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Yoshida, M.-a.

Publications and source records attributed to Yoshida, M.-a..

8 recordsLinked to original sources

Nationwide multi-omics profiling of Japanese jack mackerel reveals geographic gut microbiome structuring despite host panmixia

Host genetic markers often fail to resolve regional origins in highly connected or panmictic marine species. The Japanese jack mackerel, Trachurus japonicus, is a commercially important fishery species around Japan that shows little or no detectable population structure. Here, we used nationwide multi-omics profiling to compare host genomic variation and gut microbiome composition in wild T. japonicus collected from coastal regions across Japan. We generated MIG-seq data for 43 individuals and 16S rRNA gene profiles for 24 individuals; after quality filtering, 19 individuals remained for matched host-microbiome comparison. Genome-wide host SNP analyses showed weak or absent geographic population structure, consistent with previous evidence of panmixia in Japanese waters. In contrast, gut microbiome composition showed geographic structuring based on Bray-Curtis dissimilarity and PERMANOVA, and this pattern was not explained by proximity to river mouths or host-related variables. Locality- or individual-associated bacterial lineages contributed to the observed differences in the microbiome, while chloroplast-associated and Cyanobacteria-assigned ASVs suggested recent dietary or environmental input. These results indicate that gut microbiome can show regional biological variation not apparent from host genetic markers alone. Our study provides a proof-of-concept example of integrating host genomics and gut microbiome profiling to evaluate regional characteristics and origins in highly connected marine animals.

microbiology↗

Microstructural architecture of the argonauts' shell-like eggcase reveals the formation logic of a convergent extended phenotype

Argonautid octopods of the genus Argonauta possess a shell-like biomineralized external structure called an eggcase. A classical behavioral observation suggested that this structure is produced by the first dorsal arms rather than by the mantle tissue as seen in typical molluscan shells. In this study, we performed detailed microstructural analyses using scanning electron microscopy to investigate the characteristics of normal, undamaged eggcases and regions that had undergone post-damage repair. Our analysis revealed that the eggcase comprises five layers: an outermost organic membrane, an outer spherulitic-fibrous prismatic layer, a middle organic layer, an inner spherulitic-fibrous prismatic layer, and an innermost organic membrane. Both prismatic layers exhibit bidirectional growth from the middle organic layer, a unique feature not observed in typical molluscan shells. We propose a four-stage formation sequence to explain the observed microstructural architecture: nucleation on the organic scaffold, bidirectional crystal growth from the organic mid-layer, perpendicular growth relative to the eggcase surface, and final encapsulation by an organic membrane. Interestingly, the growth pattern and crystal shapes in the prismatic layers resemble of the internalized shells of cuttlefish, the calcified skeleton of stony corals, and avian eggshells, suggesting functional convergence. We also identified two repair mechanisms: reattachment of broken fragments and regeneration via new secretions. These findings call into question the previous assumptions about the role of the first dorsal arms in calcification. The eggcase also exemplifies the formation of a functionally and structurally complex extended phenotype through convergence.

zoology↗

Chromosomal fusions and subsequent rearrangements shaped octopus genomes

Why some animal groups retain ancestral chromosomal complements while others change significantly is a fundamental question in evolutionary genomics. Few systems exist where accumulations of chromosomal changes can be studied in the context of morphological innovation. In coleoid cephalopods (octopus, squid, cuttlefish), an ancient coleoid chromosomal rearrangement event (ACCRE) has led to a substantial increase in the chromosome number and a new set of chromosomal homologies. Compared to typical molluscan or bilaterian genomes, ACCRE has enabled the origin of many novel regulatory regions in coleoid cephalopods. However, the discrepancies between extant octopodiform (octopus, [~]30 chromosomes) and decapodiform (squid and cuttlefish, [~]46 chromosomes) karyotypes and the direction of these evolutionary changes remain unexplained. Here we provide a draft genome assembly of the vampire squid Vampyroteuthis sp., the largest cephalopod genome sequenced to-date (over 10 gigabasepairs). Through syntenic comparisons, we infer that this basally branching octopodiform species shows partial retention of the chromosomal complement of Decapodiformes, indicating its more ancestral state and the derived nature of the octopod karyotype. Together with the analysis of a new chromosome-level assembly of the pelagic octopod Argonauta hians, we identified irreversible chromosomal fusion-with-mixing events followed by inter-chromosomal translocations in octopods. We show that this secondary reduction and mixing within octopod chromosomes has enabled the origin of a more entangled genomic configuration, shedding light onto the early evolutionary transitions within the clade. Our results offer broader insights into general patterns of chromosomal evolution following large-scale rearrangement events in animal genomes. Significance statementHow changes to the ancient animal synteny result in novel chromosomal homologies is difficult to dissect due to the lack of intermediate states. Here we report that the genome of Vampyroteuthis, one of the largest animal genomes sequenced to-date (over 11 gigabasepairs), despite its phylogenetic position within the octopodiform cephalopods, partially retains squid and cuttlefish chromosomal complement, reflecting an ancestral karyotypic state that existed at the time of divergence between these cephalopod lineages. Our findings reveal karyotype reductions through chromosomal fusions were followed by inter-chromosomal translocations in octopods, leading to a more specialized genomic and gene regulatory architecture. These data show how chromosomal fusions can act as drivers of further inter-chromosomal rearrangements in animal genomes.

genomics↗

Mineral phase analysis of various marine-species shells and skeletons collected in Japan: Implications for marine biominerals

Mineral phase analysis was performed, using X-ray diffractometry (XRD), for marine-organism shell/skeleton samples of 146-148 extant species of the following 10 phyla (18 classes) collected in Japan: Rhodophyta (Florideophyceae), Foraminifera (Globothalamea and Tubothalamea), Porifera (Hexactinellida), Cnidaria (Anthozoa and Hydrozoa), Bryozoa (Gymnolaemata), Brachiopoda (Lingulata and Rhynchonellata), Mollusca (Bivalvia, Cephalopoda, Gastropoda and Polyplacophora), Annelida (Polychaeta), Arthropoda (Cirripedia), and Echinodermata (Asteroidea, Crinoidea and Echinoidea). Some of the species were analyzed for each specific part of their shells/skeletons. Almost all the samples exhibited any of calcite, aragonite or their mixed phase, predominantly depending on their taxonomy and shell/skeletal structures. For samples containing significant amounts of calcite, the MgCO3 wt % of calcite has been determined from their XRD data, which ranges from [~]0 to [~]15 wt % and indicates clear inter-taxonomic differences. Low MgCO3 values ([~]0-4 wt %) are observed for Rhynchonellata, Bivalvia, Gastropoda and Cirripedia; intermediate values ([~]4-8 wt %) for Cephalopoda; high values ([~]8-15 wt %) for Florideophyceae, Globothalamea, Tubothalamea, Polychaeta, Asteroidea and Crinoidea; low-to-high values for Gymnolaemata; intermediate-to-high values for Anthozoa and Echinoidea. These MgCO3 data show broad trends mostly consistent with general phylogenetic evolution (i.e. very similar patterns for each phylogenetic group). Distinct within-individual variability of the MgCO3 content is found for regular Echinoidea species (i.e. their teeth and spines have lower MgCO3 values than the other skeletal parts). Correlation of the MgCO3 content with seawater temperature is also examined/discussed for most of the above calcite-containing classes. In order to interpret our XRD-based observations of various marine-species shells/skeletons, detailed discussions are presented by comparing with previous studies and also by using knowledge of taxonomy, shell/skeletal structures, habitats, living modes and so on. The comprehensive dataset and discussions will provide useful implications for biomineralization studies.

zoology↗

Gene recruitments and dismissals in argonaut octopus genome provide insights to pelagic lifestyle adaptation and shell-like eggcase reacquisition

The paper nautilus, Argonauta argo, also known as the greater argonaut, is a species of octopods distinctly characterized by its pelagic lifestyle and by the presence of a spiral-shaped shell-like eggcase in females. The eggcase functions by protecting the eggs laid inside it, and by building and keeping air intakes for buoyancy. To reveal the genomic background of the species adaptation to pelagic lifestyle and the acquisition of its shell-like eggcase, we sequenced the draft genome sequence of the species. The genome size was 1.1 Gb, which is the smallest among the cephalopods known to date, with the top 215 scaffolds (average length 5,064,479 bp) covering 81% (1.09 Gb) of the total assembly. A total of 26,433 protein-coding genes were predicted from 16,802 assembled scaffolds. From these, we identified nearly intact HOX, Parahox, Wnt clusters and some gene clusters probably related to the pelagic lifestyle, such as reflectin, tyrosinase, and opsin. For example, opsin might have undergone an extensive duplication in order to adapt to the pelagic lifestyle, as opposed to other octopuses, which are mostly the benthic. Our gene models also discovered several genes homologous to those related to calcified shell formation in Conchiferan Mollusks, such as Pif-like, SOD, and TRX. Interestingly, comparative genomics analysis revealed that the homologous genes for such genes were also found in the genome of the octopus, which does not have a shell, as well as the basal cephalopods Nautilus. Therefore, the draft genome sequence of A. argo we presented here had not only helped us to gain further insights into the genetic background of the dynamic recruitment and dismissal of genes for the formation of an important, converging extended phenotypic structure such as the shell and the shell-like eggcase, but also the evolution of lifestyles in Cephalopods and the octopods, from benthic to pelagic.

genomics↗

Independent adoptions of a set of proteins found in the matrix of the mineralized shell-like eggcase of Argonaut octopuses

The Argonaut octopus, commonly called the paper nautilus, has a spiral-coiled shell-like eggcase. As the main characteristics, the eggcase has no internal septum, is composed entirely of calcite with chitosan being the main polycarbonate and is reportedly formed by organic materials secreted from the membranes of the arms. Meanwhile, the biomineralized external "true" shells of the Mollusks, which includes the Cephalopods, are secreted from the mantle tissue. Therefore, the histological origin of the two shells is completely different. The question of how the Argonauts, which phylogenetically diverged from the completely shell-less octopuses, could form a converging shell-like external structure has thus intrigued biologists for a long time. To answer this question, we performed a multi-omics analysis of the transcriptome and proteome of the two congeneric Argonaut species, Argonauta argo and A. hians. Our result indicates that the shell-like eggcase is not a homolog of the shell, even at the protein level, because the Argonauts apparently recruited a different set of protein repertoires to as eggcase matrix proteins (EcMPs). However, we also found the homologs of three shell matrix proteins (SMPs) of the Conchiferan Mollusks, Pif-like, SOD, and TRX, in the eggcase matrix. The proteins were also found in the only surviving shelled Cephalopods, the nautiloid Nautilus pompilius. Phylogenetic analysis revealed that homologous genes of the Conchiferan SMPs and EcMPs were found in the draft genome of shell-less octopuses. Our result reported here thus suggests that the SMP-coding genes are conserved in both shelled and shell-less Cephalopods. Meanwhile, the Argonauts adopted some of the SMP-coding genes and other non-SMP-coding genes, to form a convergent, non-homologous biomineralized external structure, the eggcase, which is autapomorphic to the group.

evolutionary biology↗

Hydrophilic Shell Matrix Proteins of Nautilus pompilius and The Identification of a Core Set of Conchiferan Domains

Despite being a member of the shelled mollusks (Conchiferans), most members of extant cephalopods have lost their external biomineralized shells, except for the Nautiloids. Here, we report the result of our study to identify major Shell Matrix Proteins and their domains in the Nautiloid Nautilus pompilius, in order to gain a general insight into the evolution of Conchiferan Shell Matrix Proteins. In order to do so, we conducted transcriptomics of the mantle, and proteomics of the shell of N. pompilius simultaneously. Analyses of obtained data identified 61 distinct shell-specific sequences. Of the successfully annotated 27 sequences, protein domains were predicted in 19. Comparative analysis of Nautilus sequences with four Conchiferans for which Shell Matrix Protein data were available (the pacific oyster, the pearl oyster, the limpet, and the Euhadra snail) revealed that three proteins and six domains of the shell proteins are conserved in all Conchiferans. Interestingly, when the terrestrial Euhadra snail was excluded, another five proteins and six domains were found to be shared among the four marine Conchiferans. Phylogenetic analyses indicated that most of these proteins and domains were present in the ancestral Conchiferan, but employed in shell formation later and independently in most clades. Although further studies utilizing deeper sequencing techniques to obtain genome and full-length sequences, and functional analyses, must be done in the future, our results here provide important pieces of information for the elucidation of the evolution of Conchiferan shells at the molecular level.

zoology↗

Polyandry is extremely rare in the firefly squid, Watasenia scintillans

Although polygamy has versatile benefits for both sexes, many species favor monogamy for reasons with the clarity or unclarity. In cephalopods, all species are regarded to be polygamous, which could be attributed to their common life-history traits. Contrary to this prediction, we show empirical evidence for monogamy in the firefly squid, Watasenia scintillans. The peak spawning season comes after male disappearance owning to long-reserved spermatangia deposited by male at exact locations (bilateral pouches under neck collar) on female with a symmetric distribution. Such a non-random placement of spermatangia prompted us to hypothesize that females engage in lifetime monoandry. Hence we assigned genotypes of female-stored spermatangia and offspring. We found that in 94.7 % females, the spermatangia were delivered from a single male and all embryos in the same egg string sired by sperm from stored spermatangia. Throughout the season, relative testes mass was much smaller in W. scintillans than all other cephalopods previously examined. The mean number of male-stored spermatophores was approximately 30, the equivalent to 2.5 mates. Our demographic and morphometrical data agree with the prediction that monogyny is favored when potential mates are scarce such as absence of female remating. Together, these results suggest the likelihood of mutual monogamy.

ecology↗