Pentaplacodinium saltonense gen. et sp. nov. (Dinophyceae) and its relationship to the cyst-defined genus Operculodinium and yessotoxin-producing Protoceratium reticulatum

Kenneth Neil Mertens; M. Consuelo Carbonell-Moore; Vera Pospelova; Martin J. Head; Andrea Highfield; Declan Schroeder; Haifeng Gu; Karl B. Andree; Margarita Fernandez; Aika Yamaguchi; Yoshihito Takano; Kazumi Matsuoka; Elisabeth Nézan; Gwenael Bilien; Yuri Okolodkov; Kazuhiko Koike; Mona Hoppenrath; Maya Pfaff; Grant Pitcher; Abdulrahman Al-Muftah; André Rochon; Po Teen Lim; Chui Pin Leaw; Zhen Fei Lim; Marianne Ellegaard

doi:10.1016/j.hal.2017.12.003

Pentaplacodinium saltonense gen. et sp. nov. (Dinophyceae) and its relationship to the cyst-defined genus Operculodinium and yessotoxin-producing Protoceratium reticulatum

Kenneth Neil Mertens, M. Consuelo Carbonell-Moore, Vera Pospelova, Martin J. Head, Andrea Highfield, Declan Schroeder, Haifeng Gu, Karl B. Andree, Margarita Fernandez, Aika Yamaguchi, Yoshihito Takano, Kazumi Matsuoka, Elisabeth Nézan, Gwenael Bilien, Yuri Okolodkov, Kazuhiko Koike, Mona Hoppenrath, Maya Pfaff, Grant Pitcher, Abdulrahman Al-MuftahAndré Rochon, Po Teen Lim, Chui Pin Leaw, Zhen Fei Lim, Marianne Ellegaard

Research output: Contribution to journal › Article › peer-review

10 Scopus citations

Abstract

Strains of a dinoflagellate from the Salton Sea, previously identified as Protoceratium reticulatum and yessotoxin producing, have been reexamined morphologically and genetically and Pentaplacodinium saltonense n. gen. et sp. is erected to accommodate this species. Pentaplacodinium saltonense differs from Protoceratium reticulatum (Claparède et Lachmann 1859) Bütschli 1885 in the number of precingular plates (five vs. six), cingular displacement (two widths vs. one), and distinct cyst morphology. Incubation experiments (excystment and encystment) show that the resting cyst of Pentaplacodinium saltonense is morphologically most similar to the cyst-defined species Operculodinium israelianum (Rossignol, 1962) Wall (1967) and O. psilatum Wall (1967). Collections of comparative material from around the globe (including Protoceratium reticulatum and the genus Ceratocorys) and single cell PCR were used to clarify molecular phylogenies. Variable regions in the LSU (three new sequences), SSU (12 new sequences) and intergenic ITS 1–2 (14 new sequences) were obtained. These show that Pentaplacodinium saltonense and Protoceratium reticulatum form two distinct clades. Pentaplacodinium saltonense forms a monophyletic clade with several unidentified strains from Malaysia. LSU and SSU rDNA sequences of three species of Ceratocorys (C. armata, C. gourreti, C. horrida) from the Mediterranean and several other unidentified strains from Malaysia form a well-supported sister clade. The unique phylogenetic position of an unidentified strain from Hawaii is also documented and requires further examination. In addition, based on the V9 SSU topology (bootstrap values >80%), specimens from Elands Bay (South Africa), originally described as Gonyaulax grindleyi by Reinecke (1967), cluster with Protoceratium reticulatum. The known range of Pentaplacodinium saltonense is tropical to subtropical, and its cyst is recorded as a fossil in upper Cenozoic sediments. Protoceratium reticulatum and Pentaplacodinium saltonense seem to inhabit different niches: motile stages of these dinoflagellates have not been found in the same plankton sample.

Original language	English (US)
Pages (from-to)	57-77
Number of pages	21
Journal	Harmful Algae
Volume	71
DOIs	https://doi.org/10.1016/j.hal.2017.12.003
State	Published - Jan 2018

Bibliographical note

Funding Information:
V.P. and M.J.H. each acknowledge support from a Discovery Grant of the Natural Sciences and Engineering Research Council of Canada (NSERC) . K.B.A. and M.F. were supported by the Instituto Nacional de Investigación y Tecnología Agraría y Alimentaria of the Spanish Government (project RTA2005-00109-00-00). CINVESTAV, Merida is thanked for supplying information about the Yucatan samples. Beatriz Paz is acknowledged for interesting discussions on toxicity. Anke Kremp, Maija Hutunnen, Jacob Larsen, Paul Hargraves and Ximena Vivanco kindly provided plankton samples. Nancy Lewis and Margaret Beaton generously shared information on strains from Nova Scotia, Canada. Captain Brown, crew of the MSV Strickland, Ms. Sarah Thornton, and EOS313-2010 (University of Victoria) students are all thanked for their participation in sediment sample collection. Paul Hargraves kindly provided SEM images of P. saltonense from cultures established from the Indian River Lagoon.[SS]

Keywords

Ceratocorys
Cribroperidinioideae
Operculodinium
Pentaplacodinium
Precingular plates
Protoceratium
Salton Sea

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Mertens, K. N., Carbonell-Moore, M. C., Pospelova, V., Head, M. J., Highfield, A., Schroeder, D., Gu, H., Andree, K. B., Fernandez, M., Yamaguchi, A., Takano, Y., Matsuoka, K., Nézan, E., Bilien, G., Okolodkov, Y., Koike, K., Hoppenrath, M., Pfaff, M., Pitcher, G., ... Ellegaard, M. (2018). Pentaplacodinium saltonense gen. et sp. nov. (Dinophyceae) and its relationship to the cyst-defined genus Operculodinium and yessotoxin-producing Protoceratium reticulatum. Harmful Algae, 71, 57-77. https://doi.org/10.1016/j.hal.2017.12.003

Pentaplacodinium saltonense gen. et sp. nov. (Dinophyceae) and its relationship to the cyst-defined genus Operculodinium and yessotoxin-producing Protoceratium reticulatum. / Mertens, Kenneth Neil; Carbonell-Moore, M. Consuelo; Pospelova, Vera; Head, Martin J.; Highfield, Andrea; Schroeder, Declan; Gu, Haifeng; Andree, Karl B.; Fernandez, Margarita; Yamaguchi, Aika; Takano, Yoshihito; Matsuoka, Kazumi; Nézan, Elisabeth; Bilien, Gwenael; Okolodkov, Yuri; Koike, Kazuhiko; Hoppenrath, Mona; Pfaff, Maya; Pitcher, Grant; Al-Muftah, Abdulrahman; Rochon, André; Lim, Po Teen; Leaw, Chui Pin; Lim, Zhen Fei; Ellegaard, Marianne.

In: Harmful Algae, Vol. 71, 01.2018, p. 57-77.

Research output: Contribution to journal › Article › peer-review

Mertens, KN, Carbonell-Moore, MC, Pospelova, V, Head, MJ, Highfield, A, Schroeder, D, Gu, H, Andree, KB, Fernandez, M, Yamaguchi, A, Takano, Y, Matsuoka, K, Nézan, E, Bilien, G, Okolodkov, Y, Koike, K, Hoppenrath, M, Pfaff, M, Pitcher, G, Al-Muftah, A, Rochon, A, Lim, PT, Leaw, CP, Lim, ZF & Ellegaard, M 2018, 'Pentaplacodinium saltonense gen. et sp. nov. (Dinophyceae) and its relationship to the cyst-defined genus Operculodinium and yessotoxin-producing Protoceratium reticulatum', Harmful Algae, vol. 71, pp. 57-77. https://doi.org/10.1016/j.hal.2017.12.003

Mertens, Kenneth Neil ; Carbonell-Moore, M. Consuelo ; Pospelova, Vera ; Head, Martin J. ; Highfield, Andrea ; Schroeder, Declan ; Gu, Haifeng ; Andree, Karl B. ; Fernandez, Margarita ; Yamaguchi, Aika ; Takano, Yoshihito ; Matsuoka, Kazumi ; Nézan, Elisabeth ; Bilien, Gwenael ; Okolodkov, Yuri ; Koike, Kazuhiko ; Hoppenrath, Mona ; Pfaff, Maya ; Pitcher, Grant ; Al-Muftah, Abdulrahman ; Rochon, André ; Lim, Po Teen ; Leaw, Chui Pin ; Lim, Zhen Fei ; Ellegaard, Marianne. / Pentaplacodinium saltonense gen. et sp. nov. (Dinophyceae) and its relationship to the cyst-defined genus Operculodinium and yessotoxin-producing Protoceratium reticulatum. In: Harmful Algae. 2018 ; Vol. 71. pp. 57-77.

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title = "Pentaplacodinium saltonense gen. et sp. nov. (Dinophyceae) and its relationship to the cyst-defined genus Operculodinium and yessotoxin-producing Protoceratium reticulatum",

abstract = "Strains of a dinoflagellate from the Salton Sea, previously identified as Protoceratium reticulatum and yessotoxin producing, have been reexamined morphologically and genetically and Pentaplacodinium saltonense n. gen. et sp. is erected to accommodate this species. Pentaplacodinium saltonense differs from Protoceratium reticulatum (Clapar{\`e}de et Lachmann 1859) B{\"u}tschli 1885 in the number of precingular plates (five vs. six), cingular displacement (two widths vs. one), and distinct cyst morphology. Incubation experiments (excystment and encystment) show that the resting cyst of Pentaplacodinium saltonense is morphologically most similar to the cyst-defined species Operculodinium israelianum (Rossignol, 1962) Wall (1967) and O. psilatum Wall (1967). Collections of comparative material from around the globe (including Protoceratium reticulatum and the genus Ceratocorys) and single cell PCR were used to clarify molecular phylogenies. Variable regions in the LSU (three new sequences), SSU (12 new sequences) and intergenic ITS 1–2 (14 new sequences) were obtained. These show that Pentaplacodinium saltonense and Protoceratium reticulatum form two distinct clades. Pentaplacodinium saltonense forms a monophyletic clade with several unidentified strains from Malaysia. LSU and SSU rDNA sequences of three species of Ceratocorys (C. armata, C. gourreti, C. horrida) from the Mediterranean and several other unidentified strains from Malaysia form a well-supported sister clade. The unique phylogenetic position of an unidentified strain from Hawaii is also documented and requires further examination. In addition, based on the V9 SSU topology (bootstrap values >80%), specimens from Elands Bay (South Africa), originally described as Gonyaulax grindleyi by Reinecke (1967), cluster with Protoceratium reticulatum. The known range of Pentaplacodinium saltonense is tropical to subtropical, and its cyst is recorded as a fossil in upper Cenozoic sediments. Protoceratium reticulatum and Pentaplacodinium saltonense seem to inhabit different niches: motile stages of these dinoflagellates have not been found in the same plankton sample.",

keywords = "Ceratocorys, Cribroperidinioideae, Operculodinium, Pentaplacodinium, Precingular plates, Protoceratium, Salton Sea",

author = "Mertens, {Kenneth Neil} and Carbonell-Moore, {M. Consuelo} and Vera Pospelova and Head, {Martin J.} and Andrea Highfield and Declan Schroeder and Haifeng Gu and Andree, {Karl B.} and Margarita Fernandez and Aika Yamaguchi and Yoshihito Takano and Kazumi Matsuoka and Elisabeth N{\'e}zan and Gwenael Bilien and Yuri Okolodkov and Kazuhiko Koike and Mona Hoppenrath and Maya Pfaff and Grant Pitcher and Abdulrahman Al-Muftah and Andr{\'e} Rochon and Lim, {Po Teen} and Leaw, {Chui Pin} and Lim, {Zhen Fei} and Marianne Ellegaard",

note = "Funding Information: V.P. and M.J.H. each acknowledge support from a Discovery Grant of the Natural Sciences and Engineering Research Council of Canada (NSERC) . K.B.A. and M.F. were supported by the Instituto Nacional de Investigaci{\'o}n y Tecnolog{\'i}a Agrar{\'i}a y Alimentaria of the Spanish Government (project RTA2005-00109-00-00). CINVESTAV, Merida is thanked for supplying information about the Yucatan samples. Beatriz Paz is acknowledged for interesting discussions on toxicity. Anke Kremp, Maija Hutunnen, Jacob Larsen, Paul Hargraves and Ximena Vivanco kindly provided plankton samples. Nancy Lewis and Margaret Beaton generously shared information on strains from Nova Scotia, Canada. Captain Brown, crew of the MSV Strickland, Ms. Sarah Thornton, and EOS313-2010 (University of Victoria) students are all thanked for their participation in sediment sample collection. Paul Hargraves kindly provided SEM images of P. saltonense from cultures established from the Indian River Lagoon.[SS] ",

year = "2018",

month = jan,

doi = "10.1016/j.hal.2017.12.003",

language = "English (US)",

volume = "71",

pages = "57--77",

journal = "Harmful Algae",

issn = "1568-9883",

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T1 - Pentaplacodinium saltonense gen. et sp. nov. (Dinophyceae) and its relationship to the cyst-defined genus Operculodinium and yessotoxin-producing Protoceratium reticulatum

AU - Mertens, Kenneth Neil

AU - Carbonell-Moore, M. Consuelo

AU - Pospelova, Vera

AU - Head, Martin J.

AU - Highfield, Andrea

AU - Schroeder, Declan

AU - Gu, Haifeng

AU - Andree, Karl B.

AU - Fernandez, Margarita

AU - Yamaguchi, Aika

AU - Takano, Yoshihito

AU - Matsuoka, Kazumi

AU - Nézan, Elisabeth

AU - Bilien, Gwenael

AU - Okolodkov, Yuri

AU - Koike, Kazuhiko

AU - Hoppenrath, Mona

AU - Pfaff, Maya

AU - Pitcher, Grant

AU - Al-Muftah, Abdulrahman

AU - Rochon, André

AU - Lim, Po Teen

AU - Leaw, Chui Pin

AU - Lim, Zhen Fei

AU - Ellegaard, Marianne

N1 - Funding Information: V.P. and M.J.H. each acknowledge support from a Discovery Grant of the Natural Sciences and Engineering Research Council of Canada (NSERC) . K.B.A. and M.F. were supported by the Instituto Nacional de Investigación y Tecnología Agraría y Alimentaria of the Spanish Government (project RTA2005-00109-00-00). CINVESTAV, Merida is thanked for supplying information about the Yucatan samples. Beatriz Paz is acknowledged for interesting discussions on toxicity. Anke Kremp, Maija Hutunnen, Jacob Larsen, Paul Hargraves and Ximena Vivanco kindly provided plankton samples. Nancy Lewis and Margaret Beaton generously shared information on strains from Nova Scotia, Canada. Captain Brown, crew of the MSV Strickland, Ms. Sarah Thornton, and EOS313-2010 (University of Victoria) students are all thanked for their participation in sediment sample collection. Paul Hargraves kindly provided SEM images of P. saltonense from cultures established from the Indian River Lagoon.[SS]

PY - 2018/1

Y1 - 2018/1

N2 - Strains of a dinoflagellate from the Salton Sea, previously identified as Protoceratium reticulatum and yessotoxin producing, have been reexamined morphologically and genetically and Pentaplacodinium saltonense n. gen. et sp. is erected to accommodate this species. Pentaplacodinium saltonense differs from Protoceratium reticulatum (Claparède et Lachmann 1859) Bütschli 1885 in the number of precingular plates (five vs. six), cingular displacement (two widths vs. one), and distinct cyst morphology. Incubation experiments (excystment and encystment) show that the resting cyst of Pentaplacodinium saltonense is morphologically most similar to the cyst-defined species Operculodinium israelianum (Rossignol, 1962) Wall (1967) and O. psilatum Wall (1967). Collections of comparative material from around the globe (including Protoceratium reticulatum and the genus Ceratocorys) and single cell PCR were used to clarify molecular phylogenies. Variable regions in the LSU (three new sequences), SSU (12 new sequences) and intergenic ITS 1–2 (14 new sequences) were obtained. These show that Pentaplacodinium saltonense and Protoceratium reticulatum form two distinct clades. Pentaplacodinium saltonense forms a monophyletic clade with several unidentified strains from Malaysia. LSU and SSU rDNA sequences of three species of Ceratocorys (C. armata, C. gourreti, C. horrida) from the Mediterranean and several other unidentified strains from Malaysia form a well-supported sister clade. The unique phylogenetic position of an unidentified strain from Hawaii is also documented and requires further examination. In addition, based on the V9 SSU topology (bootstrap values >80%), specimens from Elands Bay (South Africa), originally described as Gonyaulax grindleyi by Reinecke (1967), cluster with Protoceratium reticulatum. The known range of Pentaplacodinium saltonense is tropical to subtropical, and its cyst is recorded as a fossil in upper Cenozoic sediments. Protoceratium reticulatum and Pentaplacodinium saltonense seem to inhabit different niches: motile stages of these dinoflagellates have not been found in the same plankton sample.

AB - Strains of a dinoflagellate from the Salton Sea, previously identified as Protoceratium reticulatum and yessotoxin producing, have been reexamined morphologically and genetically and Pentaplacodinium saltonense n. gen. et sp. is erected to accommodate this species. Pentaplacodinium saltonense differs from Protoceratium reticulatum (Claparède et Lachmann 1859) Bütschli 1885 in the number of precingular plates (five vs. six), cingular displacement (two widths vs. one), and distinct cyst morphology. Incubation experiments (excystment and encystment) show that the resting cyst of Pentaplacodinium saltonense is morphologically most similar to the cyst-defined species Operculodinium israelianum (Rossignol, 1962) Wall (1967) and O. psilatum Wall (1967). Collections of comparative material from around the globe (including Protoceratium reticulatum and the genus Ceratocorys) and single cell PCR were used to clarify molecular phylogenies. Variable regions in the LSU (three new sequences), SSU (12 new sequences) and intergenic ITS 1–2 (14 new sequences) were obtained. These show that Pentaplacodinium saltonense and Protoceratium reticulatum form two distinct clades. Pentaplacodinium saltonense forms a monophyletic clade with several unidentified strains from Malaysia. LSU and SSU rDNA sequences of three species of Ceratocorys (C. armata, C. gourreti, C. horrida) from the Mediterranean and several other unidentified strains from Malaysia form a well-supported sister clade. The unique phylogenetic position of an unidentified strain from Hawaii is also documented and requires further examination. In addition, based on the V9 SSU topology (bootstrap values >80%), specimens from Elands Bay (South Africa), originally described as Gonyaulax grindleyi by Reinecke (1967), cluster with Protoceratium reticulatum. The known range of Pentaplacodinium saltonense is tropical to subtropical, and its cyst is recorded as a fossil in upper Cenozoic sediments. Protoceratium reticulatum and Pentaplacodinium saltonense seem to inhabit different niches: motile stages of these dinoflagellates have not been found in the same plankton sample.

KW - Ceratocorys

KW - Cribroperidinioideae

KW - Operculodinium

KW - Pentaplacodinium

KW - Precingular plates

KW - Protoceratium

KW - Salton Sea

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