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Satoh, N.

Publications and source records attributed to Satoh, N..

At least 19 recordsLinked to original sources

Evolutionary landscapes of zygotic genome activation across animals

During early animal embryogenesis, gene expression control shifts from maternally deposited products to newly transcribed RNA through zygotic genome activation (ZGA). Although essential and universal, ZGA remains poorly understood outside a few model species. Here, we generated a transcriptomic atlas of early embryogenesis across 61 animal species from 13 phyla and used a unified computational framework to infer ZGA timing systematically. We find extensive variation in ZGA onset across animals, but show that the ratio between genome size and egg cytoplasmic volume, a proxy for the nuclear-to-cytoplasmic ratio, robustly predicts when genome activation begins. We also reveal that zygotic genes also differ from maternal transcripts in genomic architecture, function and evolutionary conservation, suggesting that ZGA follows a conserved molecular logic despite flexible transcriptomic outputs.

evolutionary biology↗

Establishing genetically controlled, closed 1 colonies of an ascidian

Recent technological advances have made many "non-model" organisms accessible for experimental studies. However, reference inbred strains were not necessarily available, especially in marine invertebrates, and genetic background of organisms used for experiments are often non-uniform. This situation potentially affects experimental reproducibility. Although ascidians, Ciona intestinalis (type A, or C. robusta), are a widely used marine animal for many areas of experimental biology including developmental studies, no reference strains have been obtained despite extensive efforts. As an alternative way to improve reproducibility, we have established and maintained ascidian colonies through intra-population breeding every year from 2016 to 2020, and monitored genomic variants of these colonies. This method does not reduce genetic variations but instead manages and monitors genetic variations in the colonies, providing an easy and cost-effective way of increasing experimental reproducibility. Furthermore, we recently upgraded these genetically isolated, closed colonies that were re-established every year, and have maintained them for more than three years only through intra-population breeding and occasional back-cross using cryopreserved sperm. Genetic variants that we revealed using 3.7 tera-bases of sequence data will help to design future experiments in this species. Our data also show that two wild-populations, which were used to establish the colonies, have maintained distinct genetic backgrounds, although their habitats are directly linked to the Pacific Ocean and only 170 km apart. More importantly, genetic information regarding these colonies will undoubtedly improve experimental reproducibility and traceability, and our method will provide a realistic solution for performing reproducible experiments using non-model organisms.

developmental biology↗

The complete mitochondrial genomes of Litophyton sp. and Stereonephthya sp., members of family Nephtheidae (Cnidaria: Anthozoa: Octocorallia).

In this study, we sequenced the complete mitochondrial genomes (mitogenome) of Litophyton sp. and Stereonephthya sp. (family Nephtheidae), collected in Okinawa, Japan. The complete mitogenomes of Litophyton sp. and Stereonephthya sp. were 19,130 bp and 18,912 bp in length, respectively. They contained 17 genes (14 protein-coding genes, two rRNA genes, and one tRNA gene) and exhibited gene order pattern "A", which is the most common arrangement among octocorals. Molecular phylogenetic analysis indicated that Litophyton sp. And Stereonephthya sp. are clustered with other species belonging to family Nephtheidae, consistent with the previous research using partial mitochondrial genes. Our study provides additional mitochondrial genomic resources that contributes to comparative studies of octocoral mitogenomes.

genomics↗

The complete mitochondrial genome of Hanabira yukibana Lau, Stokvis, Imahara & Reimer, 2019 (Cnidaria: Anthozoa: Octocorallia)

In this study, we sequenced the complete mitochondrial genome (mitogenome) of Hanabira yukibana (family Clavulariidae), collected in Okinawa, Japan. The complete mitochondrial genome of this specimen was 18,690 bp in length and contained 17 genes (14 protein-coding genes, two rRNA genes, and one tRNA gene). It exhibited gene order pattern A, which is the most common arrangement among octocorals. Molecular phylogenetic analysis indicated that H. yukibana is clustered with the genus Clavularia, including Clavularia inflata (the family Clavulariidae), consistent with the previous research using partial mitochondrial genes. Our study provides an additional mitochondrial genomic resource that contributes to comparative studies of octocoral mitogenomes.

genomics↗

The mitochondrial genome of Palythoa tuberculosa (Esper, 1805) contains a novel ORF with unknown function.

Recent advances in sequencing technology have enabled rapid and cost-effective recovery of mitochondrial genomes (mt-genomes), which used in phylogenetic and evolutionary studies. Among cnidarians, the order Zoantharia possesses the largest mt-genomes on average (20,976 bp). Here, we present the complete mt-genome of Palythoa tuberculosa (Hexacorallia: Zoantharia: Sphenopidae), which was 23,044 bp in length--approximately 2,000 bp larger than the zoantharian average. Synteny analysis revealed that this increase resulted from a novel open reading frame (ORF) located between trnW and cox2. This ORF was also present in the closely related species P. caribaeorum, indicating its origin in their common ancestor. Importantly, this represents the first case of a novel ORF insertion in zoantharians, clearly distinct from previously reported ORF extensions. While mt-genome expansions are occasionally observed in cnidarians, both the insertion sites and inserted elements vary among lineages, highlighting the lineage-specific mechanisms driving mitochondrial genome evolution in this group.

genomics↗

Shifts in Coral Reef Holobiont Communities in the High-CO2 Marine Environment of Iotorishima Island

Ocean acidification (OA), driven by rising atmospheric CO2, presents a serious threat to marine biodiversity, especially within coral reef ecosystems. Natural analogue sites, such as the high-pCO2 seep at I[o]torishima Island in Japan, offer insights into future conditions. This study investigated the holobiont communities of Symbiodiniaceae and bacteria in the zoantharian Palythoa tuberculosa at I[o]torishima and compared them to specimens from control sites in Okinawa and Hawaii. Using amplicon sequencing of the dinoflagellate internal transcribed spacer 2 (ITS2) region of ribosomal DNA and microbial 16S rRNA gene, we detected significant shifts in both Symbiodiniaceae and bacterial communities under high-pCO2 conditions at I[o]torishima. Specifically, P. tuberculosa at the seep site had reduced Symbiodiniaceae diversity, predominatly featuring Cladocopium C1 and C3 types. Additionally, its bacterial communities showed lower richness with distinct taxonomic profiles, including increased levels of Mollicutes and Vibrio spp. These results highlight the potentially adverse effects of OA on hexacoral holobionts and emphasize the need for detailed, high-resolution studies across various holobiont species and geographic locations. The shifts observed specifically in Symbiodiniaceae and bacterial communities at the I[o]torishima Seep suggest that holobionts may exhibit plasticity in response to environmental stress, which has implications for resilience and adaptation of zoantharians and other reef organisms amid climate change. This research provides crucial baseline data for predicting future coral reef compositions in an OA-affected world.

microbiology↗

Brachiopod genome unveils the evolution of the BMP-Chordin network in bilaterian body patterning

Bone morphogenetic protein (BMP) signalling is crucial in regulating dorsal-ventral patterning and cell fate determination during early development in bilaterians. Interactions between BMP ligands and their main antagonist, Chordin, establish BMP gradients, subdivide embryos into distinct territories and organise body plans. However, the molecular control and evolutionary origins of dorsal-ventral patterning within spiralians, one of the three major bilaterian groups, have been obscured by their unique embryonic development. Here we present the chromosome-level genome of a spiralian with deuterostome-like development, the brachiopod Lingula anatina, and apply functional transcriptomics to study dorsal-ventral patterning under the control of BMP signalling. We uncover the presence of a dorsal-ventral BMP signalling gradient in the L. anatina gastrula with bmp2/4 and chordin expressed at its dorsal and ventral sides, respectively. Using small-molecule drugs, exogenous recombinant BMP proteins and RNA sequencing, we show that a high level of BMP pathway activation inhibits the expression of neural genes during gastrula and larval stages. We also show that BMP signalling splits the developing larval shell field into two valves. The discovery of a BMP-mediated dorsal-ventral patterning system in a spiralian, similar to those observed in deuterostomes and non-spiralian protostomes, suggests deep conservation of this mechanism across all three major bilaterian clades. This is further supported by striking similarities in the gene sets regulated by BMP signalling in brachiopods and the vertebrate model Xenopus. We argue that the spiralian ancestor retained the basal bilaterian mechanism of dorsal-ventral patterning, although downstream components of the BMP-Chordin network have undergone dynamic evolutionary changes.

evolutionary biology↗

A genome and tissue-specific transcriptomes of the large-polyp coral, Fimbriaphyllia (Euphyllia) ancora: Recipe for a coral polyp

Coral "polyps" are composed of several tissues; however, their characteristics are largely unexplored. Here we report biological characteristics of the four tissues that comprise polyps: tentacle (Te), mesenterial filament (Me), body wall (Bo), and mouth with pharynx (MP), using comparative genomic, morpho-histological, and transcriptomic analyses of the large-polyp coral, Fimbriaphyllia ancora. A draft F. ancora genome assembly of 434 Mbp was created. Morpho-histological and transcriptomic characterization of the four tissues showed that they have distinct differences in structure, primary cellular composition, and transcriptional profiles. Tissue-specific, highly expressed genes (HEGs) of Te are related to biological defense, predation, and coral-algal symbiosis. Me expresses multiple digestive enzymes, whereas Bo expresses innate immunity and biomineralization-related molecules. Many receptors for neuropeptides and neurotransmitters are expressed in MP. The established dataset and new insights into tissue functions will facilitate a deeper understanding of coral biology.

genomics↗

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↗

Coral larvae suppress the heat stress response during the onset of symbiosis thereby decreasing their odds of survival

The endosymbiosis between most corals and their photosynthetic dinoflagellate partners begins early in the host life history, when corals are larvae or juvenile polyps. The capacity of coral larvae to buffer climate-induced stress while in the process of symbiont acquisition could come with physiological trade-offs that alter larval behavior, development, settlement and survivorship. Here we examined the joint effects of thermal stress and symbiosis onset on colonization dynamics, survival, metamorphosis and host gene expression of Acropora digitifera larvae. We found that thermal stress decreased symbiont colonization of hosts by 50% and symbiont density by 98.5% over two weeks. Temperature and colonization also influenced larval survival and metamorphosis in an additive manner, where colonized larvae fared worse or prematurely metamorphosed more often than non-colonized larvae under thermal stress. Transcriptomic responses to colonization and thermal stress treatments were largely independent, while the interaction of these treatments revealed contrasting expression profiles of genes that function in the stress response, immunity, inflammation and cell cycle regulation. The combined treatment either canceled or lowered the magnitude of expression of heat-stress responsive genes in the presence of symbionts, revealing a physiological cost to acquiring symbionts at the larval stage with elevated temperatures. In addition, host immune suppression, a hallmark of symbiosis onset under ambient temperature, turned to immune activation under heat stress. Thus, by integrating the physical environment and biotic pressures that mediate pre-settlement event in corals, our results suggest that colonization may hinder larval survival and recruitment creating isolated, genetically similar populations under projected climate scenarios.

ecology↗

Multi-omics analysis reveals cross-organism interactions in coral holobiont

Corals create an ecosystem, called a holobiont, with intracellular algae (zooxanthellae) and resident bacteria. Zooxanthellae and some bacteria play major roles in the physiological properties of the coral host. However, because of the difficulties in experimental verification of cross-organism interactions, the mechanisms underpinning these interactions are largely unknown. To address this, we here generated and then analyzed multi-omics datasets for corals, zooxanthellae, and bacteria collected at Okinawa, Japan, from November 2014 to September 2016. Using cross-organism co-expression analysis, we successfully characterized the host-alga relationship in the coral holobiont. Specifically, we observed that the coral host dominates the zooxanthellae. The multi-omics analysis also suggested that infection with coral-associated bacteria Endozoicomonas likely involves coral-like ephrin ligands, triggering an immune response of the coral host. This study highlights the potential of the multi-omics approach to elucidate coral-microbe interactions.

systems biology↗

A root for massive crown-of-thorns starfish outbreaks in the Pacific Ocean

Recurring outbreaks of crown-of-thorns starfish (COTS) severely damage healthy corals in the Western Pacific Ocean. To determine the source of outbreaking COTS larvae and their dispersal routes across the Western Pacific, complete mitochondrial genomes were sequenced from 243 individuals collected in 11 reef regions. Our results indicate that Pacific COTS comprise two major clades, an East-Central Pacific clade (ECP-C) and a Pan-Pacific clade (PP-C). The ECP-C consists of COTS from French Polynesia (FP), Fiji, Vanuatu and the Great Barrier Reef (GBR), and does not appear prone to outbreaks. In contrast, the PP-C, which repeatedly spawns outbreaks, is a large clade comprising COTS from FP, Fiji, Vanuatu, GBR, Papua New Guinea, Vietnam, the Philippines, Japan, Micronesia, and the Marshall Islands. Given the nature of Pacific Ocean currents, the vast area encompassing FP, Fiji, Vanuatu, and the GBR likely supplies larvae for repeated outbreaks, exacerbated by anthropogenic environmental changes, such as eutrophication.

ecology↗

Oxidized alkyl phospholipids stimulate sodium transport in proximal tubules via PPAR-dependent pathway

The pleiotropic effects of oxidized phospholipids (oxPLs) have been identified. 1-O-hexadecyl-2-azelaoyl-sn-glycero-3-phosphocholine (azPC), an oxPL formed from alkyl phosphatidylcholines, is a potent peroxisome proliferator-activated receptor {gamma} (PPAR{gamma}) agonist. Although it has been reported that thiazolidinediones can induce volume expansion by enhancing renal sodium and water retention, the role of azPC, an endogenous PPAR{gamma} agonist, in renal transport functions is unknown. In the present study, we investigated the effect of azPC on renal proximal tubule (PT) transport using isolated PTs and kidney cortex tissues. We showed that azPC rapidly stimulated Na+/HCO3- cotransporter 1 activity and luminal Na+/H+ exchanger (NHE) activities in a dose-dependent manner, at submicromolar concentrations, in isolated PTs from rats and humans. Additionally, the stimulatory effects were completely blocked by a specific PPAR{gamma} antagonist, 2-chloro-5-nitro-N-phenylbenzamide (GW9662), and a mitogen-activated protein/extracellular signal-regulated kinase (MEK) inhibitor, PD98059. Treatment with an siRNA against PPAR{gamma} significantly suppressed the expression of PPAR{gamma} mRNA, and it completely blocked the stimulation of both Na+/HCO3- cotransporter 1 and NHE activities by azPC. Moreover, azPC induced extracellular signal-regulated kinase (ERK) phosphorylation in rat and human kidney cortex tissues, and the induced ERK phosphorylation by azPC was completely suppressed by GW9662 and PD98059. These results suggest that azPC stimulates renal PT sodium-coupled bicarbonate transport via the PPAR{gamma}/MEK/ERK pathway. The stimulatory effects of azPC on PT transport may be partially involved in the development of volume expansion.

physiology↗

Color morphs of the coral, Acropora tenuis, show different responses to environmental stress and different expression profiles of fluorescent-protein genes

Corals of the family Acroporidae are key structural components of reefs that support the most diverse marine ecosystems. Due to increasing anthropogenic stresses, coral reefs are in decline. Along the coast of Okinawa, Japan, three different color morphs of Acropora tenuis have been recognized for decades. These include brown (N morph), yellow-green (G) and purple (P) forms. The tips of axial coral polyps exhibit specific fluorescence spectra. This attribute is inherited asexually, and color morphs do not change seasonally. In Okinawa Prefecture, during the summer of 2017, the N and P morphs experienced bleaching, in which some N morphs died while P morphs recovered. In contrast, G morphs successfully withstood the stress. Symbiotic dinoflagellates are essential symbiotic partners of scleractinian corals. Photosynthetic activity of symbionts was reduced in July in N and P morphs; however, the three color-morphs host similar sets of Clade-C zoothanthellae, suggesting that beaching of N and P morphs cannot be attributed to differences in symbiont clades. The decoded Acropora tenuis genome includes five genes for green fluorescent proteins (GFP), two for cyan fluorescent proteins (CFP), three for red fluorescent proteins (RFP), and seven genes for chromoprotein (ChrP). A summer survey of gene expression profiles demonstrated that (a) expression of CFP and REP was quite low in all three morphs, (b) P morphs expressed higher levels of ChrP, (c) both N and G morphs expressed GFP highly, and (d) GFP expression was reduced in N morphs, compared to G morphs, which maintained higher levels of GFP expression throughout the summer. Although further studies are required to understand the biological significance of these color morphs of Acropora tenuis, our results suggest that thermal stress resistance is modified by genetic mechanisms that coincidentally lead to diversification of color morphs.

evolutionary biology↗

Chloroplast acquisition without the gene transfer in kleptoplastic sea slugs

Some sea slugs sequester chloroplasts from algal food in their intestinal cells and photosynthesize for months. This phenomenon, kleptoplasty, poses a question of how the chloroplast retains its activity without the algal nucleus. There have been debates on the horizontal transfer of algal genes to the animal nucleus. To settle the arguments, this study reported the genome of a kleptoplastic sea slug Plakobranchus ocellatus and found no evidence of photosynthetic genes encoded on the nucleus. Nevertheless, it was confirmed that light illumination prolongs the life of mollusk under starvation. These data presented a paradigm that a complex adaptive trait, as typified by photosynthesis, can be transferred between eukaryotic kingdoms by a unique organelle transmission without nuclear gene transfer. Our phylogenomic analysis showed that genes for proteolysis and immunity undergo gene expansion and are up-regulated in chloroplast-enriched tissue, suggesting that these molluskan genes are involved in the DNA-independent phenotype acquisition.

evolutionary biology↗

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↗

GenoDup Pipeline: a tool to detect genome duplication using the dS-based method

Understanding whole genome duplication (WGD), or polyploidy, is fundamental to investigating the origin and diversification of organisms in evolutionary biology. The wealth of genomic data generated by next generation sequencing (NGS) has resulted in an urgent need for robust and accurate tools to detect WGD. Here, we present a useful and user-friendly pipeline called GenoDup for inferring WGD using the dS-based method. We have successfully applied GenoDup to identify WGD in empirical data from both plants and animals. The GenoDup Pipeline provides a reliable and useful tool to infer WGD from NGS data.

bioinformatics↗

Comparative genomics-first approach to understand diversification of secondary metabolite biosynthetic pathways in symbiotic dinoflagellates

Symbiotic dinoflagellates of the genus Symbiodinium are photosynthetic and unicellular. They possess smaller nuclear genomes than other dinoflagellates and produce structurally specialized, biologically active, secondary metabolites. Polyketide biosynthetic genes of toxic dinoflagellates have been studied extensively using transcriptomic analyses; however, a comparative genomic approach to understand secondary metabolism has been hampered by their large genome sizes. Here, we use a combined genomic and metabolomics approach to investigate the structure and diversification of secondary metabolite genes to understand how chemical diversity arises in three decoded Symbiodinium genomes (A3, B1 and C). Our analyses identify 71 polyketide synthase and 41 non-ribosomal peptide synthetase genes from two newly decoded genomes of clades A3 and C. Additionally, phylogenetic analyses indicate that almost all of the gene families are derived from lineage-specific gene duplications in Symbiodinium clades, suggesting divergence for environmental adaptation. Few metabolic pathways are conserved among the three clades and we detect metabolic similarity only in the recently diverged clades, B1 and C. We establish that secondary metabolism protein architecture guides substrate specificity and that gene duplication and domain shuffling have resulted in diversification of secondary metabolism genes.

genomics↗