bioRxiv Science⌕ Search

Biology subjects

Khalturin, K.

Publications and source records attributed to Khalturin, K..

7 recordsLinked to original sources

Hidden diversity and host specificity of Cladocopium symbionts revealed by phylotranscriptomics in giant sea anemones.

Giant sea anemones form an intricate, metabolically linked symbiosis with anemonefish (genus Amphiprion) and dinoflagellates (family Symbiodiniaceae). While the association between fish and anemone is well documented, the identity and distribution of resident Symbiodiniaceae remains poorly characterized. Here, we used RNA-sequencing of anemone tentacles and post-assembly filtering to recover Symbiodiniaceae sequences from Japanese anemones. Using transcriptome-wide phylogenetic approaches, we identified distinct Symbiodiniaceae strains in seven sea anemone species and four cryptic lineages of Entacmaea quadricolor. Phylogenies of 1300 and 214 nuclear genes resolved relationships among these symbionts with greater sensitivity than traditional molecular markers such as the Internal Transcribed Spacer 2 (ITS2) or partial 28S ribosomal DNA. Marker-based assessments indicate these Symbiodiniaceae as novel and specific to sea anemone hosts. Our transcriptome-wide phylogenies reveal previously undescribed Cladocopium (Clade C) strains associated with giant sea anemones, with symbionts clustering according to host species and lineage. Cophylogenetic analysis revealed significant phylogenetic congruence between anemone and Symbiodiniaceae, indicating a nonrandom association between host and symbiont evolutionary histories. Two sympatric cryptic lineages of E. quadricolor previously identified through host transcriptomics harbor distinct, specific Symbiodiniaceae assemblages. Analysis of genes under positive selection indicates functional divergence between these Symbiodiniaceae; three-dimensional reconstructions of symbiont cells using serial block-face scanning electron microscopy show consistent differences in cellular organization between two strains, further supporting their distinct functional identity. Together, our results uncover a hidden diversity of host-specific Symbiodiniaceae and suggest that cryptic diversification in giant sea anemones is mirrored by diversification of their algal symbionts within this tripartite symbiosis.

evolutionary biology↗

Anemonefish are better taxonomists than humans.

The symbiosis between giant sea anemones, photosynthetic algae of the family Symbiodiniaceae, and anemonefish is an iconic example of a mutualistic "menage a 3"1. Patterns of associations among 28 species of anemonefish and 10 species of giant sea anemone hosts are complex: Some anemonefish species are highly specialized to inhabit only one species of sea anemone (e.g., Amphiprion frenatus with Entacmaea quadricolor), whereas others are more generalist and can live in almost any host species (e.g., Amphiprion clarkii)1,2,3. Reasons for host preferences and the mechanisms involved are obscured, among other things, by the lack of resolution of giant sea anemone phylogeny. Recent molecular analyses have shown that giant sea anemones hosting anemonefish belong to three distinct clades: Entacmaea, Stichodactyla, and Heteractis4,5,6. Inside these clades, however, species delimitation has been impeded by morphological variability of the giant sea anemones and is poorly resolved with classical markers4,5. Here, we employed an extensive transcriptomic dataset from 55 sea anemones collected from southern Japan to build a robust phylogeny. With this dataset, we observed that the bubble-tip sea anemone E. quadricolor, currently considered to be a single species, can in fact be separated into at least four distinct cryptic lineages (A-D). Moreover, these lineages can be precisely distinguished by their association with anemonefish: A. frenatus is only found associated with lineage D, whereas A. clarkii lives in the other three lineages.

evolutionary biology↗

The genetic basis for adaptation in giant sea anemones to their symbiosis with anemonefish and Symbiodiniaceae

Sea anemones in the order Anthozoa play an integral part in marine ecosystems by providing refuge and habitat for various organisms. Despite this, much of their molecular ecology remains elusive. Sea anemones can nurture numerous symbiotic relationships; the most iconic being the one between giant sea anemones and anemonefish. However, the genes and biological processes associated with this symbiosis in the sea anemones in unknown. Additionally, it is unclear how genes can mediate interactions between sea anemones, anemonefish, and symbionts from the algal family Symbiodiniaceae. Here we compared the gene expression profiles of tentacles from several cnidarians to uncover the genetic basis for adaptations in giant sea anemones to their symbiosis with anemonefish and Symbiodiniaceae. We found that tentacle transcriptomes of cnidarians are highly diverse, with closely related species having more similar expression patterns. However, despite an overall high correlation between gene expression and phylogeny, the giant sea anemones showed distinct expression patterns. The giant sea anemones had gene co-expression clusters enriched for processes involved in nutrient exchange and metabolism. These genes were not only differentially expressed, but also experienced evolutionary shifts in expression in giant sea anemones. Using a phylogenetic multilevel model, we found that Symbiodiniaceae and anemonefish significantly affect gene expression in giant sea anemone tentacles. By characterizing gene expression patterns, we identify genes and biological processes that provide evidence for the cross-talk between Symbiodiniaceae, anemonefish, and giant sea anemones. Our study demonstrates how integrated biological processes can lead to the evolution of a successful multi-organism interaction.

evolutionary biology↗

Response of coral reef dinoflagellates to nanoplastics under experimental conditions

Plastic products contribute heavily to anthropogenic pollution of the oceans. Small plastic particles in the micro- and nanoscale ranges have been found in all marine ecosystems, but little is known about their effects upon marine organisms. In this study we examine changes in cell growth, aggregation, and gene expression of two symbiotic dinoflagellates of the family Symbiodiniaceae, Symbiodinium tridacnidorum (clade A3) and Cladocopium sp. (clade C), under exposure to 42-nm polystyrene beads. In laboratory experiments, cell number and aggregation were reduced after 10 days of nanoplastic exposure at 0.01, 0.1, and 10 mg/L concentrations, but no clear correlation with plastic concentration was observed. Genes involved in dynein motor function were upregulated compared to control conditions, while genes related to photosynthesis, mitosis, and intracellular degradation were downregulated. Overall, nanoplastic exposure led to more genes being downregulated than upregulated and the number of genes with altered expression was larger in Cladocopium sp. than in S. tridacnidorum, suggesting different sensitivity to nanoplastic between species. Our data show that nanoplastic inhibits growth and alters aggregation properties of microalgae, which may negatively affect the uptake of these indispensable symbionts by coral reef organisms.

ecology↗

A Reference Genome from the symbiotic hydrozoan, Hydra viridissima

Cnidarians are one of the oldest eumetazoan taxa, and are thought to be a sister group to all bilaterians. In spite of comparatively simple morphology, cnidarians exhibit diverse body forms and life histories. In addition, many cnidarian species establish symbiotic relationships with microalgae. Various Hydra species have been employed as model organisms since the 18th century. Introduction of transgenic and knock-down technologies made them ideal experimental systems for studying cellular and molecular mechanisms involved in regeneration, body-axis formation, senescence, symbiosis, and holobiosis. In order to provide an important reference for genetic studies, the Hydra magnipapillata genome was sequenced. However, the initial published version of the H. magnipapillata genome did not achieve assembly continuity comparable to those of other model systems, due mainly to a large number of transposable elements. For almost a decade, the highly fragmented genome assembly of H. magnipapillata (scaffold N50=128Kb) has remained the only genomic resource for this genus with several dozen species. Here we report a draft 280-Mbp genome assembly for Hydra viridissima strain A99, a symbiotic, early diverging member of the Hydra clade, with a scaffold N50 of 1.1 Mbp. The H. viridissima genome contains an estimated 21,476 protein-coding genes. Comparative analysis of Pfam domains and orthologous proteins highlights characteristic features of H. viridissima, such as diversification of innate immunity genes that are important for host-symbiont interactions. Thus, the Hydra viridissima assembly provides an important hydrozoan genome reference that will facilitate symbiosis research and better comparisons of metazoan genome architectures.

genomics↗

Molecular signatures of the rediae, cercariae and adult worm stages in the complex life cycles of parasitic flatworms (Psilostomatidae, Trematoda)

Trematodes are one of the most remarkable animals with complex life cycles with several generations. Life histories of a parasitic flatworms include several stages with disparate morphological and physiological characteristics follow each other and infect hosts ranging from mollusks to higher vertebrates. How does one genome regulate the development of various life forms and how many genes are needed to the functioning of each stages? How similar are molecular signatures of life stages in closely related species of parasitic flatworms? Here we present the comparative analysis of transcriptomic signatures of the rediae, cercaria and adult worm stages in two representatives of the family Psilostomatidae (Echinostomata, Trematoda) - Psilotrema simillimum and Sphaeridiotrema pseudoglobulus. Our results indicate that the transitions between the stages of the complex life cycle are associated with massive changes in gene expression with thousands of genes being stage-specific. In terms of expression dynamics, the adult worm is the most similar stage between Psilotrema and Spaeridiotrema, while expression patterns of genes in the rediae and cercariae stages are much more different. This study provides transcriptomic evidences not only for similarities and differences between life stages of two related species, but also for cryptic species in Sphaeridiotrema.

zoology↗

Metabolic co-dependence drives the evolutionary ancient Hydra-Chlorella symbiosis

Many multicellular organisms rely on symbiotic associations for support of metabolic activity, protection, or energy. Understanding the mechanisms involved in controlling such interactions remains a major challenge. In an unbiased approach we identified key players that control the symbiosis between Hydra viridissima and its photobiont Chlorella sp. A99. We discovered significant upregulation of Hydra genes encoding a phosphate transporter and glutamine synthetase suggesting regulated nutrition supply between host and symbionts. Interestingly, supplementing the medium with glutamine temporarily supports in vitro growth of the otherwise obligate symbiotic Chlorella, indicating loss of autonomy and dependence on the host. Genome sequencing of Chlorella A99 revealed a large number of amino acid transporters and a degenerated nitrate assimilation pathway, presumably as consequence of the adaptation to the host environment. Our observations portray ancient symbiotic interactions as a codependent partnership in which exchange of nutrients appears to be the primary driving force.

evolutionary biology↗