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Protistology 17 (1): 30-37 (2023) | doi:10.21685/1680-0826-2023-17-l-3
Protistology
Original article
Phylogenetic analysis of the amino acid sequences of peridinin-containing protein complexes lHc from dinoflagellate transcriptomes, with emphasis on Prorocentrum cordatum (Ostenfeld) Dodge, 1975
Sofia A. Pechkovskaya*, Sergei O. Skarlato and Natalia A. Filatova
Institute ofCytology, Russian Academy ofSciences, Saint Petersburg 194064, Russia | Submitted January 11, 2023 | Accepted February 20, 2023 |
Summary
This research continues a series of studies of physiology and phylogeny of the potentially toxic dinoflagellate Prorocentrum cordatum (Ostenfeld) Dodge, 1975, a eukaryotic unicellular alga capable of forming harmful algal blooms (HABs) in marine coastal areas. P. cordatum is a highly adaptable invasive species, which recently colonized brackish-water Baltic Sea. HAB dynamics of this and other dinoflagellates are influenced by various abiotic and biotic factors, such as nutrient enrichment, temperature, salinity and irradiance. Light plays an important role in regulating the growth rate and nutrient assimilation by phytoplankton. Some dinoflagellate species possess unique pigments, such as peridinin, which is associated with light-harvesting protein complex acpPC, belonging to the LHC protein family. This protein binds chlorophyll a/c and carotenoids and functions as a light-harvesting antenna. In this work, we phylogenetically characterized the LHC-like amino acid sequences of dinoflagellates found in unannotated transcriptomes of the Marine Microbial Eukaryote Transcriptome Sequencing Project database (MMETSP). The obtained LHC-like sequences have strong phylogenetic relationships with homologous proteins of algae from other taxa and share typical conservative amino acid motifs with them. Phylogenetic analysis showed that the LHC-like sequenced dinoflagellates grouped together with other fucoxanthin-chlorophyll a/c-containing algae. Within this group, acpPC sequences from the peridinin-containing dinoflagellate species formed a well-supported distinct clade. The evolutionary relationships of peridinin-containing dinoflagellates P. cordatum with other dinoflagellates and various algal taxa were analyzed. The obtained results provide a deeper insight into advanced physiological adaptation strategies ofbloom-forming dinoflagellates thus contributing to HABs modeling, forecasting and management.
Key words: dinoflagellates, light-harvesting complex, peridinin, phylogeny, Prorocentrum cordatum, transcriptome
https://doi.org/10.21685/1680-0826-2023-17-1-3
© 2023 The Author(s)
Protistology © 2023 Protozoological Society Affiliated with RAS
Corresponding author: Sofia Pechkovskaya. Institute of Cytology RAS, Tikhoretsky Ave. 4, 194064 St. Petersburg, Russia; sapechkovskaya@gmail.com
Introduction
The potentially toxic dinoflagellate Prorocent-rum cordatum (Ostenfeld) Dodge, 1975 (major synonym: Prorocentrum minimum (Pavillard) Schiller, 1933) is a eukaryotic unicellular alga capable of forming harmful blooms in coastal areas (Hajdu et al., 2005). This highly invasive species is demonstrating remarkable adaptation strategies (Knyazev et al., 2018; Skarlato et al., 2018a, 2018b; Telesh et al., 2021). The species successfully colonized the oligohaline Baltic Sea in the early 1980s, eventually outcompeted the native congener Prorocentrum balticum (Telesh et al., 2016), and currently forms blooms throughout the region (Telesh et al., 2020; Telesh and Skarlato, 2022a, 2022b). Harmful algal blooms (HABs) of dinofla-gellates cause a multitude of stressful effects in ecosystems that can lead to major ecological and economical losses particularly in the coastal areas (Berdalet et al., 2015; Glibert, 2020; Telesh et al., 2021).
The spread of blooms, their intensity and duration are influenced by ecological factors such as nutrient enrichment, temperature, salinity, pH, turbulence and irradiance. Light plays an important role in regulating the growth rate and nutrient assimilation in phytoplankton species (Nicklisch et al., 2008; David et al., 2018), since they require a certain amount of light for photosynthesis. The intensity of light at the surface and at depth is significantly different, and many dinoflagellates migrate during the day because light intensity affects the maximum depth, which dinoflagellate cells can reach in the water column (Ji and Franks, 2007; Richter et al., 2008). Moreover, it was shown that photoperiodicity influences many biochemical and physiological processes in the cell, including protein synthesis (Hastings, 2013; Pechkovskaya et al., 2021).
Dinoflagellates possess a wide diversity ofplastid types (Schnepf and Elbr^chter, 1999). Most dino-flagellates have plastids containing chlorophylls a and c2, the carotenoid beta-carotene and other unique carotenoids such as peridinin, dinoxanthin and diadinoxanthin (Hackett et al., 2004; Yamada et al., 2015). Some species have acquired a carotenoid fucoxanthin, which apparently is the result of tertiary symbiosis with haptophyte algae (Tengs et al., 2000). Peridinin is an unusual carotenoid, which is uniquely present in the majority of dinoflagellate species (Fig. 1). Inside the cell, peridinin is asso-
Fig. 1. Molecular structure of the peridinin.
ciated with two unrelated light-harvesting protein complexes: the soluble peripheral antenna peri-dinin-chlorophyll a-protein (PCP), where the bound carotenoids stoichiometrically outnumber the chlorophyll (Schulte et al., 2009; Dorrell et al., 2019), and chlorophyll a-chlorophyll c2-peridinin protein complex (acpPC, encoded by Lhc genes). Overall, the LHC superfamily is divided into three major groups by the type of chlorophyll associated with the protein. The LHC of green plants and chlorophytes bind chlorophylls a and b, rhodophyte and cyanobacteria LHCs bind chlorophyll a, and chlorophyll c-containing algae possess LHCs that bind chlorophylls a and c and carotenoid fucoxanthin (fucoxanthin-chlorophyll proteins, FCP) (Green and Durnford, 1996.)
Dinoflagellate acpPC complexes share sequence similarity with the other known LHC proteins that belong to the chlorophyll a/c subfamily of LHCs (Hiller et al., 1993). Besides the peridinin, acpPC also binds the carotenoid diadinoxanthin, which role in the complex is not fully understood yet (Jiang et al., 2014). No crystal structure of acpPC has been determined.
In routine monitoring ofphytoplankton assemblages, identification of pigments composition can be used as a biomarker of the presence of dinoflagellates in the algal community (Bustillos-Guzman et al., 2004; Richardson and Pinckney, 2004; Shan et al., 2022).
Currently, the Symbiodinium sp. EST library screening revealed the presence of multiple LHC family sequences in these dinoflagellates, divided into several clades within the Chl a/c binding LHC family (Boldt et al., 2012). AcpPC structure has been described at the protein level for Symbiodinium sp. (Jiang et al., 2014). Moreover, the transfer of energy between Chl a and carotenoid was characterized using the example of acpPC complex acquired from the dinoflagellate Amphidinium carterae (Kvicalova et al., 2016).
Previously, the phylogenetic analysis of LHC family proteins revealed a wide diversity of LHC genes inside the group of dinoflagellates as well as
Fig. 2. Amino acid sequence alignment of LHC family homologs of the representatives of the major taxonomic groups. Three predicted membrane-spanning regions (MSR) are highlighted with the boxes. Conserved sites are labelled with black dots. Abbreviations for species and accession numbers in MMETSP or GenBank: Prorocentrum cordatum CCMP1329, 260471; Heterosigma akashiwo, CAA68028; Krypthecodinium foliaceum, 241269; Macrocystis pyrifera, AAC49021; Fragilariacrotonensis, KAI2513900; Rhodomonassp., CS24, CAI91154; Pinus remota, AAU89262; Anabaena cylindrica, AFZ56611.
the presence of numerous paralogs (Hoffman et al., 2011). However, the phylogenetic and evolutionary relationships among dinoflagellates are not fully resolved, and there is a lack of understanding of P. cordatum phylogenetic position among other dinoflagellates, including toxic HAB-forming species.
The aim of this study is to investigate the evolutionary relationships of the protein homologs of acpPC complex belonging to the LHC family, inferred from transcriptomes of the dinoflagellate P. cordatum, with other dinoflagellate species and different algal taxa.
Material and methods
Transcriptome analysis
The homologous amino acid sequences of the LHC family proteins were identified in the unannotated dinoflagellate transcriptomes in the publicly available database of the Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP; Keeling et al., 2014). The Symbiodini-um microadriaticum amino acid sequence (accession number OLP90953) from the National Center for Biotechnology Information (NCBI; http://www. ncbi.nlm.nih.gov/protein) was used as query for LHC protein sequence search. A local BLAST search was performed by means ofthe BioEdit 7.2.5 software (Hall, 1999) with BLOSUM62 matrix (E-value < 10-50).
Sequence analysis
Protein conservative domains in the assumed LHC sequences were identified using Conserved Domains Search service (Lu et al., 2020). The signature motifs and conserved residues for LHC family proteins identified in the studied sequences were described by Green and Kühlbrandt (1995). Amino acid sequences were aligned using the MAFFT online service (Katoh et al., 2019). The alignments were manually inspected and edited.
Phylogeny analysis
Phylogenetic analysis was performed using PhyML for maximum likelihood and MrBayes for Bayesian inference. The analysis of the LHC-like amino acid sequences of the dinoflagellate species and the other taxa's LHCs available in GenBank database and sufficient for phylogenetic reconstructions was carried out. Conserved blocks were selected manually with the SeaView software (Gouy et al., 2010). The resulting dataset of LHC family homologs contained 59 amino acid sequences and 155 positions. Phylogenetic analysis was performed by means of the RAxML 8.2.1 (Stama-takis, 2014) provided by the CIPRES Science Gateway service (Miller et al., 2010). For the analysis, we generated 100 RaxML tree searches to obtain the best ML tree as the starting tree. ML analysis was performed using LG (Le and Gascuel, 2008) substitution matrix. The most suitable substitution matrix was determined by means of
MEGA software (Kumar et al., 2018). Topological robustness was statistically tested by non-parametric bootstrap analysis from 1000 bootstrap replications. The Bayesian phylogenetic analysis for LHC tree was performed using MrBayes 3.2.7 (Ronquist et al., 2012) available online on CIPRES servers using the LG + G model. The most suitable substitution matrix was determined using ModelTest-NG (Flouri et al., 2014; Darriba et al., 2020) software on CIPRES servers. 4000000 generations with first 25% discarded (burn-in) were run for three independent analyses of four chains each, sampling every 250 generations. The tree was visualized using SeaView software. All trees were rooted using cyanobacterial sequences.
Results and discussion
Characteristics of LHC homologs
Multiple sequences ofthe LHC protein homologs were identified in unannotated transcriptomes of12 species ofdinoflagellates presented in the MMETSP database. Some sequences were short copies of the same transcripts or incomplete reads and were not included in the analysis. All dinoflagellate LHC paralogs found in transcriptomes contained the conservative chlorophyll a/c binding domains identified by means of the CD-Search in NCBI service.
In preliminary phylogenetic reconstructions, LHC paralogs formed the monophyletic clade; for further analysis, the sequences corresponding to the shortest branches were chosen. Twenty-five amino acid LHC homologous sequences were recovered from the transcriptomes of P. cordatum strains CCMP1329 and CCMP2233. Hypothetical acpPC sequence retrieved for strain CCMP1329 is 917 aa long encoding the putative 98.9 kDa protein with theoretical isoelectric point (pI) 5.7. AcpPC homologous sequence retrieved for strain CCMP2233 is 701 aa long and encodes the putative 75.8 kDa protein with theoretical pi 8.8.
The analysis of the obtained sequences revealed the signature residues of the LHC family proteins described by Green and Kuhlbrandt (1995). Conservative Chl a-binding sites E139, H142, R144, G149, E260, N263 and R265 were found in the acpPC homologs (Fig. 2), although in some cases there were residue substitutions. Three conserved membrane-spanning regions (MSR) were predicted in the dinoflagellate acpPC sequences, which is consistent with the existing LHC structure model (Green and
Kühlbrandt, 1995). MSR domains 1 and 3 intersect each other in the thylakoid membrane, thereby stabilizing the LHC protein complex (Green and Kühlbrandt, 1995). They share the common conservative motif EXXH(N)XR, which is quite conventional among other LHC homologs of dinoflagellates and other microalgae species.
Phylogenetic analysis
To examine the relationship between the dinoflagellates' LHC-like homologs and the LHC family proteins of other taxa, a maximum likelihood tree was constructed using RAxML. The analysis was carried out with dinoflagellate sequences retrieved from MMETSP transcriptomes and the annotated LHC family sequences of other microalgae taxa retrieved from GenBank database. Cyanobacteria were used as an outgroup (Fig. 3).
Phylogenetic analysis ofthe LHC family protein homologous sequences showed a clear separation into two major groups corresponding to the Chl a/b and Chl a/c binding protein lineages. The first group contains Chl a/c and includes amino acid sequences from dinoflagellates, ochrophytes, diatoms, hapto-phytes, cryptophytes, and rhodophytes. The second group includes proteins from green plants, chloro-phytes, and euglenophytes.
Within the first group, several clades can be distinguished. The dinoflagellate sequences were divided into groups depending on the carotenoid they bound. AcpPC homologs binding peridinin formed a separate well-maintained subclade. Sequences of fucoxanthin-containing FCP proteins of dinoflagellates were mixed with other taxa ofmicro-algae.
our phylogenetic analysis indicates that the majority of LHCs in dinoflagellates group together as a sister branch to fucoxanthin-Chl a/c binding LHCs (FCPs) from diatoms, brown algae, and cryptophytes. Fucoxanthin is the major carotenoid in Chl c-containing organisms. Apparently, peridinin-containing complex acpPC have a sister relationship with FCP complex of other Chl a/c binding taxa.
Some dinoflagellate species (Lingulodinium polyedra, Scripsiella trochoidea) possess several LHC paralogs that are distributed among different phylo-genetic groups. The presence of such paralogs can be associated with the repeated acquisition of plastids during the evolution of dinoflagellates.
The first group (as we classified above) contains a separate clade of red algae-like LHC sequences, which belongs to the subfamily of proteins binding
Fig. 3. Protein phylogeny of LHC homologous protein sequences with LHC homologs from the transcriptomes of dinoflagellates and other taxa. The tree is inferred using RAxML under the LG model and 1000 bootstrap replicates, posterior probabilities are inferred using MrBayes 3.2.7 under the LG + G model. Bayesian analysis generated similar topology to the ML tree. The first and second numbers at the nodes display bootstrap proportions (>50%) in ML and posterior probability (>0.50) in Bayesian, respectively. Sequences are colored according to the major taxonomic groups. P. cordatum sequences are highlighted with frame. The number corresponding to the number of sequences in the unannotated transcriptomes or the accession number in the database (GenBank) is indicated. Cyanobacteria were used as an outgroup.
only Chl a and zeaxanthin (Pi et al., 2018). This LHC lineage is considered one of the most primitive forms of LHC proteins that serve as the reaction center of photosystem I in cyanobacteria and red algae (Engelken et al., 2011).
The distribution of LHC family homologs among the groups depending on the bound pigments, revealed in this study, are generally consistent with the previous phylogenetic studies of the LHC evolutionary relationships (Hoffman, 2011; Pan,
2011; Boldt, 2012). A wide diversity of LHC family proteins and an abundance of paralogs in the group of dinoflagellates was found. This, apparently, is the result of complex history of gene duplication, horizontal transfer, multiple plastid losses and repeated acquisitions through tertiary endosymbiosis (Hoffman et al., 2011). The division of LHC proteins into groups in our analysis corresponds to different LHC subfamilies allocated depending on the type of chlorophyll, which they bind (a/c, a/b or only a).
We confirmed that, as in the earlier published data, dinoflagellate acpPC sequences form a sister group with FCP sequences from diatoms, haptophytes, and pelagophytes that also bind chlorophyll a/c and fucoxanthin (Pan et al., 2011; Boldt et al., 2012). This finding is also consistent with the data showing that individual species (like L. polyedra and S. trochoidea) can contain LHCs from different subfamilies, and that LHC subfamilies are not lineage-specific (Hoffman et al., 2011).
Conclusions
In essence, the phylogenetic analysis made in this study revealed the evolutionary relationships of the LHC family homologous proteins inferred from the dinoflagellate transcriptomes to the LHC homologs from other taxa, which allows to expand our understanding of their evolutionary history. Multiple sequences of acpPC homologs were revealed in the transcriptomes ofthe potentially toxic dinoflagellate P. cordatum; they formed a monophyletic clade within the group of peridinin-containing LHC protein sequences. The acpPC homologs of P. cordatum were clustered with sequences of other peridinin-containing dinoflagellates and formed a well-supported distinct clade within the group of chlorophyll a/c binding LHC subfamily sequences. These findings provide a deeper insight into advanced physiological adaptation strategies of bloom-forming dinoflagellates and contribute to reliable modeling, forecasting and management of HABs.
Acknowledgements
This research was funded by the Russian Science Foundation (project 22-14-00056).
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