Details of a Researcher - Arakawa, Kazuharu

Papers - Arakawa, Kazuharu

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Patterns of population structure and complex haplotype sharing among field isolates of the green alga Chlamydomonas reinhardtii

Craig R.J., Böndel K.B., Arakawa K., Nakada T., Ito T., Bell G., Colegrave N., Keightley P.D., Ness R.W.

Molecular Ecology (Molecular Ecology) 28 ( 17 ) 3977 - 3993 2019.09

ISSN 09621083

© 2019 John Wiley & Sons Ltd The nature of population structure in microbial eukaryotes has long been debated. Competing models have argued that microbial species are either ubiquitous, with high dispersal and low rates of speciation, or that for many species gene flow between populations is limited, resulting in evolutionary histories similar to those of macroorganisms. However, population genomic approaches have seldom been applied to this question. Here, we analyse whole-genome resequencing data for all 36 confirmed field isolates of the green alga Chlamydomonas reinhardtii. At a continental scale, we report evidence for putative allopatric divergence, between both North American and Japanese isolates, and two highly differentiated lineages within N. America. Conversely, at a local scale within the most densely sampled lineage, we find little evidence for either spatial or temporal structure. Taken together with evidence for ongoing admixture between the two N. American lineages, this lack of structure supports a role for substantial dispersal in C. reinhardtii and implies that between-lineage differentiation may be maintained by reproductive isolation and/or local adaptation. Our results therefore support a role for allopatric divergence in microbial eukaryotes, while also indicating that species may be ubiquitous at local scales. Despite the high genetic diversity observed within the most well-sampled lineage, we find that pairs of isolates share on average ~9% of their genomes in long haplotypes, even when isolates were sampled decades apart and from different locations. This proportion is several orders of magnitude higher than the Wright–Fisher expectation, raising many further questions concerning the evolutionary genetics of C. reinhardtii and microbial eukaryotes generally.

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Complete genome sequence of halophilic deep-sea bacterium halomonas axialensis strain Althf1

Tsurumaki M., Deno S., Galipon J., Arakawa K.

Microbiology Resource Announcements (Microbiology Resource Announcements) 8 ( 31 ) 2019.08

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Complete genome sequence of halomonas sulfidaeris strain esulfide1 isolated from a metal sulfide rock at a depth of 2,200 meters, obtained using nanopore sequencing

Saito M., Nishigata A., Galipon J., Arakawa K.

Microbiology Resource Announcements (Microbiology Resource Announcements) 8 ( 23 ) 2019.06

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Nanopore sequencing: Review of potential applications in functional genomics

Kono N., Arakawa K.

Development Growth and Differentiation (Development Growth and Differentiation) 61 ( 5 ) 316 - 326 2019.06

ISSN 00121592

© 2019 Japanese Society of Developmental Biologists Molecular biology has been led by various measurement technologies, and increased throughput has developed omics analysis. The development of massively parallel sequencing technology has enabled access to fundamental molecular data and revealed genomic and transcriptomic signatures. Nanopore sequencers have driven such evolution to the next stage. Oxford Nanopore Technologies Inc. provides a new type of single molecule sequencer using protein nanopore that realizes direct sequencing without DNA synthesizing or amplification. This nanopore sequencer can sequence an ultra-long read limited by the input nucleotide length, or can determine DNA/RNA modifications. Recently, many fields such as medicine, epidemiology, ecology, and education have benefited from this technology. In this review, we explain the features and functions of the nanopore sequencer, introduce various situations where it has been used as a critical technology, and expected future applications.

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Complete genome sequence of halomonas olivaria, a moderately halophilic bacterium isolated from olive processing effluents, obtained by nanopore sequencing

Nagata S., Ii K., Tsukimi T., Miura M., Galipon J., Arakawa K.

Microbiology Resource Announcements (Microbiology Resource Announcements) 8 ( 18 ) 2019.05

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Complete genome sequence of Psychrobacter sp. Strain KH172YL61, isolated from deep-sea sediments in the Nankai Trough, Japan

Evans-Yamamoto D., Takeuchi N., Masuda T., Murai Y., Onuma Y., Mori H., Masuyama N., Ishiguro S., Yachie N., Arakawa K.

Microbiology Resource Announcements (Microbiology Resource Announcements) 8 ( 16 ) 2019.04

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Anti-tumor effects and potential therapeutic response biomarkers in α-emitting meta-<sup>211</sup>At-astato-benzylguanidine therapy for malignant pheochromocytoma explored by RNA-sequencing

Ohshima Y., Kono N., Yokota Y., Watanabe S., Sasaki I., Ishioka N.S., Sakashita T., Arakawa K.

Theranostics (Theranostics) 9 ( 6 ) 1538 - 1549 2019

© Ivyspring International Publisher. Targeted α-particle therapy is a promising option for patients with malignant pheochromocytoma. Recent observations regarding meta-211At-astato-benzylguanidine (211At-MABG) in a pheochromocytoma mouse model showed a strong anti-tumor effect, though the molecular mechanism remains elusive. Here, we present the first comprehensive RNA-sequencing (RNA-seq) data for pheochromocytoma cells based on in vitro 211At-MABG administration experiments. Key genes and pathways in the tumor α-particle radiation response are also examined to obtain potential response biomarkers. Methods: We evaluated genome-wide transcriptional alterations in the rat pheochromocytoma cell line PC12 at 3, 6, and 12 h after 211At-MABG treatment; a control experiment using 60Co γ-ray irradiation was carried out to highlight 211At-MABG-specific gene expression. For comparisons, 10% and 80% iso-survival doses (0.8 and 0.1 kBq/mL for 211At-MABG and 10 and 1 Gy for 60Co γ-rays) were used. Results: Enrichment analysis of differentially expressed genes (DEGs) and analysis of the gene expression profiles of cell cycle checkpoints revealed similar modes of cell death via the p53-p21 signaling pathway after 211At-MABG treatment and γ-ray irradiation. The top list of ranked DEGs demonstrated the expression of key genes on the decrease in the survival following 211At-MABG exposure, and four potential genes (Mien1, Otub1, Vdac1 and Vegfa genes) of 211At-MABG therapy. Western blot analysis indicated increased expression of TSPO in 211At-MABG-treated cells, suggesting its potential as a PET imaging probe. Conclusion: Comprehensive RNA-seq revealed contrasting cellular responses to γ-ray and α-particle therapy, leading to the identification of four potential candidate genes that may serve as molecular imaging and 211At-MABG therapy targets.

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Comparison of Sexual Reproductive Behaviors in Two Species of Macrobiotidae (Tardigrada: Eutardigrada)

Sugiura K., Minato H., Suzuki A.C., Arakawa K., Kunieda T., Matsumoto M.

Zoological Science (Zoological Science) 36 ( 2 ) 120 - 127 2019

ISSN 02890003

© 2019 Zoological Society of Japan. Reproductive strategy is an important aspect of biological diversity. In tardigrades, several reproductive modes, including sexual reproduction, are known. However, tardigrade mating behavior has been observed only rarely in most species, and in some cases, especially in the freely ovipositing eutardigrades, remains entirely unknown. In the present study, we cultured two sexually reproducing tardigrade species that lay eggs freely, Paramacrobiotus sp. TYO strain and Macrobiotus shonaicus, to investigate and compare their courtship, mating, and chromosome morphology. Mating behavior was observed and recorded in both species. The entire mating sequence, including courtship, was categorized into five discrete steps common to two species, as follows: [1] Tracking: the male tracks and orientates toward the female; [2] Touching: the male makes contact with the cloaca of the female; [3] Standstill: the female ceases movement until male ejaculation is complete; [4] Ejaculation: the male curls its caudal end and ejaculates into the cloaca from close range; [5] Contraction: the female contracts its ventral side after ejaculation to capture spermatozoa deposited in the external environment in close proximity to the cloaca. Some notable differences between the two species were observed in the steps 3-4. First, oviposition was observed at 40 min in Paramacrobiotus sp. TYO strain, and a few days after mating in M. shonaicus, respectively. Comparisons of chromosome morphology before and after mating indicated that oocytes are arrested at metaphase I in both species. Spermatozoa attach to the interior of the chorion of laid eggs.

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Comparative proteomic analysis of mitochondria isolated from Euglena gracilis under aerobic and hypoxic conditions

Tamaki S., Nishino K., Ogawa T., Maruta T., Sawa Y., Arakawa K., Ishikawa T.

PLoS ONE (PLoS ONE) 14 ( 12 ) 2019

© 2019 Tamaki et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. The unicellular microalga Euglena gracilis produces wax esters for ATP acquisition under low-oxygen conditions. The regulatory mechanism of wax ester production is not yet understood. Indeed, our previous transcriptomic analysis showed that transcript levels of genes involved in the wax ester synthesis hardly changed under hypoxic conditions, suggesting contribution of post-transcriptional regulation. In this study, we conducted a proteome analysis of E. gracilis mitochondria, as this organelle employs the fatty-acid synthesis pathway under hypoxic conditions. Mitochondria were isolated from E. gracilis SM-ZK strain treated with both aerobic and hypoxic conditions and used for shotgun proteomic analysis. Three independent proteomic analyses succeeded in identifying a total of 714 non-redundant proteins. Of these, 229 were detected in common to all experiments, and 116 were significantly recognized as differentially expressed proteins. GO enrichment analysis suggested dynamic changes in mitochondrial metabolic pathways and redox reactions under aerobic and hypoxic conditions. Protein levels of bifunctional enzymes isocitrate lyase and malate synthase in glyoxylate cycle were 1.35-fold higher under hypoxic conditions. Abundances of the propionyl- CoA synthetic enzymes, succinyl-CoA synthetase and propionyl-CoA carboxylase, were also 1.35- and 1.47-fold higher, respectively, under hypoxic conditions. Protein levels of pyruvate: NADP+ oxidoreductase, a key enzyme for anaerobic synthesis of acetyl-CoA, which serves as a C2 donor for fatty acids, showed a 1.68-fold increase under hypoxic conditions, whereas those of pyruvate dehydrogenase subunits showed a 0.77-0.81-fold decrease. Protein levels of the fatty-acid synthesis enzymes, 3-ketoacyl-CoA thiolase isoforms (KAT1 and KAT2), 3-hydroxyacyl-CoA dehydrogenases, and acyl-CoA dehydrogenase were up-regulated by 1.20- to 1.42-fold in response to hypoxic treatment. Overall, our proteomic analysis revealed that wax ester synthesis-related enzymes are up-regulated at the protein level posttranscriptionally to promote wax ester production in E. gracilis under low-oxygen conditions.

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Molecular palaeontology illuminates the evolution of ecdysozoan vision

Fleming J., Kristensen R., Sørensen M., Park T., Arakawa K., Blaxter M., Rebecchi L., Guidetti R., Williams T., Roberts N., Vinther J., Pisani D.

Proceedings of the Royal Society B: Biological Sciences (Proceedings of the Royal Society B: Biological Sciences) 285 ( 1892 ) 2018.12

ISSN 09628452

© 2018 The Authors. Colour vision is known to have arisen only twice—once in Vertebrata and once within the Ecdysozoa, in Arthropoda. However, the evolutionary history of ecdysozoan vision is unclear. At the molecular level, visual pigments, composed of a chromophore and a protein belonging to the opsin family, have different spectral sensitivities and these mediate colour vision. At the morphological level, ecdysozoan vision is conveyed by eyes of variable levels of complexity; from the simple ocelli observed in the velvet worms (phylum Onychophora) to the marvellously complex eyes of insects, spiders, and crustaceans. Here, we explore the evolution of ecdysozoan vision at both the molecular and morphological level; combining analysis of a large-scale opsin dataset that includes previously unknown ecdysozoan opsins with morphological analyses of key Cambrian fossils with preserved eye structures. We found that while several non-arthropod ecdysozoan lineages have multiple opsins, arthropod multi-opsin vision evolved through a series of gene duplications that were fixed in a period of 35 – 71 million years (Ma) along the stem arthropod lineage. Our integrative study of the fossil and molecular record of vision indicates that fossils with more complex eyes were likely to have possessed a larger complement of opsin genes.

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Ultralow input genome sequencing library preparation from a single tardigrade specimen

Yoshida Y., Konno S., Nishino R., Murai Y., Tomita M., Arakawa K.

Journal of Visualized Experiments (Journal of Visualized Experiments) 2018 ( 137 ) 2018.07

ISSN 1940087X

© 2018 Journal of Visualized Experiments. Tardigrades are microscopic animals that enter an ametabolic state called anhydrobiosis when facing desiccation and can return to their original state when water is supplied. The genomic sequencing of microscopic animals such as tardigrades risks bacterial contamination that sometimes leads to erroneous interpretations, for example, regarding the extent of horizontal gene transfer in these animals. Here, we provide an ultralow input method to sequence the genome of the tardigrade, Hypsibius dujardini, from a single specimen. By employing rigorous washing and contaminant exclusion along with an efficient extraction of the 50 ~ 200 pg genomic DNA from a single individual, we constructed a library sequenced with a DNA sequencing instrument. These libraries were highly reproducible and unbiased, and an informatics analysis of the sequenced reads with other H. dujardini genomes showed a minimal amount of contamination. This method can be applied to unculturable tardigrades that could not be sequenced using previous methods.

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The complete mitochondrial genome of Echiniscus testudo (Heterotardigrada: Echiniscidae)

Arakawa K.

Mitochondrial DNA Part B: Resources (Mitochondrial DNA Part B: Resources) 3 ( 2 ) 810 - 811 2018.07

© 2018, © 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. The complete mitchondrial genome of Echiniscus testudo, a cosmopolitan heterotardigrade collected in Japan, has been sequenced using a single molecule real-time (SMRT) sequencing long read after whole genome amplification from a single individual. The genome has a total length of 15,817 bp, consisting of 13 protein-coding genes, 20 tRNA, 2 rRNA genes, and an AT-rich control region. The nucleotide composition was extremely AT-rich, with 78.41% AT. Being in a different class of the phylum Tardigrada, there is a large sequence divergence from the previously reported mitochondrial genome of the eutardigrade Ramazzottius varieornatus, but the gene order of protein-coding genes are mostly conserved. This is the first report of a complete mitochondrial genome of a heterotardigrade.

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The complete mitochondrial genome of Eumeta variegata (Lepidoptera: Psychidae)

Arakawa K., Kono N., Ohtoshi R., Nakamura H., Tomita M.

Mitochondrial DNA Part B: Resources (Mitochondrial DNA Part B: Resources) 3 ( 2 ) 812 - 813 2018.07

© 2018, © 2018 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. The complete mitochondrial genome of Eumeta variegate, largest bagworm moth in Japan, has been sequenced using a nanopore sequencer as a single long read. The genome has a total length of 16,601 bp, consisting of 13 protein-coding genes, 20 tRNA, 2 rRNA genes, and an AT-rich control region. The nucleotide composition was extremely AT-rich, with 42.4% A, 40.4% T, 6.67% G, and 10.6% C. This is the second report of a complete mitochondrial genome of Psychidae, and the sequence information together with a phylogenetic analysis would provide a reference data in the future studies of Lepidoptera and Psychidae.

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Collaborative environmental DNA sampling from petal surfaces of flowering cherry Cerasus × yedoensis ‘Somei-yoshino’ across the Japanese archipelago

Ohta T., Kawashima T., Shinozaki N.O., Dobashi A., Hiraoka S., Hoshino T., Kanno K., Kataoka T., Kawashima S., Matsui M., Nemoto W., Nishijima S., Suganuma N., Suzuki H., Taguchi Y.H., Takenaka Y., Tanigawa Y., Tsuneyoshi M., Yoshitake K., Sato Y., Yamashita R., Arakawa K., Iwasaki W.

Journal of Plant Research (Journal of Plant Research) 131 ( 4 ) 709 - 717 2018.07

ISSN 09189440

© 2018, The Botanical Society of Japan and Springer Japan KK, part of Springer Nature. Recent studies have shown that environmental DNA is found almost everywhere. Flower petal surfaces are an attractive tissue to use for investigation of the dispersal of environmental DNA in nature as they are isolated from the external environment until the bud opens and only then can the petal surface accumulate environmental DNA. Here, we performed a crowdsourced experiment, the “Ohanami Project”, to obtain environmental DNA samples from petal surfaces of Cerasus × yedoensis ‘Somei-yoshino’ across the Japanese archipelago during spring 2015. C. × yedoensis is the most popular garden cherry species in Japan and clones of this cultivar bloom simultaneously every spring. Data collection spanned almost every prefecture and totaled 577 DNA samples from 149 collaborators. Preliminary amplicon-sequencing analysis showed the rapid attachment of environmental DNA onto the petal surfaces. Notably, we found DNA of other common plant species in samples obtained from a wide distribution; this DNA likely originated from the pollen of the Japanese cedar. Our analysis supports our belief that petal surfaces after blossoming are a promising target to reveal the dynamics of environmental DNA in nature. The success of our experiment also shows that crowdsourced environmental DNA analyses have considerable value in ecological studies.

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An integrative description of Macrobiotus shonaicus sp. nov. (Tardigrada: Macrobiotidae) from Japan with notes on its phylogenetic position within the hufelandi group

Stec D., Arakawa K., Michalczyk Ł.

PLoS ONE (PLoS ONE) 13 ( 2 ) 2018.02

Copyright: © 2018 Stec et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Tardigrade research in Japan dates back over 100 years, and to date, 167 species of this ecdysozoan phylum have been reported from the country. Of these species, the Macrobiotus hufelandi complex has been represented only by the nominal taxon of this group, Macrobiotus hufelandi. In this article, a new species of the hufelandi group from Japan, Macrobiotus shonaicus sp. nov., is described using integrative taxonomy. In addition to the detailed morphological and morphometric data, obtained using phase contrast light microscopy (PCM) and scanning electron microscopy (SEM), we provide DNA sequences of four molecular markers (both nuclear and mitochondrial). The new species belongs to the persimilis subgroup and is most similar to M. anemone from USA, M. naskreckii from Mozambique, and M. patagonicus from Argentina, but it can be easily distinguished from these species by the presence of thin flexible filaments on terminal discs of the egg process. By the latter character, the new species is most similar to M. paulinae and M. polypiformis, but it can be easily distinguished from them by having a solid egg surface between egg processes (i.e., without pores or reticulum). A phylogenetic analysis of available DNA sequences of the COI marker for the hufelandi group revealed that the new species clusters with the two other species that exhibit filaments on egg process discs (M. paulinae and M. polypiformis) and with two species that have entire egg processes modified into filaments (M. kristenseni and M. scoticus). All five species form a clade distinct from all other sequenced species of the hufelandi group with typical mushroom- or inverted goblet-shaped egg processes, which may suggest that the ancestor of the five species with atypical egg processes had a mutation allowing derivations from the mushroom or inverted chalice-like shape of egg processes.

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Accelerated laboratory evolution reveals the influence of replication on the GC skew in Escherichia coli

Kono N., Tomita M., Arakawa K.

Genome Biology and Evolution (Genome Biology and Evolution) 10 ( 11 ) 3110 - 3117 2018

© The Author(s) 2018. Most bacterial genomes display contrasting strand asymmetry in a variety of features, such as nucleotide composition and gene orientation, of the two replichores separated by the replication origin and terminus. The cause for the polarization is often attributed to mutations arising from the asymmetric replication machinery. Notably, a base compositional bias known as a GC skew is focused on as a footprint of the bacterial genome evolution driven by DNA replication. Previously, although a replication driven mutation pattern responsible for the GC skew formation or the related mathematical models have been well reported, an exact impact of the replication-related elements on the genomic structure is yet actively debated, and not confirmed experimentally. However, the GC skew formation is very time consuming and challenging in the laboratory. We, therefore, used cytosine deaminase as a DNA mutator, and by monitoring the mutations during an accelerated laboratory evolution procedure with Illumina sequencing, we enabled the trial and error of the GC skew formation in high resolution. Using this technology, we succeeded in reconfirming the influence of bacterial replication machinery on the genomic structure at high resolution.

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Evaluation of the impact of RNA preservation methods ofspiders for de novo transcriptome assembly

Kono, Nobuaki, Nakamura, Hiroyuki, Ito, Yusuke, Tomita, Masaru, Arakawa, Kazuharu

MOLECULAR ECOLOGY RESOURCES 16 ( 3 ) 662 - 672 2016.05

Research paper (scientific journal), ISSN 1755-098X

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No evidence for extensive horizontal gene transfer from the draft genome of a tardigrade

Arakawa, Kazuharu

PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA 113 ( 22 ) E3057 - E3057 2016.05

Research paper (scientific journal), ISSN 0027-8424

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De novo assembly and comparative transcriptome analysis of Euglena gracilis in response to anaerobic conditions

Yoshida, Yuta, Tomiyama, Takuya, Maruta, Takanori, Tomita, Masaru, Ishikawa, Takahiro, Arakawa, Kazuharu

BMC GENOMICS 17 2016.03

Research paper (scientific journal), ISSN 1471-2164

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Merging Multiple Omics Datasets In Silico: Statistical Analyses and Data Interpretation

ARAKAWA Kazuharu, Tomita M

Methods Mil. Biol. 985 459-470 2013

Research paper (scientific journal), Joint Work

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