Combined Morphological and Molecular Phylogenetic Analysis of the Genus Tripos (Dinophyceae) from the Persian Gulf

Document Type : Original Article

Authors

1 Department of Marine Biology, Faculty of Marine Sciences and Oceanography, Khorramshahr University of Marine Science and Technology

2 Department of Marine Biology, Faculty of Marine Sciences and Oceanography, Khorramshahr University of Marine Sciences and Technology

Abstract

The genus Tripos (the marine Ceratium) often comprises a major part of micro-phytoplankton in terms of abundance and diversity that plays an important role in annual primary production; however, it has received little attention in the Persian Gulf. The morphology and phylogeny of Tripos furca, T. massiliense, and T. concilians were investigated in the present research. Samples collected from the Persian Gulf were identified morphologically under an inverted microscope, and the SSU rDNA sequence from individual cells was amplified using a polymerase chain reaction. The SSU rDNA sequence was determined for Iranian strains of these species and registered in the GenBank. The results of the phylogenetic analysis indicated the formation of a monophyletic clade of the family Ceratiaceae with high support. In this clade, freshwater species of Ceratium were grouped in a highly supported subclade, and marine species comprised another subclade. These results well demonstrated the separation (divergence) of marine and freshwater species of Ceratium. Altogether, the present results agree with previous studies where a considerable evolutionary distance is suggested for marine and freshwater species and support the formation of two highly distinct monophyletic clades based on SSU rDNA and LSU rDNA fragments and the number of cingular plates.

Keywords

References

Aein Jamshid K, Mohsenizadeh F, Omidi S. (2016). Effects of environmental parameters and nutrients on microalgae communities around the shrimp farm complexes in Bushehr province, in the Persian Gulf. Iranian Journal of Fisheries Sciences. 5 (3): 1044-1054. https://jifro.ir/article-1-2319-en.html.
Accattatis V, Piccini C, Huber P, Metz S, Rueda E, Devercelli M. )2020(. Identifying invaders: the case of Ceratium furcoides (Gonyaulacales, Dinophyceae) in South America. Journal of Phycology. 56(5): 1362-1366. DOI: 10.1111/jpy.13015.
Alemzadeh E, Haddad R, Ahmadi AR. (2014). Phytoplanktons and DNA barcoding: characterization and molecular analysis of phytoplanktons on the Persian Gulf. Iranian Journal of Microbiology. 6 (4): 296-302. PMID: 25802715
Al-Kandari M, Al-Yamani F, Al-Rifaie K. (2009). Marine phytoplankton atlas of Kuwait’s waters. Kuwait Institute for Scientific Research. 351.
Alverson AJ, Jansen RK, Theriot EC. (2007). Bridging the Rubicon: phylogenetic analysis reveals repeated colonizations of marine and fresh waters by thalassiosiroid diatoms. Molecular Phylogenetics and Evolution. 45 (1): 193-210. DOI: 10.1016/j.ympev.2007.03.024.
 Attaran-Fariman G, Khodami S, Bolch CJS. (2011). The cyst-motile stage relationship of three Protoperidinium species from the southeast coast of Iran. Iranian Journal of Fisheries Sciences. 10 (1): 1-12. http://jifro.ir/article-1-120-fa.html.
Attaran-Fariman G, Javid P. (2013). The phylogeny of Heterocapsa sp. (Dinophyceae) isolated from the south coast of Iran during a Cochlodinium polykrikoides bloom. Turkish Journal of Botany. 37(4): 778-783. DOI: 10.3906/bot-1206-40.
Balech E. (1974). El genero 'Protoperidinium'Bergh, 1881 ('Peridinium' Ehrenberg, 1831, partim). Rev. Museo Argentino de Ciencias Naturales Bernardino Rivadavia e Instituto Nacional de Investigación de las Ciencias Naturales. 4: 1-79.
Balech E. (1980). On the thecal morphology of dinoflagellates with special emphasis on cingular and sulcal plates. Anales del Instituto de Ciencias del Mar y Limnologia, Universidad Nacional Autonoma de Mexico. 7: 57-68.
Balech E. 1988. Los dinoflagelados del Atlántico sudoccidental. Publicaciones Especiales. Instituto Espanol de Oceanografia. 1: 1-310.
Brokaw CJ and Wright L. (1963). Bending waves of the posterior flagellum of Ceratium. Science. 142 (3596): 1169-1170. DOI: 1126/science.142.3596.1169.
Culverhouse PF, Williams R, Reguera B, Herry V, González-Gil S. (2003). Do experts make mistakes? A comparison of human and machine identification of dinoflagellates. Marine ecology progress series. 247: 17-25. DOI: 10.3354/MEPS247017.
De Meester L, Gómez A, Okamura B, Schwenk K. (2002). The Monopolization Hypothesis and the Dispersal–gene flow paradoxes in aquatic organisms. Acta oecologica. 23 (3): 121-135.  DOI: 10.1016/S1146-609X(02)01145-1.
Dodge JD and Marshall HG. (1994). Biogeographic analysis of the armored planktonic Dinoflagelate Ceratium in the North Atlantic and adjacent seas 1. Journal of Phycology. 30 (6): 905-922. DOI: 10.1111/j.0022-3646.1994.00905.x.
Dorgham MM. (2013). Plankton research in the ROPME Sea Area, Achievements and Gaps. International journal of environmental research. 7: 767-778. DOI: 10.22059/IJER.2013.656.
Dujardin F. (1841). Histoire naturelle des zoophytes: Infusoires, comprenant la physiologie et la classificatin de ces animaux, et la manière de les étudier à l'aide du microscope. (Vol. 1). Roret. DOI: 10.5962/bhl.title.10127.
Elbrachter M. (1973). Population dynamics of Ceratium in coastal waters of Kiel Bay. Oikos. 15: 43-48. https://cir.nii.ac.jp/crid/1571135650390010624.
Fatemi SMR, Nabavi SMB, Vosoghi G, Fallahi M, Mohammadi M. (20120. The relation between environmental parameters of the Hormuzgan coastline in the Persian Gulf and the occurrence of the first harmful algal bloom of Cochlodinium polykrikoides (Gymnodiniaceae). Iranian Journal of Fisheries Sciences. 11 (3): 475-489. http://dorl.net/dor/20.1001.1.15622916.2012.11.3.3.3.
Figueroa RI, Rengefors K. (2006). Life cycle and sexuality of the freshwater Raphidophyte Gonostomum semen (Raphidophyceae) 1. Journal of Phycology. 42 (4): 859-871. DOI: 10.1111/j.1529-8817.2006.00240.x.
Finlay BJ. (2002). Global dispersal of free-living microbial eukaryote species. Science. 296 (5570): 1061-1063. DOI: 10.1126/science.1070710
Gaston KJ, O'Neill MA. (2004). Automated species identification: why not? Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences. 359 (1444): 655-667. DOI: 10.1098/rstb.2003.1442.
Gómez F, Moreira D, López-García P. (2010). Neoceratium gen. nov., a new genus for all marine species currently assigned to Ceratium (Dinophyceae). Protist. 161 (1): 35-54. DOI: 10.1016/j.protis.2009.06.004.
Gómez F. (2013). Reinstatement of the dinoflagellate genus Tripos to replace Neoceratium, marine species of Ceratium (Dinophyceae, Alveolata). Cicimar Oceánides. 28 (1): 1-22. DOI: 10.37543/oceanides.v28i1.119.
Guiry MD and Guiry GM. AlgaeBase (2017). World-wide electronic publication, National University of Ireland, Galway.
Hamzehei S, Bidokhti AA, Mortazavi MS, Gheiby A, Ebrahimi M, Saraji F. (2012). Field study of the 2008-2009 red tide in the northern Strait of Hormuz. Life Science Journal. 9 (4): 4727-4733.
Hansen G, Daugbjerg N, Henriksen P. (2000). Study of Gymnodinium mikimotoi and Gymnodinium aureolum, comb. nov. (= Gyrodinium aureolum) based on morphology, pigment composition, and molecular data. Journal of Phycology. 36 (2): 394-410. DOI: 10.1046/j.1529-8817.2000.99172.x.
Hasle GR, Syvertsen EE, Steidinger KA, Tangen K, Tomas CR. (1996). Identifying marine diatoms and dinoflagellates. Elsevier. P. 598. DOI: 10.1016/B978-0-12-693015-3.X5000-1.
Hoef-Emden K, Marin B, Melkonian M. (2002). Nuclear and nucleomorph SSU rDNA phylogeny in the Cryptophyta and the evolution of Cryptophyte diversity. Journal of molecular evolution. 55 (2): 161-179. DOI: 10.1007/s00239-002-2313-5.
Holzmann M, Habura A, Giles H, Bowser SS, Pawlowski JAN. (2003). Freshwater foraminiferans were revealed by analysis of environmental DNA samples. Journal of Eukaryotic Microbiology. 50 (2): 135-139. DOI: 10.1111/j.1550-7408.2003.tb00248.x.
Ibrahim AMM. (2014). Marine plankton and Genus Ceratium on the west coast of the Red Sea. Blue Biotechnology Journal. 3(3): 295-341.
IPCC. (2014). Climate Change: Synthesis Report. Contribution of working groups I, II, and III to the fifth assessment report of the intergovernmental panel on climate change [Core Writing Team, Pachauri RK and Meyer LA. IPCC, Geneva, Switzerland. p. 151.
Jacobson DM. (1999). A Brief History of Dinoflagellate Feeding Research. Journal of Eukaryotic Microbiology. 46(4): 376-381. DOI: 10.1111/j.1550-7408.1999.tb04616.x.
Jalilli M and Rezai H. (2010) Composition, abundance and distribution of phytoplankton in the Strait of Hormuz, Persian Gulf. In a first national conference on the biological science of Makran Sea. 30 (2): 97.
John DM. (2012). Marine algae (seaweed) are associated with coral reefs in the Gulf. In: Riegl BM, Purkis SJ (eds) (2012) Coral Reefs of the Gulf. Dordrecht: Springer, Netherlands. 309-335.
Johns DG, Edwards M, Richardson A, Spicer JI. (2003). Increased blooms of a dinoflagellate in the NW Atlantic. Marine Ecology Progress Series. 265: 283-287. DOI: 10.3354/meps265283.
Jorgensen E. (1911). Die Ceratien. Eine kurze Monographie des Gattung Ceratium Schrank. Internationale Revue der gesamten Hydrobiologie und Hydrographie. 4 (2): 1-124.
Katz LA, McManus GB, Snoeyenbos-West OL, Griffin A, Pirog K, Costas B, Foissner W. (2005). Reframing the ‘Everything is everywhere’ debate: evidence for high gene flow and diversity in ciliate morphospecies. Aquatic Microbial Ecology. 41 (1): 55-65. DOI: 10.3354/ame041055.
Kudela RM, Berdalet E, Enevoldsen H, Pitcher G, Raine R, Urban E. (2017). GEOHAB: The Global Ecology and Oceanography of Harmful Algal Blooms Program; motivation, goals, and legacy. Oceanography. 30 (1):12-21. DOI: 10.5670/oceanog.2017.106.
Latz, MI, Nauen, JC, Rohr J. (2004). Bioluminescence response of four species of dinoflagellates to fully developed pipe flow. Journal of Plankton Research. 26 (12): 1529-1546. DOI: 10.1093/plankt/fbh141.
Lee CE and Bell MA. (1999). Causes and consequences of recent freshwater invasions by saltwater animals. Trends in Ecology and Evolution. 14 (7): 284-288. DOI: 10.1016/S0169-5347(99)01596-7.
Lefèvre E, Bardot C, Noël C, Carrias JF, Viscogliosi E, Amblard C, Sime‐Ngando T. (2007). Unveiling fungal zooflagellates as members of freshwater picoeukaryotes: evidence from a molecular diversity study in a deep meromictic lake. Environmental Microbiology. 9 (1): 61-71. DOI: 10.1111/j.1462-2920.2006.01111.x.
Logares R, Shalchian-Tabrizi K, Boltovskoy A, Rengefors K. (2007). Extensive dinoflagellate phylogenies indicate infrequent marine–freshwater transitions. Molecular Phylogenetics and Evolution. 45 (3): 887-903. DOI: 10.1016/j.ympev.2007.08.005.
Lovejoy NR, Albert JS, Crampton WG. (2006). Miocene marine incursions and marine/freshwater transitions: Evidence from Neotropical fishes. Journal of South American Earth Sciences. 21(1-2): 5-13. DOI: 10.1016/j.jsames.2005.07.009.
Methé BA, Hiorns WD, Zehr JP. (1998). Contrasts between marine and freshwater bacterial community composition: analyses of communities in Lake George and six other Adirondack lakes. Limnology and Oceanography. 43 (2): 368-374. DOI: 10.4319/lo.1998.43.2.0368.
Mijares AJ, Sevcik C, Barboza CA, Saavedra JA. (1985). Ichthyotoxism by a paralytic toxin produced by marine dinoflagellates of the genus Ceratium: relationship to fraction β isolated from the sponge Tedania ignis. Toxicon. 23 (2): 221-233. DOI: 10.1016/0041-0101(85)90145-X.
Miller MF and Labandeira CC. (2002). Slow crawl across the salinity divide: delayed colonization of freshwater ecosystems by invertebrates. Geological Society of America. 12: 4-10. DOI: 10.1130/1052-5173(2002)012<0004:SCATSD>2.0.CO;2.
Moreira RA, Rocha O, Santos RM, Laudares-Silva R, Dias ES, Eskinazi-Sant’Anna EM. (2015). First record of Ceratium furcoides (Dinophyta), an invasive species, in a temporary high-altitude lake in the Iron Quadrangle (MG, Southeast Brazil). Brazilian Journal of Biology. 75. DOI: 98-103. 10.1590/1519-6984.08013.
Morton SL, Shuler A, Paternoster J, Fanolua S, Vargo D. (2011). Coastal eutrophication, land use changes, and Ceratium furca (Dinophyceae) blooms in Pago Pago Harbor, American Samoa 2007–2009. Chinese Journal of Oceanology and Limnology. 29 (4): 790-794. DOI: 10.1007/s00343-011-0507-7.
Nielsen TG. (1991). Contribution of zooplankton grazing to the decline of a Ceratium bloom. Limnology and Oceanography. 36 (6): 1091-1106.
Nitzsch CL. (1817). Beitrag zur Infusionenkunde oder Naturbeschreibung der Zerkarien und Bazillarien. Neue Schriften der Naturforschenden Gesellschaft zu Halle. 3: 1-128.
Orellana-Cepeda E, Granados-Machuca C, Serrano-Esquer J. (2002). Ceratium furca: One possible cause of mass mortality of cultured bluefin tuna at Baja California, Mexico. In Proceedings of the Xth International Conference on Harmful Algae. St. Petersburg Beach, Florida, USA. pp. 514-516.
Pawlowski J, Holzmann M. (2002). Molecular phylogeny of Foraminifera a review. European Journal of Protistology. 38(1): 1-10. DOI: 10.1078/0932-4739-00857.
Pitcher GC, Probyn TA. (2011). Anoxia in southern Benguela during the autumn of 2009 and its linkage to a bloom of the dinoflagellate Ceratium balechii. Harmful Algae. 11: 23-32.  DOI: 10.1016/j.hal.2011.07.001
Pizay MD, Lemée R, Simon N, Cras AL, Laugier JP, Dolan JR. (2009). Night and day morphologies in a planktonic dinoflagellate. Protist. 160 (4): 565-575. DOI: 10.1016/j.protis.2009.04.003.
Rabbaniha M, Izadpanahi GH, Mohsenizadeh F, Owfi F. (2012). Comparing of phytoplankton assemblage in inshore and offshore waters of the Persian Gulf (Bushehr province waters). In International conference on land-sea interactions in the coastal zone, Lebanon. 10 pp.
Raine R, White M, Dodge JD. (2002). The summer distribution of net plankton dinoflagellates and their relation to water movements in the NE Atlantic Ocean, west of Ireland. Journal of Plankton Research. 24 (11): 1131-1147. DOI: 10.1093/plankt/24.11.1131.
Reguera B, Velo-Suárez L, Raine R, Park MG. (2012). Dinophysis species: A review. Harmful Algae. 14: 87-106.  DOI: 10.1016/j.hal.2011.10.016.
Rezai H. (1995). Blooms of phytoplankton along the northeastern coast of the Persian Gulf. Iranian Fisheries Research and Training Organization Report. 1: 1-55.
Richards TA, Vepritskiy AA, Gouliamova DE, Nierzwicki‐Bauer SA. (2005). The molecular diversity of freshwater picoeukaryotes from an oligotrophic lake reveals diverse, distinctive, and globally dispersed lineages. Environmental Microbiology. 7 (9): 1413-1425. DOI: 10.1111/j.1462-2920.2005.00828.x.
Saldarriaga JF, Cavalier-Smith T, Menden-Deuer S, Keeling PJ. (2004). Molecular data and the evolutionary history of dinoflagellates. European Journal of Protistology. 40 (1): 85-111. DOI: 10.1016/j.ejop.2003.11.003.
Sato H, Greuet C, Cachon M, Cosson J. (2004). Analysis of the contraction of an organelle using its birefringence: The R-fibre of the Ceratium (Dinoflagellate) flagellum. Cell Biology International. 28 (5): 387-396.  DOI: 10.1016/j.cellbi.2004.03.007.
Scheckenbach F, Wylezich C, Mylnikov AP, Weitere M, Arndt H. (2006).  Molecular comparisons of freshwater and marine isolates of the same morphospecies of heterotrophic flagellates. Applied and Environmental Microbiology. 72 (10): 6638-6643. DOI: 10.1128/AEM.02547-05.
Schiller J. (1937). Dinoflagellatae (Peridinineae) in monographischer Behandlung. In: Rabenhorst L (ed) Kryptogamen-Flora von Deutschland, Österreichs und der Schweiz. Akad Verlag, Leipzig. 10 (3): 1-589.
Schrank FVP. (1793). Mikroskopische Wahrnehmungen. Der Naturforscher (Halle). 27: 26-37. https://www.algaebase.org/search/species/detail/?species_id=56083.
Sheppard C, Al-Husiani M, Al-Jamali F, Al-Yamani F, Baldwin R, Bishop J, Benzoni F, Dutrieux E, Dulvy NK, Durvasula SRV, Jones DA. (2010). The Gulf: a young sea in decline. Marine Pollution Bulletin. 60 (1): 13-38. DOI: 10.1016/j.marpolbul.2009.10.017
Sims PA, Mann DG, Medlin LK. (2006). Evolution of the diatoms: insights from fossil, biological and molecular data. Phycologia. 45(4): 361-402. DOI: 10.2216/05-22.1.
Skovgaard A, Hansen PJ, Stoecker DK. (2000). Physiology of the mixotrophic dinoflagellate Fragilidium subglobosum. I. Effects of phototrophy and irradiance on photosynthesis and carbon content. Marine Ecology Progress Series. 201: 129-136. https://www.jstor.org/stable/24863575.
Smalley GW, Coats DW, Adam EJ. (1999). A new method using fluorescent microspheres to determine grazing on ciliates by the mixotrophic dinoflagellate Ceratium furca. Aquatic Microbial Ecology. 17 (2): 167-179. DOI: 10.3354/ame017167.
Snoke MS, Berendonk TU, Barth D, Lynch M. (2006). Large global effective population sizes in Paramecium. Molecular Biology and Evolution. 23 (12): 2474-2479. DOI: 10.1093/molbev/msl128.
Sournia A. (1967). Le genre Ceratium (Péridinien planctonique) dans le canal du Mozambique. Contribution à une révision mondiale. Vie et milieu/ Laboratoire Arago, Université P. et M. Curie, 18: 375-440. https://www.sudoc.fr/020993137.
Steidinger KA and Tangen K. (1997). Dinoflagellates. In Tomas CR (ed) Identifying Marine Phytoplankton. Elsevier, Academic Press, SanDiego, 387-584.
Sullivan JM and Swift E, (1995). Photo enhancement of bioluminescence capacity in natural and laboratory populations of the autotrophic dinoflagellate Ceratium fusus (Ehrenb.) Dujardin. Journal of Geophysical Research: Oceans. 100 (4): 6565-6574. DOI: 10.1029/94JC01511.
Tamadoni Jahrom S, Sofiman Othman A, Saraji F, Abdolalian E, Moezzi M, Roohani K. (2011). Identification and molecular phylogeny of the dinoflagellate (Cochlodinium polykrikoides) from the Persian Gulf. International Journal of Review in Life Science. 1 (4): 193-200.
Tan TH, Leaw CP, Leong SCY, Lim LP, Chew SM, Teng ST, Lim PT. (2016). Marine micro-phytoplankton of Singapore, with a review of harmful microalgae in the region. Raffles Bulletin of Zoology. 34: 78-96. http://ir.unimas.my/id/eprint/12646.
Teen LP, GireS USUP, Pin LC. (2012). Harmful algal blooms in Malaysian waters. Sains Malaysiana. 41 (12): 1509-1515. http://ir.unimas.my/id/eprint/2272.
Tunin-Ley A, Ibañez F, Labat JP, Zingone A, Lemée R. (2009). Phytoplankton biodiversity and NW Mediterranean Sea warming: changes in the dinoflagellate genus Ceratium in the 20th century. Marine Ecology Progress Series. 375: 85-99. DOI: 10.3354/meps07730.
Vermeij GJ and Wesselingh FP. (2002). Neogastropod mollusks from the Miocene of western Amazonia, with comments on marine to freshwater transitions in mollusks. Journal of Paleontology. 76 (2): 265-270. DOI: 10.1666/0022-3360(2002)076<0265:NMFTMO>2.0.CO;2.
Warnecke F, Amann R, Pernthaler J. (2004). Actinobacterial 16S rRNA genes from freshwater habitats cluster in four distinct lineages. Environmental Microbiology. 6 (3): 242-253. DOI: 10.1111/j.1462-2920.2004.00561.x.
Weiler CS. (1980). Population structure and in situ division rates of Ceratium in oligotrophic waters of the North Pacific central gyre. Limnology and Oceanography. 25 (4): 610-619. DOI: 10.4319/lo.1980.25.4.0610.
Zarei Darki B and Krakhmalnyi A. (2017). Report of armored dinoflagellates from waters surrounding Hormuz island (the Strait of Hormuz). Iranian Journal of Botany. 23 (2): 145-160. DOI: 10.22092/IJB.2017.114012.
Zingone A and Enevoldsen HO. (2000). The diversity of harmful algal blooms: a challenge for science and management. Ocean and Coastal Management. 43 (8-9): 725-748. DOI: 10.1016/S0964-5691(00)00056-9.
Zwart G, Hiorns WD, Methé BA, van Agterveld MP, Huismans R, Nold SC, Zehr JP, Laanbroek HJ. (1998). Nearly identical 16S rRNA sequences recovered from lakes in North America and Europe indicate the existence of clades of globally distributed freshwater bacteria. Systematic and Applied Microbiology. 21 (4): 546-556. DOI: 10.1016/S0723-2020(98)80067-2.
Zwart G, Crump BC, Kamst-van Agterveld MP, Hagen F, Han SK. (2002). Typical freshwater bacteria: an analysis of available 16S rRNA gene sequences from plankton of lakes and rivers. Aquatic Microbial Ecology. 28 (2): 141-155. DOI: 10.3354/ame028141.
Plant, Algae, and Environment
Volume 7, Issue 1
2023
Pages 969-987

Files

Share

How to cite

Statistics