Author: cslamo

ISME J. 2024 Apr 24:wrae059. doi: 10.1093/ismejo/wrae059. Online ahead of print.

ABSTRACT

Dinoflagellates in the family Symbiodiniaceae are taxonomically diverse, predominantly symbiotic lineages that are well-known for their association with corals. The ancestor of these taxa is believed to have been free-living. The establishment of symbiosis (i.e., symbiogenesis) is hypothesised to have occurred multiple times during Symbiodiniaceae evolution, but its impact on genome evolution of these taxa is largely unknown. Among Symbiodiniaceae, the genus Effrenium is a free-living lineage that is phylogenetically positioned between two robustly supported groups of genera within which symbiotic taxa have emerged. The apparent lack of symbiogenesis in Effrenium suggests that the ancestral features of Symbiodiniaceae may have been retained in this lineage. Here we present de novo assembled genomes (1.2-1.9 Gbp in size) and transcriptome data from three isolates of Effrenium voratum and conduct a comparative analysis that includes 16 Symbiodiniaceae taxa and the other dinoflagellates. Surprisingly, we find that genome reduction, which is often associated with a symbiotic lifestyle, predates the origin of Symbiodiniaceae. The free-living lifestyle distinguishes Effrenium from symbiotic Symbiodiniaceae vis-à-vis their longer introns, more-extensive mRNA editing, fewer (~30%) lineage-specific gene sets, and lower (~10%) level of pseudogenisation. These results demonstrate how genome reduction and the adaptation to distinct lifestyles intersect to drive diversification and genome evolution of Symbiodiniaceae.

PMID:38655774 | DOI:10.1093/ismejo/wrae059

EMBO Rep. 2024 Mar 18. doi: 10.1038/s44319-024-00103-y. Online ahead of print.

ABSTRACT

Dinoflagellates are a diverse group of ecologically significant micro-eukaryotes that can serve as a model system for plastid symbiogenesis due to their susceptibility to plastid loss and replacement via serial endosymbiosis. Kareniaceae harbor fucoxanthin-pigmented plastids instead of the ancestral peridinin-pigmented ones and support them with a diverse range of nucleus-encoded plastid-targeted proteins originating from the haptophyte endosymbiont, dinoflagellate host, and/or lateral gene transfers (LGT). Here, we present predicted plastid proteomes from seven distantly related kareniaceans in three genera (Karenia, Karlodinium, and Takayama) and analyze their evolutionary patterns using automated tree building and sorting. We project a relatively limited ( ~ 10%) haptophyte signal pointing towards a shared origin in the family Chrysochromulinaceae. Our data establish significant variations in the functional distributions of these signals, emphasizing the importance of micro-evolutionary processes in shaping the chimeric proteomes. Analysis of plastid genome sequences recontextualizes these results by a striking finding the extant kareniacean plastids are in fact not all of the same origin, as two of the studied species (Karlodinium armiger, Takayama helix) possess plastids from different haptophyte orders than the rest.

PMID:38499810 | DOI:10.1038/s44319-024-00103-y

STAR Protoc. 2024 Mar 12;5(2):102941. doi: 10.1016/j.xpro.2024.102941. Online ahead of print.

ABSTRACT

Dinoflagellate genomes often are very large and difficult to assemble, which has until recently precluded their analysis with modern functional genomic tools. Here, we present a protocol for mapping three-dimensional (3D) genome organization in dinoflagellates and using it for scaffolding their genome assemblies. We describe steps for crosslinking, nuclear lysis, denaturation, restriction digest, ligation, and DNA shearing and purification. We then detail procedures sequencing library generation and computational analysis, including initial Hi-C read mapping and 3D-DNA scaffolding/assembly correction. For complete details on the use and execution of this protocol, please refer to Marinov et al.¹.

PMID:38483898 | DOI:10.1016/j.xpro.2024.102941

Environ Microbiol Rep. 2024 Apr;16(2):e13238. doi: 10.1111/1758-2229.13238.

ABSTRACT

Bacterial-algal interactions strongly influence marine ecosystems. Bacterial communities in cultured dinoflagellates of the family Symbiodiniaceae have been characterized by metagenomics. However, little is known about whole-genome analysis of marine bacteria associated with these dinoflagellates. We performed in silico analysis of four bacterial genomes from cultures of four dinoflagellates of the genera Symbiodinium, Breviolum, Cladocopium and Durusdinium. Comparative analysis showed that the former three contain the alphaproteobacterial family Parvibaculaceae and that the Durusdinium culture includes the family Sphingomonadaceae. There were no large genomic reductions in the alphaproteobacteria with genome sizes of 2.9-3.9 Mb, implying they are not obligate intracellular bacteria. Genomic annotations of three Parvibaculaceae detected the gene for diacetylchitobiose deacetylase (Dac), which may be involved in the degradation of dinoflagellate cell surfaces. They also had metabolic genes for dissimilatory nitrate reduction to ammonium (DNRA) in the nitrogen (N) cycle and cobalamin (vitamin B₁₂ ) biosynthetic genes in the salvage pathway. Those three characters were not found in the Sphingomonadaceae genome. Predicted biosynthetic gene clusters for secondary metabolites indicated that the Parvibaculaceae likely produce the same secondary metabolites. Our study suggests that the Parvibaculaceae is a major resident of Symbiodiniaceae cultures with antibiotics.

PMID:38444256 | DOI:10.1111/1758-2229.13238

Sci Rep. 2024 Feb 29;14(1):4986. doi: 10.1038/s41598-024-55362-5.

ABSTRACT

Protists make up the vast diversity of eukaryotic life and play a critical role in biogeochemical cycling and in food webs. Because of their small size, cryptic life cycles, and large population sizes, our understanding of speciation in these organisms is very limited. We performed population genomic analyses on 153 strains isolated from eight populations of the recently radiated dinoflagellate genus Apocalathium, to explore the drivers and mechanisms of speciation processes. Species of this genus inhabit both freshwater and saline habitats, lakes and seas, and are found in cold temperate environments across the world. RAD sequencing analyses revealed that the populations were overall highly differentiated, but morphological similarity was not congruent with genetic similarity. While geographic isolation was to some extent coupled to genetic distance, this pattern was not consistent. Instead, we found evidence that the environment, specifically salinity, is a major factor in driving ecological speciation in Apocalathium. While saline populations were unique in loci coupled to genes involved in osmoregulation, freshwater populations appear to lack these. Our study highlights that adaptation to freshwater through loss of osmoregulatory genes may be an important speciation mechanism in free-living aquatic protists.

PMID:38424140 | DOI:10.1038/s41598-024-55362-5

Ecotoxicol Environ Saf. 2024 Feb 26;273:116146. doi: 10.1016/j.ecoenv.2024.116146. Online ahead of print.

ABSTRACT

Filter-feeding bivalves could accumulate paralytic shellfish toxins (PSTs) produced by harmful dinoflagellates through diet. Despite that bivalves are resistant to these neurotoxins due to possessing PST-resistant sodium channel, exposure to PSTs-producing dinoflagellates impair bivalve survival. We hypothesized that ingesting PSTs-PSTs-producing dinoflagellates may influence the gut microbiota, and then the health of bivalves. To test this idea, we compared the gut microbiota of the scallop Patinopecten yessoensis, after feeding with PST-producing or non-toxic dinoflagellates. Exposure to PSTs-PSTs-producing dinoflagellates resulted in a decline of gut microbial diversity and a disturbance of community structure, accompanied by a significant increase in the abundance and richness of pathogenic bacteria, represented by Vibrio. Moreover, network analysis demonstrated extensive positive correlations between pathogenic bacteria abundances and PSTs concentrations in the digestive glands of the scallops. Furthermore, isolation of a dominant Vibrio strain and its genomic analysis revealed a variety of virulence factors, including the tolC outer membrane exporter, which were expressed in the gut microbiota. Finally, the infection experiment demonstrated scallop mortality caused by the isolated Vibrio strain; further, the pathogenicity of this Vibrio strain was attenuated by a mutation in the tolC gene. Together, these findings demonstrated that the PSTs may affect gut microbiota via direct and taxa-specific interactions with opportunistic pathogens, which proliferate after transition from seawater to the gut environment. The present study has revealed novel mechanisms towards deciphering the puzzles in environmental disturbances-caused death of an important aquaculture species.

PMID:38412634 | DOI:10.1016/j.ecoenv.2024.116146

Eur J Protistol. 2024 Feb 3;93:126061. doi: 10.1016/j.ejop.2024.126061. Online ahead of print.

ABSTRACT

Recent progress in high-throughput sequencing technologies has dramatically increased availability of genome data for prokaryotes and eukaryotes. Dinoflagellates have distinct chromosomes and a huge genome size, which make their genomic analysis complicated. Here, we reviewed the nuclear genomes of core dinoflagellates, focusing on the genome and cell size. Till now, the genome sizes of several dinoflagellates (more than 25) have been measured by certain methods (e.g., flow cytometry), showing a range of 3-250 pg of genomic DNA per cell. In contrast to their relatively small cell size, their genomes are huge (about 1-80 times the human haploid genome). In the present study, we collected the genome and cell size data of dinoflagellates and compared their relationships. We found that dinoflagellate genome size exhibits a positive correlation with cell size. On the other hand, we recognized that the genome size is not correlated with phylogenetic relatedness. These may be caused by genome duplication, increased gene copy number, repetitive non-coding DNA, transposon expansion, horizontal gene transfer, organelle-to-nucleus gene transfer, and/or mRNA reintegration into the genome. Ultimate verification of these factors as potential causative mechanisms would require sequencing of more dinoflagellate genomes in the future.

PMID:38394997 | DOI:10.1016/j.ejop.2024.126061

NAR Genom Bioinform. 2024 Feb 10;6(1):lqae016. doi: 10.1093/nargab/lqae016. eCollection 2024 Mar.

ABSTRACT

Dinoflagellates are a diverse group of phytoplankton, ranging from harmful bloom-forming microalgae to photosymbionts of coral reefs. Genome-scale data from dinoflagellates reveal atypical genomic features, extensive genomic divergence, and lineage-specific innovation of gene functions. Long non-coding RNAs (lncRNAs), known to regulate gene expression in eukaryotes, are largely unexplored in dinoflagellates. Here, using high-quality genome and transcriptome data, we identified 48039 polyadenylated lncRNAs in three dinoflagellate species: the coral symbionts Cladocopium proliferum and Durusdinium trenchii, and the bloom-forming species, Prorocentrum cordatum. These lncRNAs have fewer introns and lower G+C content than protein-coding sequences; 37 768 (78.6%) are unique with respect to sequence similarity. We classified all lncRNAs based on conserved motifs (k-mers) into distinct clusters, following properties of protein-binding and/or subcellular localisation. Interestingly, 3708 (7.7%) lncRNAs are differentially expressed under heat stress, algal lifestyle, and/or growth phase, and share co-expression patterns with protein-coding genes. Based on inferred triplex interactions between lncRNA and putative promoter regions, we identified 19 460 putative gene targets for 3721 lncRNAs; 907 genes exhibit differential expression under heat stress. These results reveal, for the first time, the diversity of lncRNAs in dinoflagellates and how lncRNAs may regulate gene expression as a heat-stress response in these ecologically important microbes.

PMID:38344275 | PMC:PMC10858649 | DOI:10.1093/nargab/lqae016

Genome Biol Evol. 2024 Feb 1;16(2):evae014. doi: 10.1093/gbe/evae014.

ABSTRACT

Reef-building corals (Scleractinia, Anthozoa, Cnidaria) are the keystone organisms of coral reefs, which constitute the most diverse marine ecosystems. Since the first decoded coral genome reported in 2011, about 40 reference genomes are registered as of 2023. Comparative genomic analyses of coral genomes have revealed genomic characters that may underlie unique biological characteristics and coral diversification. These include existence of genes for biosynthesis of mycosporine-like amino acids, loss of an enzyme necessary for cysteine biosynthesis in family Acroporidae, and lineage-specific gene expansions of DMSP lyase-like genes in the genus Acropora. While symbiosis with endosymbiotic photosynthetic dinoflagellates is a common biological feature among reef-building corals, genes associated with the intricate symbiotic relationship encompass not only those shared by many coral species, but also genes that were uniquely duplicated in each coral lineage, suggesting diversified molecular mechanisms of coral-algal symbiosis. Coral genomic data have also enabled detection of hidden, complex population structures of corals, indicating the need for species-specific, local-scale, carefully considered conservation policies for effective maintenance of corals. Consequently, accumulating coral genomic data from a wide range of taxa and from individuals of a species not only promotes deeper understanding of coral reef biodiversity, but also promotes appropriate and effective coral reef conservation. Considering the diverse biological traits of different coral species and accurately understanding population structure and genetic diversity revealed by coral genomic analyses during coral reef restoration planning could enable us to “archive” coral reef environments that are nearly identical to natural coral reefs.

PMID:38271267 | DOI:10.1093/gbe/evae014

Curr Biol. 2024 Jan 19:S0960-9822(23)01769-4. doi: 10.1016/j.cub.2023.12.069. Online ahead of print.

ABSTRACT

Brown algae are the only group of heterokont protists exhibiting complex multicellularity. Since their origin, brown algae have adapted to various marine habitats, evolving diverse thallus morphologies and gamete types. However, the evolutionary processes behind these transitions remain unclear due to a lack of a robust phylogenetic framework and problems with time estimation. To address these issues, we employed plastid genome data from 138 species, including heterokont algae, red algae, and other red-derived algae. Based on a robust phylogeny and new interpretations of algal fossils, we estimated the geological times for brown algal origin and diversification. The results reveal that brown algae first evolved true multicellularity, with plasmodesmata and reproductive cell differentiation, during the late Ordovician Period (ca. 450 Ma), coinciding with a major diversification of marine fauna (the Great Ordovician Biodiversification Event) and a proliferation of multicellular green algae. Despite its early Paleozoic origin, the diversification of major orders within this brown algal clade accelerated only during the Mesozoic Era, coincident with both Pangea rifting and the diversification of other heterokont algae (e.g., diatoms), coccolithophores, and dinoflagellates, with their red algal-derived plastids. The transition from ancestral isogamy to oogamy was followed by three simultaneous reappearances of isogamy during the Cretaceous Period. These are concordant with a positive character correlation between parthenogenesis and isogamy. Our new brown algal timeline, combined with a knowledge of past environmental conditions, shed new light on brown algal diversification and the intertwined evolution of multicellularity and sexual reproduction.

PMID:38262417 | DOI:10.1016/j.cub.2023.12.069