Genetics and Morphology Characterize the Dinoflagellate Symbiodinium voratum, n. sp., (Dinophyceae) as the Sole Representative of Symbiodinium Clade E
Dinoflagellates in the genus Symbiodinium are ubiquitous in shallow marine habitats where they commonly exist in symbiosis with cnidarians. Attempts to culture them often retrieve isolates that may not be symbiotic, but instead exist as free‐living species. In particular, cultures of Symbiodinium cl...
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| Published in: | The Journal of eukaryotic microbiology Vol. 61; no. 1; pp. 75 - 94 |
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| Main Authors: | , , , , , , , , , |
| Format: | Journal Article |
| Language: | English |
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Blackwell Publishing Ltd
01-01-2014
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| Abstract | Dinoflagellates in the genus Symbiodinium are ubiquitous in shallow marine habitats where they commonly exist in symbiosis with cnidarians. Attempts to culture them often retrieve isolates that may not be symbiotic, but instead exist as free‐living species. In particular, cultures of Symbiodinium clade E obtained from temperate environments were recently shown to feed phagotrophically on bacteria and microalgae. Genetic, behavioral, and morphological evidence indicate that strains of clade E obtained from the northwestern, southwestern, and northeastern temperate Pacific Ocean as well as the Mediterranean Sea constitute a single species: Symbiodinium voratum n. sp. Chloroplast ribosomal 23S and mitochondrial cytochrome b nucleotide sequences were the same for all isolates. The D1/D2 domains of nuclear ribosomal DNA were identical among Western Pacific strains, but single nucleotide substitutions differentiated isolates from California (USA) and Spain. Phylogenetic analyses demonstrated that S. voratum is well‐separated evolutionarily from other Symbiodinium spp. The motile, or mastigote, cells from different cultures were morphologically similar when observed using light, scanning, and transmission electron microscopy; and the first complete Kofoidian plate formula for a Symbiodinium sp. was characterized. As the largest of known Symbiodinium spp., the average coccoid cell diameters measured among cultured isolates ranged between 12.2 (± 0.2 SE) and 13.3 (± 0.2 SE) μm. Unique among species in the genus, a high proportion (approximately 10–20%) of cells remain motile in culture during the dark cycle. Although S. voratum occurs on surfaces of various substrates and is potentially common in the plankton of coastal areas, it may be incapable of forming stable mutualistic symbioses. |
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| AbstractList | Dinoflagellates in the genus Symbiodinium are ubiquitous in shallow marine habitats where they commonly exist in symbiosis with cnidarians. Attempts to culture them often retrieve isolates that may not be symbiotic, but instead exist as free-living species. In particular, cultures of Symbiodinium clade E obtained from temperate environments were recently shown to feed phagotrophically on bacteria and microalgae. Genetic, behavioral, and morphological evidence indicate that strains of clade E obtained from the northwestern, southwestern, and northeastern temperate Pacific Ocean as well as the Mediterranean Sea constitute a single species: Symbiodinium voratum n. sp. Chloroplast ribosomal 23S and mitochondrial cytochrome b nucleotide sequences were the same for all isolates. The D1/D2 domains of nuclear ribosomal DNA were identical among Western Pacific strains, but single nucleotide substitutions differentiated isolates from California (USA) and Spain. Phylogenetic analyses demonstrated that S. voratum is well-separated evolutionarily from other Symbiodinium spp. The motile, or mastigote, cells from different cultures were morphologically similar when observed using light, scanning, and transmission electron microscopy; and the first complete Kofoidian plate formula for a Symbiodinium sp. was characterized. As the largest of known Symbiodinium spp., the average coccoid cell diameters measured among cultured isolates ranged between 12.2 (± 0.2 SE) and 13.3 (± 0.2 SE) μm. Unique among species in the genus, a high proportion (approximately 10-20%) of cells remain motile in culture during the dark cycle. Although S. voratum occurs on surfaces of various substrates and is potentially common in the plankton of coastal areas, it may be incapable of forming stable mutualistic symbioses. Dinoflagellates in the genus Symbiodinium are ubiquitous in shallow marine habitats where they commonly exist in symbiosis with cnidarians. Attempts to culture them often retrieve isolates that may not be symbiotic, but instead exist as free‐living species. In particular, cultures of Symbiodinium clade E obtained from temperate environments were recently shown to feed phagotrophically on bacteria and microalgae. Genetic, behavioral, and morphological evidence indicate that strains of clade E obtained from the northwestern, southwestern, and northeastern temperate Pacific Ocean as well as the Mediterranean Sea constitute a single species: Symbiodinium voratum n. sp. Chloroplast ribosomal 23S and mitochondrial cytochrome b nucleotide sequences were the same for all isolates. The D1/D2 domains of nuclear ribosomal DNA were identical among Western Pacific strains, but single nucleotide substitutions differentiated isolates from California (USA) and Spain. Phylogenetic analyses demonstrated that S. voratum is well‐separated evolutionarily from other Symbiodinium spp. The motile, or mastigote, cells from different cultures were morphologically similar when observed using light, scanning, and transmission electron microscopy; and the first complete Kofoidian plate formula for a Symbiodinium sp. was characterized. As the largest of known Symbiodinium spp., the average coccoid cell diameters measured among cultured isolates ranged between 12.2 (± 0.2 SE) and 13.3 (± 0.2 SE) μm. Unique among species in the genus, a high proportion (approximately 10–20%) of cells remain motile in culture during the dark cycle. Although S. voratum occurs on surfaces of various substrates and is potentially common in the plankton of coastal areas, it may be incapable of forming stable mutualistic symbioses. Dinoflagellates in the genus Symbiodinium are ubiquitous in shallow marine habitats where they commonly exist in symbiosis with cnidarians. Attempts to culture them often retrieve isolates that may not be symbiotic, but instead exist as free-living species. In particular, cultures of Symbiodinium clade E obtained from temperate environments were recently shown to feed phagotrophically on bacteria and microalgae. Genetic, behavioral, and morphological evidence indicate that strains of clade E obtained from the northwestern, southwestern, and northeastern temperate Pacific Ocean as well as the Mediterranean Sea constitute a single species: Symbiodinium voratum n. sp. Chloroplast ribosomal 23S and mitochondrial cytochrome b nucleotide sequences were the same for all isolates. The D1/D2 domains of nuclear ribosomal DNA were identical among Western Pacific strains, but single nucleotide substitutions differentiated isolates from California (USA) and Spain. Phylogenetic analyses demonstrated that S. voratum is well-separated evolutionarily from other Symbiodinium spp. The motile, or mastigote, cells from different cultures were morphologically similar when observed using light, scanning, and transmission electron microscopy; and the first complete Kofoidian plate formula for a Symbiodinium sp. was characterized. As the largest of known Symbiodinium spp., the average coccoid cell diameters measured among cultured isolates ranged between 12.2 ( plus or minus 0.2 SE) and 13.3 ( plus or minus 0.2 SE) mu m. Unique among species in the genus, a high proportion (approximately 10-20%) of cells remain motile in culture during the dark cycle. Although S. voratum occurs on surfaces of various substrates and is potentially common in the plankton of coastal areas, it may be incapable of forming stable mutualistic symbioses. Dinoflagellates in the genus Symbiodinium are ubiquitous in shallow marine habitats where they commonly exist in symbiosis with cnidarians. Attempts to culture them often retrieve isolates that may not be symbiotic, but instead exist as free‐living species. In particular, cultures of Symbiodinium clade E obtained from temperate environments were recently shown to feed phagotrophically on bacteria and microalgae. Genetic, behavioral, and morphological evidence indicate that strains of clade E obtained from the northwestern, southwestern, and northeastern temperate Pacific Ocean as well as the Mediterranean Sea constitute a single species: Symbiodinium voratum n. sp. Chloroplast ribosomal 23S and mitochondrial cytochrome b nucleotide sequences were the same for all isolates. The D1/D2 domains of nuclear ribosomal DNA were identical among Western Pacific strains, but single nucleotide substitutions differentiated isolates from California ( USA ) and Spain. Phylogenetic analyses demonstrated that S. voratum is well‐separated evolutionarily from other Symbiodinium spp. The motile, or mastigote, cells from different cultures were morphologically similar when observed using light, scanning, and transmission electron microscopy; and the first complete Kofoidian plate formula for a Symbiodinium sp. was characterized. As the largest of known Symbiodinium spp., the average coccoid cell diameters measured among cultured isolates ranged between 12.2 (± 0.2 SE ) and 13.3 (± 0.2 SE ) μm. Unique among species in the genus, a high proportion (approximately 10–20%) of cells remain motile in culture during the dark cycle. Although S. voratum occurs on surfaces of various substrates and is potentially common in the plankton of coastal areas, it may be incapable of forming stable mutualistic symbioses. |
| Author | Lim, An Suk Kang, Nam Seon Yoo, Yeong Du Lee, Sung Yeon Lee, Moo Joon Kim, Hyung Seop LaJeunesse, Todd C. Jeong, Hae Jin Yih, Wonho Yamashita, Hiroshi |
| Author_xml | – sequence: 1 givenname: Hae Jin surname: Jeong fullname: Jeong, Hae Jin organization: School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University, 151-747, Seoul, Korea – sequence: 2 givenname: Sung Yeon surname: Lee fullname: Lee, Sung Yeon organization: School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University, 151-747, Seoul, Korea – sequence: 3 givenname: Nam Seon surname: Kang fullname: Kang, Nam Seon organization: School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University, 151-747, Seoul, Korea – sequence: 4 givenname: Yeong Du surname: Yoo fullname: Yoo, Yeong Du organization: School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University, 151-747, Seoul, Korea – sequence: 5 givenname: An Suk surname: Lim fullname: Lim, An Suk organization: School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University, 151-747, Seoul, Korea – sequence: 6 givenname: Moo Joon surname: Lee fullname: Lee, Moo Joon organization: School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University, 151-747, Seoul, Korea – sequence: 7 givenname: Hyung Seop surname: Kim fullname: Kim, Hyung Seop organization: Department of Oceanography, Kunsan National University, 573-701, Kunsan, Korea – sequence: 8 givenname: Wonho surname: Yih fullname: Yih, Wonho organization: Department of Oceanography, Kunsan National University, 573-701, Kunsan, Korea – sequence: 9 givenname: Hiroshi surname: Yamashita fullname: Yamashita, Hiroshi organization: Seikai National Fisheries Research Institute, Fisheries Research Agency, Fukai-Ohta, 907-0451, Ishigaki Okinawa, Japan – sequence: 10 givenname: Todd C. surname: LaJeunesse fullname: LaJeunesse, Todd C. email: tcl3@psu.edu organization: Department of Biology, 327 Mueller Laboratory, Pennsylvania State University, PA, 16802, University Park, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/24460699$$D View this record in MEDLINE/PubMed |
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| Notes | National Research Foundation/Ministry of Science, ICT & Future Planning - No. NRF-C1ABA001-2010-0020702 ArticleID:JEU12088 ark:/67375/WNG-LH2F3ZGQ-F Fig. S1. Temperate Pacific Ocean and Mediterranean Sea origins of cultured isolates assigned to Symbiodinium clade E and used in this research to investigate genetic, morphological, ecological, and behavioral traits (designated by solid circles). Open white circles represent additional locals where clade E was reported to be cultured from water samples, but these cultures were not investigated in this study. Fig. S2. Consensus Bayesian tree based on 1,814 bp aligned positions of the small subunit (SSU) region, using the GTR + G + I model with Prorocentrum micans as an outgroup taxa. The parameters were as follows: assumed nucleotide frequency with equal; substitution rate matrix with A-C substitutions = 0.0586, A-G substitutions = 0.2383, A-T substitutions = 0.0869, C-G substitutions = 0.0578, C-T substitutions = 0.5156, G-T substitutions = 0.0428; proportion of sites assumed to be invariable = 0.7004; and rates for variable sites assumed to follow a gamma distribution with shape parameter = 0.0800. The branch lengths are proportional to the amount of character changes. The numbers above the branches indicate the Bayesian posterior probability (left) and maximum likelihood (ML) bootstrap values (right). Posterior probabilities ≥ 0.5 are shown. The rDNA sequences of the strains shown in bold were analyzed in this study. Fig. S3. Consensus Bayesian tree based on 853 bp aligned positions of the internal transcribed spacer 1 (ITS1), 5.8s, and internal transcribed spacer 2 (ITS2) regions, using the GTR + G + I model and Akashiwo sanguinea as an outgroup taxa. The parameters were as follows: assumed nucleotide frequency with equal; substitution rate matrix with A-C substitutions = 0.1038, A-G substitutions = 0.2646, A-T substitutions = 0.1320, C-G substitutions = 0.0625, C-T substitutions = 0.3480, G-T substitutions = 0.0892; proportion of sites assumed to be invariable = 0.1153; and rates for variable sites assumed to follow a gamma distribution with shape parameter = 1.5640. The branch lengths are proportional to the amount of character changes. The numbers above the branches indicate the Bayesian posterior probability (left) and maximum likelihood (ML) bootstrap values (right). Posterior probabilities ≥ 0.5 are shown. Strain EU074907 marked with an asterisk represents a combination of other similar species (EU074916, EU074917, EU074919, EU074920, EU074921, EU074922, EU074923, and EU074924). Fig. S4. Partial psbA and psbAncr alignments identify four distinct haplotypes (hap1-hap4). The start of gray areas indicates regions where chromatograms change abruptly from a high quality to non-interpretable multipeak sequences. Fig. S5. Position of the nucleus in mastigotes of SvFL 1. (A-C) light micrographs of flagellated cells and (D-F) corresponding epi-fluorescent micrographs showing the variable location of DAPI stained nuclei. Fig. S6. Scanning electron micrographs of the motile cell of CCMP 421. (A) Apical view showing the rare example of a cell with seven apical plates. (B) Enlarged figure of apical plate in S4. (C) Apical view showing a cell with six apical plates. (D) Enlarged figure of apical plate in S6. All scale bars = 1 μm. Fig. S7. Scanning electron micrographs of motile cells of SvFL 1. (A) Antapical view showing the hyposome. Micrograph showing a rare cell with seven postcingular plates and heptagonal 2″″ plates. (B). Drawing of antapical view of SvFL 1. (C) Micrograph showing an example of a cell with three antapical plates. (D) Drawing of antapical view of SvFL 1. All scale bars = 1 μm. Fig. S8. The pyrenoid (PY) in the cells of isolates (A) SvFL 1 and (B) CCMP 421 possessed two stalks. The thylakoids from associated chloroplast do not intrude. Table S1. Primers and TaqMan probes for qPCR detection of Symbiodinium voratum (clade E). Table S2. Symbiodinium spp. used to test the cross-reactivity of clade E primers and Taqman probe in qPCR detection. Ecological Disturbance Research Program Korea Institute of Marine Science & Technology Promotion/KMLTM istex:8A79EA2EA39D1DF0FA8104F3FCC09874A2BEC602 The National Science Foundation - No. OCE-0928764 Mid-career Researcher Program - No. 2012-R1A2A2A01010987 ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 |
| PMID | 24460699 |
| PQID | 1492686990 |
| PQPubID | 23479 |
| PageCount | 20 |
| ParticipantIDs | proquest_miscellaneous_1500800873 proquest_miscellaneous_1492686990 crossref_primary_10_1111_jeu_12088 pubmed_primary_24460699 wiley_primary_10_1111_jeu_12088_JEU12088 istex_primary_ark_67375_WNG_LH2F3ZGQ_F |
| PublicationCentury | 2000 |
| PublicationDate | January/February 2014 |
| PublicationDateYYYYMMDD | 2014-01-01 |
| PublicationDate_xml | – month: 01 year: 2014 text: January/February 2014 |
| PublicationDecade | 2010 |
| PublicationPlace | United States |
| PublicationPlace_xml | – name: United States |
| PublicationTitle | The Journal of eukaryotic microbiology |
| PublicationTitleAlternate | J. Eukaryot. Microbiol |
| PublicationYear | 2014 |
| Publisher | Blackwell Publishing Ltd |
| Publisher_xml | – name: Blackwell Publishing Ltd |
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D. (e_1_2_7_2_1) 2004; 11 Spector D. L. (e_1_2_7_74_1) 1984 e_1_2_7_90_1 e_1_2_7_73_1 e_1_2_7_94_1 e_1_2_7_50_1 e_1_2_7_71_1 e_1_2_7_92_1 e_1_2_7_25_1 e_1_2_7_31_1 e_1_2_7_52_1 e_1_2_7_77_1 e_1_2_7_23_1 e_1_2_7_33_1 e_1_2_7_54_1 e_1_2_7_75_1 e_1_2_7_96_1 e_1_2_7_21_1 e_1_2_7_35_1 e_1_2_7_56_1 e_1_2_7_37_1 e_1_2_7_58_1 e_1_2_7_79_1 e_1_2_7_39_1 e_1_2_7_6_1 Swofford D (e_1_2_7_81_1) 2000 e_1_2_7_4_1 e_1_2_7_80_1 e_1_2_7_8_1 e_1_2_7_18_1 e_1_2_7_84_1 e_1_2_7_16_1 e_1_2_7_40_1 e_1_2_7_61_1 e_1_2_7_82_1 e_1_2_7_42_1 e_1_2_7_63_1 e_1_2_7_88_1 e_1_2_7_12_1 e_1_2_7_44_1 e_1_2_7_65_1 e_1_2_7_10_1 e_1_2_7_46_1 e_1_2_7_67_1 e_1_2_7_48_1 e_1_2_7_69_1 e_1_2_7_27_1 e_1_2_7_29_1 e_1_2_7_91_1 e_1_2_7_72_1 e_1_2_7_95_1 e_1_2_7_51_1 e_1_2_7_70_1 e_1_2_7_93_1 Fitt W. K. (e_1_2_7_14_1) 1981; 31 e_1_2_7_30_1 e_1_2_7_53_1 e_1_2_7_76_1 e_1_2_7_24_1 e_1_2_7_32_1 LaJeunesse T. C. (e_1_2_7_38_1) 2004; 23 e_1_2_7_55_1 Trench R. K. (e_1_2_7_86_1) 1993; 9 e_1_2_7_22_1 e_1_2_7_34_1 e_1_2_7_57_1 e_1_2_7_20_1 e_1_2_7_36_1 e_1_2_7_59_1 e_1_2_7_78_1 |
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| Snippet | Dinoflagellates in the genus Symbiodinium are ubiquitous in shallow marine habitats where they commonly exist in symbiosis with cnidarians. Attempts to culture... Dinoflagellates in the genus Symbiodinium are ubiquitous in shallow marine habitats where they commonly exist in symbiosis with cnidarians. Attempts to culture... |
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| Title | Genetics and Morphology Characterize the Dinoflagellate Symbiodinium voratum, n. sp., (Dinophyceae) as the Sole Representative of Symbiodinium Clade E |
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