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Phylogeny of the psbC Gene, Coding a Photosystem II Component CP43, Suggests Separate Origins for the Peridinin- and Fucoxanthin Derivative-Containing Plastids of Dinoflagellates

Posted on: Thursday, 10 March 2005, 03:00 CST

Recently, the evolutionary relationship between peridinin- and fucoxanthin derivative (19'-hexanoyloxy-fucoxanthin and 19'- butanoyloxy-fucoxanthin)-containing plastids in dinoflagellates has become a controversial issue. It was widely accepted that the peridinin- and the fucoxanthin derivative-type plastids originated from independent photosynthetic organisms: the former type from a red alga through secondary endosymbiosis, and the latter from a haptophyte through tertiary endosymbiosis. However, a recent phylogenetic analysis using two plastid-encoded genes, psaA (encoding the P700 chlorophyll a apoprotein of photosystem I) and psbA (encoding the D1 protein of photosystem II) has suggested that the two types of dinoflagellate plastids share a single common haptophyte ancestor. In the present study, nucleotide sequences of another representative plastid gene, psbC (coding the CP43 of photosystem II), from both peridinin- and fucoxanthin derivative- containing dinoflagellates were determined using the reverse transcription polymerase chain reaction, cloning and sequencing for phylogenetic analysis. The phylogenetic tree showed that the peridinin- and fucoxanthin derivative-type species of dinoflagellates were not monophyletic, although both of them were placed within the monophyletic clade of other chlorophyll-a/c- containing organisms (a cryptophyte, a heterokont and haptophytes) and red algae. Furthermore, the fucoxanthin derivative-type species had phylogenetic affinity with haptophytes, whereas the peridinin- type did not. These results support the conventional view of separate origins for the peridinin- and fucoxanthin derivative-type plastids of dinoflagellates.

INTRODUCTION

In the unicellular eukaryotic algal group, dinoflagellates, there is a great diversity of plastids with respect to pigment composition and ultrastructure, unlike other groups of photosynthetic eukaryotes (such as red algae, green algae, heterokonts, cryptophytes, euglenophytes, haptophytes, etc.). This diversity is thought to have resulted from various independent endosymbiotic events in which photosynthetic organisms have been engulfed by host dinoflagellates.

Most dinoflagellate plastids contain chlorophyll-a and -C^sub 2^ with peridinin as the major carotenoid, and are surrounded by three membranes (Dodge 1975, 1989; Jeffrey 1989). Along with the pigment composition and plastic! membrane structure, recent phylogenetic analyses based on several plastid-encoded and nuclear-encoded plastid-targeted genes have supported a hypothesis that this typical type of plastid with peridinin arose through a secondary endosymbiosis in which a red alga was engulfed by a heterotrophic host (Takishita & Uchida 1999; Zhang et al. 1999, 2000; Fast et al. 2001; Ishida & Green 2002).

On the other hand, several minor groups of photosynthetic dinoflagellates have plastids that lack peridinin but have a pigment composition and ultrastructure similar to those of other algal groups. One of these anomalously pigmented types of plastids contains chlorophyll-a, -C^sub 1^, -C^sub 2^ and fucoxanthin derivatives (19'-hexanoyloxy-fucoxanthin and 19'- butanoyloxyfucoxanthin) as the major pigments (Tangen & Bjornland 1981; Bjornland & Liaaen-Jensen 1989; Jeffrey 1989; Suzuki & Ishimaru 1992; Hansen et al. 2000) and is found only in the three dinoflagellate genera Karenia Gert Hansen & Moestrup, Karlodinium Larsen (Daugbjerg et al. 2000) and Takayama de Salas, Bolch, Botes & Hallegraeff (de Salas et al. 2003). The pigment composition, together with the plastid ultrastructure, of these dinoflagellate genera resembles that of some haptophyte species (Steidinger et al. 1978; Kite & Dodge 1985, 1988; Bjornland 1990). The phylogenetic analyses based on plastid-encoded genes [plastid small-subunit ribosomal DNA (rDNA) and rbcL encoding the large subunit of form I- type RuBisCO] and a nuclear-encoded plastid-targeted gene (psbO encoding oxygen-evolving enhancer 1 protein) have also demonstrated that the plastids of the fucoxanthin derivative-containing dinoflagellates and haptophytes are closely related (Takishita et al. 1999, 2000; Tengs et al. 2000; Ishida & Green 2002). Thus, all these data have led to the widely accepted conclusion that the fucoxanthin derivative-type plastids originated from a haptophyte endosymbiont. Because the plastids of haptophytes are themselves thought to be secondary in origin (Gibbs 1981; Cavalier-Smith 1993; Medlin et al. 1997), it is reasonable to assume that the fucoxanthin derivative-type plastids resulted in a tertiary endosymbiosis.

Gene phylogenies based on nuclear large- and small-subunit rDNA sequences of dinoflagellates have shown that the peridinin-type species are not monophyletic, but widely distributed within the diversity of dinoflagellates (Saunders et al. 1997; Daugbjerg et al. 2000; Saldarriaga et al. 2001 ; Takishita et al. 2002). Thus, it is highly likely that this type of plastid was present in the common ancestor of most (and perhaps all) dinoflagellates. In contrast, fucoxanthin derivative-containing species, as well as other anomalously pigmented ones, constitute a single clade within the diversity of peridinin-containing dinoflagellates (Saunders et al. 1997; Daugbjerg et al. 2000; Inagaki et al. 2000; Tengs et al. 2000; Saldarriaga et al 2001; Takishita et al. 2002), implying that the fucoxanthin derivative-containing dinoflagellates may have originally possessed the peridinin-type plastids and lost them subsequently, followed by the adoption of new plastids from a haptophyte alga (Tengs et al. 2000; Saldarriaga et al. 2001).

However, Yoon et al. (2002) challenged the above view on the dinoflagellate plastid evolution in a phylogenetic study of the plastid genes psaA encoding the P700 chlorophyll-aapoprotein of photosystem I and psbA encoding the D1 protein of photosystem II. The combined psaA + psbA trees have shown robust support for the monophyly of peridinin- and fucoxanthin derivative-containing dinoflagellates as sisters to the haptophytes. Based on this result, Yoon et al. (2002) concluded that the plastids of peridinin- and fucoxanthin derivative-containing dinoflagellates originated from a single common ancestor of a haptophyte alga through a tertiary endosymbiosis before the split of these two types, and the fucoxanthin derivative-type was recognized as the primitive form of the dinoflagellate plastids.

To obtain a more reliable picture of the evolution of peridinin- and fucoxanthin derivative-type plastids of dinoflagellates, additional analyses using other genetic markers would be desirable. In the present study, we isolated another representative plastid gene psbC encoding the CP43 of photosystem II from both peridinin- and fucoxanthin derivative-type dinoflagellates, and also from haptophytes. To avoid amplifying the possible pseudogenes of psbC, which have been reported in Heterocapsa triquetra Stein (Zhang et al. 2001), the reverse transcription polymerase chain reaction (RT- PCR) method was applied, and then phylogenetic analyses based on the psbC gene sequences from various photosynthetic organisms were performed to re-examine the evolutionary origin and the relationship of the peridinin- and the fucoxanthin derivative-type plastids of dinoflagellates.

MATERIAL AND METHODS

Culture strains

Symbiodinium Freudenthal strains PSPl-05, P083-2 and HPiH-2 have previously been isolated by our group (Carlos et al. 1999; lshikura et al. 2004). Symbiodinium strains CS-156 and CS-161 were obtained from the Australia's Commonwealth Scientific and Industrial Research Organization (CSIRO) Collection of Living Microalgae. Symbiodinium strains JCUCS-I and JCUSG-I were isolated from a jellyfish and a soft coral, respectively, in Australia (Carlos et al. 1999). All strains were grown according to Carlos et al. (1999) and lshikura et al. (2004). Other dinoflagellate and haptophyte species were obtained from various culture collections: Gymnodinium impudicum (Fraga & Bravo) Gert Hansen & Moestrup CCMP2214, Gymnodinium simplex (Lohmann) Kofoid & Swezy CCMP419, Karenla brevis (Davis) Gert Hansen & Moestrup CCMP2229, Karlodinium micrum (Leadbeater & Dodge) Larsen CCMP415 and Lingulodinium polyedrum (Stein) Dodge CCMPl738 from the Provasoli-Guillard National Center for Culture of Marine Phytoplankton (CCMP); Alexandrium catenella Balech NIES674, Amphidinum carterae Hulburt NIES331, Karenia mikimotoi (Miyake & Kominami ex Oda) Gert Hansen & Moestrup NIES680, Prorocentrum micans Ehrenberg NIES218 and Scrippsiella trochoidea (Stein) Loeblich III NIES369 from the National Institute for Environmental Studies (NIES); and Akashiwo sanguined (Hirasaka) Gert Hansen & Moestrup MBICl 1145, Polarella glacialis Montresor, Procaccini & Stoecker MBIC10565, Prorocentrum dentatum Stein MBICl 1146, Prorocentrum triestinum Schiller MBICl 1147, Pavlova Butcher sp. MBIC10389 and Gephyrocapsa oceanica Kamptner MBICl 1100 from the Marine Biotechnology Institute Culture Collection (MBIC). They were grown according to the protocols of the individual culture collections.

Total RNA extraction

Cells were harvestedfrom 100-150 ml culture of each strain by centrifugation (5000 g, 5 min, 4C). Total RNA was extracted using the Absolutely RNA RT-PCR Miniprep Kit (Stratagene, La Jolla, CA, USA) after homogenizing the cell pellets with glass beads in the lysis buffer from this kit.

RT-PCR amplification

Synthesis of complementary DNA (cDNA) from total RNA and PCR amplification using the cDNA as a template were performed using Superscript II RNase H reverse transcriptase (Invitrogen, Carlsbad, CA, USA) and TaKaRa Ex Taq (TaKaRa, Tokyo, Japan) according to the respective manufacturers' instructions. The psbC genes were amplified using a set of primers (forward: 5'-TGGTGGWSIGGIAAYGCIMG- 3' and reverse: 5'-GGIGCRTGIGTCATRTAYTC-3'), under the following thermal cycle conditions: 30 cycles of 1 min at 94C, 1 min at 58C and 2 min at 72C, followed by a final elongation step of 10 min at 72C. The amplified products were confirmed on 1.0% agarose by gel electrophoresis.

Cloning and sequencing

The PCR-amplified DNA fragments were cloned into the pCR2.1 vector of the TOPO TA Cloning Kit (Invitrogen) and sequenced with an ABI PRISM 3700 DNA Analyzer (Applied Biosystems, Foster City, CA, USA) using a BigDye Terminator Cycle Sequencing Ready Reaction Kit (Applied Biosystems). The sequences were analysed using GENETYX-MAC version 8.0 (Software Development, Tokyo, Japan).

Phylogenetic analysis

Using CLUSTAL W version 1.8 (Thompson et al. I994), the nucleotide sequences of psbC and its deduced amino acid sequences from dinoflagellate and haptophyte taxa obtained in this study were aligned with those from various photosynthetic prokaryotcs and eukaryotes that were retrieved from the DNA Data Bank of Japan (DDBJ) (Table 1). The generated alignments were inspected by eye and manually edited. Because nucleotide sequences of protein-coding genes have codon structure, the psbC nucleotide sequences were aligned according to the corresponding amino acid sequence alignment. The alignment data sets are available on request from the corresponding author. Based on the alignment data of the first and second codon positions of nucleotide sequences of pxbC (41 taxa, 716 positions), maximum likelihood (ML) analysis with PAUP* version 4 (Swofford 1998) was performed with the general time-reversible (GTR) model (Rodrguez et al. 1990) incorporating invariable sites and a discrete gamma distribution (four categories) (GTR + I + Γ). The GTR + I + Γ model was selected by MODELTEST version 3.06 (Posada & Crandall 1998). The proportion of invariable sites, a discrete gamma distribution and base frequencies of the model were estimated from the dataset. For the nucleotide sequence data, the ML distance bootstrap analysis (Felsenstein 1985) (1000 replicates) was also performed with PAUP*. Distances for each data set were calculated under GTR + I + Γ. Each tree was constructed using the neighbour joining (NJ) (Saitou & Nei 1987) method. For the alignment data of deduced amino acid sequences of PsbC (41 taxa, 358 positions), the ML analysis with the PROML algorithm of PHYLIP 3.6a2.1 (Felsenstein 2001) was performed with the Jones-Taylor- Thornton (JTT) model (Jones et al. 1992) incorporating invariable sites and a discrete gamma distribution (eight categories) (JTT + I + Γ). The parameters obtained from the distance analysis with TREE-PUZZLE 5.0 (Schmidt et al. 2002) were used for this gamma correction. For bootstrap analysis, 100 data sets were created using the SEQBOOT program in the PHYLIP package. Distances for each data set were calculated using the PUZZLEBOOT script (by M. Holder and A. Roger, available at http://www.tree-puzzle.de/ttpuzzleboot) with JTT + I + Γ. The NJ tree was constructed from each distance matrix with the NEIGHBOR program of PHYLIP. The consensus bootstrap tree was obtained with the CONSENSE program of PHYLIP.

Table I. List of species used for the phylogenctic analysis of psbC.

RESULTS

Nucleotide and deduced amino acid sequences of the psbC gene

Multiple clones of PCR-amplified DNA fragments of psbC genes were sequenced from the species of dinoflagellates and haptophytes used in the present study. The psbC gene sequences from all species of peridinin- and fucoxanthin derivative-containing dinoflagellates showed small heterogeneity. Therefore, only one representative sequence from each dinoflagellate species was used for the following phylogenetic analysis because it was clear that the heterogeneity does not affect the overall topology of the phylogenetic trees.

The sequences of two haptophytes species (Pavlova sp. and Gephyrocapsa oceanica) and three species of fucoxanthin derivative- containing dinoflagellates (Karenia mikimotoi, K. brevis and Karlodinium inicrum) determined in this study were 1057 bp in length. This length was just identical to that of corresponding regions from all photosynthetic organisms previously reported (a heterokont, a cryptophyte, a euglenophyte, a glaucophyte, green algae, red algae and cyanobacteria). However, the lengths of the sequences from peridinintype dinoflagellates varied considerably (1006-1069 bp). Consequently, there were some insertions and deletions among the psbC sequences from this type of dinoflagellate. In particular, large unique deletions (nine and 23 amino acid residues) were identified in the sequences from Symbiodinium spp. and Gymnodinium impudicum, respectively (Fig. 1). The new psbC gene sequences obtained in the present study have been deposited in GenBank under accession numbers AB158769-AB15 8791 (Table 1).

Phylogenetic analysis

The psbC genes of dinoflagellates are expected to have extremely high evolutionary rates, because other dinoflagellate plastid- encoded genes previously reported have high rates (Takishita & Uchida 1999; Zhang et al. 1999, 2000; Barbrook & Howe 2000; Barbrook et al. 2001 ; Yoon et al, 2002). Thus, exclusion of third codon positions (for nucleotide sequence data) and gamma correction (for both nucleotide and deduced amino acid sequence data) were applied for the phylogenetic analysis to avoid a serious artifact caused by mutational saturation. Here, the phylogenetic trees based on the nucleotide and deduced amino acid sequences are referred to as the psbC (Fig. 2) and CP43 (Fig. 3) trees, respectively. In both trees, three species of cyanobacteria Synechocystis sp. (PCC 6803), Nostoc sp. (PCC 7120) and Prochlomthrix hollandica were used as outgroups. The topologies of the psbC and CP43 trees were similar, with the photosynthetic eukaryotes being composed of two major clades, the chlorophyll-a/fc-containing and chlorophyll-a/c-containing (including red algae) groups. Both peridinin- and fucoxanthin derivative-containing dinoflagellates were within the radiation of the chlorophyll-a/c-lineage. The peridinin-type dinoflagellates constituted a monophyletic group with high bootstrap values (100%), but this group did not show a specific affinity with any other chlorophyll-a/c-containing algae (Figs 2, 3). The fucoxanthin derivative-containing dinoflagellates were also monophylclic in both trees (Figs 2, 3), although it was only weakly supported by the bootstrap analysis. The lineage comprising the three fucoxanthin derivative-containing species was a sister to the haptophyte Gephyrocapsa oceanica in both trees with 72-76% bootstrap supports (Figs 2, 3).

Fig. 1. Two blocks of the CP43 amino sequence alignment correspond to amino acids 74-94 (left block) and 123-157 (right block) of the Heterocapsa triquelra psbC gene. The left and right blocks indicate large deletions specifie to Symbioclinium spp. and Gymnodinium impudicum, respectively.

DISCUSSION

In the present study, we performed phylogenetic analyses based on the plastid-encoded gene psbC to examine the evolutionary relationship between peridinin- and fucoxanthin derivative-type plastids. Our data did not support the monophyly of the peridinin- and fucoxanthin derivative-type plastids, suggesting that these two types originated from independent photosynthetic organisms. Furthermore, based on the phylogeny, the psbC sequences of the fucoxanthin derivative-containing dinoflagellates were closely related to that of the haptophyte alga G. oceanica (although bootstrap support was not so high). This finding supports that the fucoxanthin derivative-type plastids are of haptophyte origin and agrees with the results of previous studies of other plastid- encoded genes (plastid small-subunit rDNA and rbcL) (Takishita et al. 1999, 2000; Tengs et al. 2000) and the nuclear-encoded plastid- targeted gene psbO (Ishida & Green 2002). The phylogenetic position of another haptophyte species, Pavlova sp., was unclear within the chlorophyll-a/c-clade, and did not show a close relationship with the fucoxanthin derivative-containing dinoflagellates. This suggests that the origin of the fucoxanthin derivative-type plastids was a haptophyte cell related to the class Prymnesiophyceae Hibberd emend. Cavalier-Smith rather than the Pavlovophyceae (Cavalier-Smith) Green & Medlin. Because the peridinin-type lineage did not robustly cluster with any other taxa within the chlorophyll-a/c-clade, it is difficult to discuss the origin of the peridinin-type plastids based on the present analyses alone.

Fig. 2. The ML tree of the psbC nucleotide sequence reconstructed under the GTR + I + Γ model. Three species of cyanobacteria, Nostoc sp. PCC 7120, Synechocystis sp. PCC 6803 and Prochlorolhrix hollandica were used to root the tree. Numbers at the nodes refer to the percentage (> 50%) of bootstrap support of ML distance analysis.

Fig. 3. The ML tree of the CP43 amino sequence reconstructed under the JTT + I + Γ model. Three species of cyanobacteria, Nostoc sp. PCC 7120, Synechocystis sp. PCC 6803 and Prochlorothrix hollandica were used to root the tree. Numbers at the nodes refer to the percentage (> 50%) of bootstrap support.

Recently, the combined psaA + psbA phylogeny has prov\ided surprising data indicating that the peridinin- and fucoxanthin derivative-type plastids of dinoflagellates share a common origin and that the plastids of haptophytes and dinoflagellates (both peridinin- and fucoxanthin derivative-types) are monophyletic, leading to the suggestion that an ancestor of all photosynthetic dinoflagellates acquired its plastid from a haptophyte through a tertiary endosymbiosis before the split of the peridinin- and the fucoxanthin derivatives type lineages (Yoon et al. 2002). This conclusion contradicts the conventional and our present views that the original peridinin-type plastid was replaced by the fucoxanthin derivative-type plastid of a haptophyte alga via a tertiary endosymbiosis occurring in the common ancestor of the fucoxanthin derivativecontaining dinoflagellates. Inagaki et ai (2004) have reanalysed the amino acid sequence alignment data (PsaA + PsbA) of Yoon et al. (2002) using the ML method with JTT + I + Γ, and also have pointed out a novel artifact 'codon usage heterogeneity' in the nucleotide sequence analyses by Yoon et al. (2002). In the analyses of Inagaki et al. (2004), there was no indication of a close relationship between the peridinin- and fucoxanthin derivative- type plastids of dinoflagellates, nor between the haptophyte and peridinin-type dinoflagellate plastids. Instead, the peridinin-type plastids were grouped with the plastids of heterokonts and the fucoxanthin derivative-type plastids were grouped with the haptophyte plastids, although neither was well supported by bootstrap probabilities. The combination of our present approach with the results of Inagaki el al. (2004) indicates separate origins of the peridinin- and the fucoxanthin derivative-type plastids, rather than a single common origin. Along with the results of previous studies about plastid small-subunit rDNA (Takishita et al. 1999; Tengs et al. 2000), rbcL (Takishita et al. 2000) and psbO (Ishida & Green 2002), it is also possible to conclude that the fucoxanthin derivative-type plastids originated from the plastids of a haptophyte endosymbiont through a tertiary endosymbiosis. On the other hand, the results of previous phylogenetic analyses based on several plastid-encoded genes and a nuclear-encoded plastid- targeted gene implied that the peridinin-type plastids were acquired from a red alga through secondary endosymbiosis (Zhang et al. 1999, 2000; Ishida & Green 2002). Furthermore, analyses of nuclear small- subunit ribosomal RNA weakly support a relationship between alveolates (comprising dinoflagellates, apicomplexuns and ciliates) and heterokonts (Van de Peer & De Wachter 1997; Ben AH et al. 2001); multiple nuclear protein (alphatubulin, beta-tubulin, actin and elongation factor 1-alpha)-coding genes weakly support a grouping of heterokonts, apicomplexans and ciliates (Baldauf et al. 2000); and RNA polymerase II gene phylogenies give moderate support for the grouping of apicomplexans and heterokonts (Dacks et al. 2002). (However, taxon sampling was poor in some of these phylogenetic studies.) Thus, the grouping of heterokonts and peridinin-type dinoflagellates in the PsaA + PsbA phylogeny may not mean that the peridinin-type plastids are derived from a heterokont alga, but that the hosts of these two algal groups are phylogenetically related and their plastids share a red alga as a common ancestor.

More accurate understanding of the evolutionary history of the dinoflagellate plastids may be achieved by comprehensive phylogenetic analysis with more varied plastid-encoded and nuclear- encoded plastid-targeted genes. Yoon et al. (2002) have argued that the fucoxanthin derivative-type plastids are in fact more primitive than the peridinin-type plastids and not newly adopted as widely believed. If this is the case, the fucoxanthin derivative- containing dinoflagellates (hosts) might have diverged first among the photosynthetic dinoflagellate lineage. However, this view has not yet been supported by any phylogenetic studies of nuclear rDNA (Saunders et al. 1997; Daugbjerg et al. 2000; Tengs et al. 2000; Saldarriaga et al. 2001; Takishita et al. 2002) or protein coding genes (Saldarriaga et al. 2003) from the dinoflagellates. Thus, it will also be important to clearly elucidate the phylogenetic relationship between the 'hosts' of peridinin- and fucoxanthin derivative-containing dinoflagellates in the future.

ACKNOWLEDGEMENTS

We thank Mr M. Kawato (Marine Work Japan) for technical assistance. This work was performed as a part of the project 'Study for Understanding of Function and Structure of the Marine Ecosystems in the Earth Systems' of JAMSTEC.

K. TAKISHTIA, K.-I. IShIDA, M. ISHIKURA AND T. MARUYAMA. 2005. PhylogEny of the psbC gene, coding a photosystem II component CP43, suggests separate origins for the peridinin- and fucoxanthin derivative-containing plastids of dinoflagellates. Phycologia 44: 26- 34.

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Received 20 January 2004; accepted 1 August 2004

Communicating editor: S. Blackburn

KIYOTAKA TAKISHITA1*, KEN-ICHIRO IsHiDA2, MASAHARU ISHIKURA3 AND TADASHI MARUYAMA1

1 Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Kanagawa 237-0061, Japan

2 Division of Natural Science & Technology, Kanazawa, University, Kanazawa, Ishikawa 920-1192, Japan

3 Research and Development Operations, Yamaha Motor Company, Iwata, Shizuoka 438-8501, Japan

* Corresponding author (takishitak@jamstec.go.jp).

Copyright International Phycological Society Jan 2005

Source: Phycologia

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