactivities in
Jeju Island, Korea. African Journal of Biotechnology, 13(6), 792-805. https://doi.org/10.5897/
AJB2013.13250
Ronquist, F., Teslenko, M., van der Mark, P., Ayres,
D.L., Darling, A., Höhna, S.,…Huelsenbeck, J.P.
MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large
model space. Systematic Biology, 61(3), 539-542.
https://doi.org/10.1093/sysbio/sys029
Ruh, W.W., Ahmad, A., Mat Isa, M.N., Mahadi, N.M.,
Marasan, N.A., y Usup, G. (2009). Diversity of
bacteria associated with the benthic marine dinoflagellates Coolia monotis and Ostreopsis ovata
from Malaysian waters. Journal of Science and
Technology in the Tropics, 5, 23-33.
Salvador, N., Gómez Garreta, A., Lavelli, L., y Ribe- ra, M.A. (2007). Antimicrobial activity of Iberian
Efectos de Dictyota dichotoma en el crecimiento de Coolia malayensis 17
macroalgae. Scientia Marina, 71(1), 101-113.
https://doi.org/10.3989/scimar.2007.71n1101
Sepúlveda-Villarraga, M. (2017). Dinoflagelados potencialmente tóxicos asociados a macroalgas en
la Bahía de La Paz, B.C.S. (Tesis de maestría).
CICIMAR-IPN, La Paz, Baja California Sur, México.
StatSoft, Inc. (2007). STATISTICA (data analysis
software system), version 8.0. Recuperado de
www.statsoft.com
Tarazona-Janampa, U.I., Cembella, A.D., Pelayo-Zárate, M.C., Pajares, S., Márquez-Valdelamar,
L.M., Okolodkov, Y.B.,…Durán-Riveroll, L.M.
(2020). Associated bacteria and their effects on
growth and toxigenicity of the dinoflagellate
Prorocentrum lima species complex from epi- benthic substrates along Mexican coasts. Fron- tiers in Marine Science, 7(569), 1-18. https://doi.
org/10.3389/fmars.2020.00569
Ten-Hage, L., Turquet, J., Quod, J.P., y Couté, A.
(2000). Coolia areolata sp. nov. (Dinophyceae),
a new sand-dwelling dinoflagellate from the sou- thwestern Indian Ocean. Phycology, 39, 377-383.
https://doi.org/10.2216/i0031-8884-39-5-377.1
Ternon, E., Paix, B., Thomas, O.P., Briand, J.F., y Culioli, G. (2020). Exploring the role of macroalgal surface metabolites on the settlement of the
benthic dinoflagellate Ostreopsis cf. ovata. Frontiers in Marine Science, 7(683), 1-16. https://doi.
org/10.3389/fmars.2020.00683
Throndsen, J. (1979). Special methods-micromanipulators. En R.J. Stein. (Ed.), Handbook of phycological methods: culture methods and growth
measurements (pp. 139-144). London, UK: Cambridge University Press.
Tibiriçá, C.E.J.A., Sibat, M., Fernandes, L. F., Bilien, G., Chomérat, N., Hess, P., y Mafra Jr., L.L.
(2020). Diversity and toxicity of the genus Coolia Meunier in Brazil, and detection of 44-methyl
gambierone in Coolia tropicalis. Toxins, 12(5),
https://doi.org/10.3390/toxins12050327
Tindall, D.R., y Morton, S.L. (1998). Community
dynamics and physiology of epiphytic/benthic
dinoflagellates associated with ciguatera. En
D.M. Anderson, A.D. Cembella y G. Hallegraeff (Eds.). Physiological ecology of harmful blooms
(pp. 293-314). Heidelberg, Berlin, Germany:
Springer-Verlag.
Tomas, C.R. (1997). Identifying marine phytoplankton. San Diego, CA, USA: Academic Press.
Villegas-Silva, V.A. (2014). Evaluación del potencial
de Sargassum lapazeanum Setchell y N.L. Gardner (Ochrophyta: Fucales, Phaeophyceae) como
fuente de compuestos antibacterianos, antioxidantes y anticoagulantes (Tesis de licenciatura).
UABCS, La Paz, Baja California Sur, México.
Wakeman, K.C., Yamaguchi, A., Roy, M.C., y
Jenke-Kodama, H. (2015). Morphology, phylogeny and novel chemical compounds from Coolia malayensis (Dinophyceae) from Okinawa,
Japan. Harmful Algae, 44, 8-19. https://doi.org/10.1016/j.hal.2015.02.00
Downloads
Published
How to Cite
Issue
Section
License
Copyright (c) 2022 Ana Emilia Ramos Santiago

This work is licensed under a Creative Commons Attribution 4.0 International License.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License 4.0 that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.