Details of a Researcher - Arakawa, Kazuharu

Papers - Arakawa, Kazuharu

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Molecular Evidence of Chemical Disguise by the Socially Parasitic Spiny Ant Polyrhachis lamellidens (Hymenoptera: Formicidae) When Invading a Host Colony

Iwai H., Mori M., Tomita M., Kono N., Arakawa K.

Frontiers in Ecology and Evolution 10 2022.06

While most ant species establish a colony independently, some socially parasitic ants build the foundation of their colony by invading other ant (host) colonies and utilizing their labor forces. Many socially parasitic ants disguise their cuticular hydrocarbon (CHC) profile, which is also known as signature mixture for nestmate discrimination, when invading the host colony. Since the strategy of chemical disguise is widespread in socially parasitic ants, elucidating the mechanism of chemical disguise will promote knowledge on the evolutionary history of social parasitism. However, detailed knowledge is still lacking, as the relevant information has only originated from circumstantial evidence, which was obtained from ecological observations. In this study, we investigated the mechanism of chemical disguise in a new queen of a temporary socially parasitic spiny ant (Polyrhachis lamellidens) by measuring its CHC profile, performing a tracing assay with labeled substances, and analyzing gene expression levels. First, after rubbing behavior was observed against the host workers, the CHC profile in P. lamellidens shifted to pronounced peaks that closely resembling that of the host workers. We also observed a reduction in aggressive behaviors by the host ant against P. lamellidens after rubbing behavior was performed. In addition, P. lamellidens acquired artificially-applied labeling substances from host workers through their rubbing behaviors, while gene expression profiling showed the expression of CHC synthesis-related genes did not change during this behavior. These results suggest that P. lamellidens directly obtains host CHCs through rubbing behavior, and these host CHCs enables P. lamellidens to remain disguised during colony invasion.

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Tardigrade Secretory-Abundant Heat-Soluble Protein Varies Entrance Propensity Depending on the Amino-Acid Sequence

Miyazawa K., Itoh S.G., Yoshida Y., Arakawa K., Okumura H.

Journal of Physical Chemistry B 126 ( 12 ) 2361 - 2368 2022.03

ISSN 15206106

Secretory-abundant heat-soluble (SAHS) proteins, which constitute a protein family unique to tardigrades, are thought to be essential for anhydrobiosis. Our previous study has revealed that one of the SAHS proteins of Ramazzottius varieornatus (RvSAHS1) has a more flexible entrance than a mammalian fatty-acid-binding protein, which has a crystal structure similar to that of RvSAHS1. Recently, SAHS paralogs that are expressed abundantly and specifically in the early embryos of this tardigrade and Hypsibius exemplaris have been identified. Comparing these amino-acid sequences with that of RvSAHS1, we have found characteristic differences as I113F and D146T. In this study, we investigate I113F and D146T mutants' properties of RvSAHS1 using molecular dynamics simulations and compare the structures and fluctuations of their entrances with those of the wild type. The two mutants exhibit different properties at the entrance of the β-barrel structure. The I113F mutant tends to close the entrance more than the wild type due to the enhanced hydrophobic network inside the cavity. The D146T mutant, in contrast to the I113F mutant, tends to open the entrance. The mechanism by which this mutation opens the entrance is also discussed. Even though only a single mutation located far from the entrance is added to the wild type, there is a clear difference in the tendency to open and close the β-barrel entrance. It indicates that the entrance properties of the SAHS protein are sensitive to the amino-acid sequence.

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Initial parasitic behaviour of the temporary social parasitic ant Polyrhachis lamellidens can be induced by host-like cuticles in laboratory environment

Kurihara Y., Iwai H., Kono N., Tomita M., Arakawa K.

Biology Open 11 ( 3 ) 2022.03

Polyrhachis lamellidens is a temporary social parasitic species. When a newly mated queen encounters a host worker, it opens its jaws and then mounts and rubs the body of the host worker, called rubbing behaviour. This behaviour is different from aggressive behaviour and is considered to be a preparatory action before invasion of the host colony. However, it is unclear what cues trigger rubbing behaviour. Therefore, in this study, we used glass beads that imitated the insect body surfaces and searched for triggers. Although P. lamellidens did not respond to the cuticular compounds only, cuticular compounds and chitin coatings on glass beads elicited responses that were similar to those towards live samples. The rubbing behaviour of P. lamellidens was elicited in response to a cuticle-like surface that mimicked a procuticle by combining the compounds with chitin. These results suggest that host recognition and nest-mate recognition are supported by different mechanisms.

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Examples of Extreme Survival: Tardigrade Genomics and Molecular Anhydrobiology

Arakawa K.

Annual Review of Animal Biosciences 10 17 - 37 2022.02

ISSN 21658102

Tardigrades are ubiquitous meiofauna that are especially renowned for their exceptional extremotolerance to various adverse environments, including pressure, temperature, and even ionizing radiation. This is achieved through a reversible halt of metabolism triggered by desiccation, a phenomenon called anhydrobiosis. Recent establishment of genome resources for two tardigrades, Hypsibius exemplaris and Ramazzottius varieornatus, accelerated research to uncover the molecular mechanisms behind anhydrobiosis, leading to the discovery of many tardigrade-unique proteins. This review focuses on the history, methods, discoveries, and current state and challenges regarding tardigrade genomics, with an emphasis on molecular anhydrobiology. Remaining questions and future perspectives regarding prospective approaches to fully elucidate the molecular machinery of this complex phenomenon are discussed.

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Liquid‒liquid phase separation seen in tardigrade anhydrobiosis and spider silk spinning

Arakawa K.

Seikagaku 94 ( 4 ) 537 - 547 2022

ISSN 00371017

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Darwin's bark spider shares a spidroin repertoire with Caerostris extrusa but achieves extraordinary silk toughness through gene expression

Kono N., Ohtoshi R., Malay A.D., Mori M., Masunaga H., Yoshida Y., Nakamura H., Numata K., Arakawa K.

Open Biology 11 ( 12 ) 2021.12

Spider silk is a protein-based material whose toughness suggests possible novel applications. A particularly fascinating example of silk toughness is provided by Darwin's bark spider (Caerostris darwini) found in Madagascar. This spider produces extraordinarily tough silk, with an average toughness of 350 MJ m -1 and over 50% extensibility, and can build river-bridging webs with a size of 2.8 m 2. Recent studies have suggested that specific spidroins expressed in C. darwini are responsible for the mechanical properties of its silk. Therefore, a more comprehensive investigation of spidroin sequences, silk thread protein contents and phylogenetic conservation among closely related species is required. Here, we conducted genomic, transcriptomic and proteomic analyses of C. darwini and its close relative Caerostris extrusa. A variety of spidroins and low-molecular-weight proteins were found in the dragline silk of these species; all of the genes encoding these proteins were conserved in both genomes, but their genes were more expressed in C. darwini. The potential to produce very tough silk is common in the genus Caerostris, and our results may suggest the existence of plasticity allowing silk mechanical properties to be changed by optimizing related gene expression in response to the environment.

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Comprehensive Transcriptome Sequencing of Tanaidacea with Proteomic Evidences for Their Silk

Kakui K., Fleming J.F., Mori M., Fujiwara Y., Arakawa K.

Genome Biology and Evolution 13 ( 12 ) 2021.12

Tanaidaceans are small benthic crustaceans that mainly inhabit diverse marine environments, and they comprise one of the most diverse and abundant macrofaunal groups in the deep sea. Tanaidacea is one of the most thread-dependent taxa in the Crustacea, constructing tubes, spun with their silk, for shelter. In this work, we sequenced and assembled the comprehensive transcriptome of 23 tanaidaceans encompassing 14 families and 4 superfamilies of Tanaidacea, and performed silk proteomics of Zeuxo ezoensis to search for its silk genes. As a result, we identified two families of silk proteins that are conserved across the four superfamilies. The long and repetitive nature of these silk genes resembles that of other silk-producing organisms, and the two families of proteins are similar in composition to silkworm and caddisworm fibroins, respectively. Moreover, the amino acid composition of the repetitive motifs of tanaidacean silk tends to be more hydrophilic, and therefore could be a useful resource in studying their unique adaptation of silk use in a marine environment. The availability of comprehensive transcriptome data in these taxa, coupled with proteomic evidence of their silk genes, will facilitate evolutionary and ecological studies.

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Desiccation-induced fibrous condensation of CAHS protein from an anhydrobiotic tardigrade

Yagi-Utsumi M., Aoki K., Watanabe H., Song C., Nishimura S., Satoh T., Yanaka S., Ganser C., Tanaka S., Schnapka V., Goh E.W., Furutani Y., Murata K., Uchihashi T., Arakawa K., Kato K.

Scientific Reports 11 ( 1 ) 2021.12

Anhydrobiosis, one of the most extensively studied forms of cryptobiosis, is induced in certain organisms as a response to desiccation. Anhydrobiotic species has been hypothesized to produce substances that can protect their biological components and/or cell membranes without water. In extremotolerant tardigrades, highly hydrophilic and heat-soluble protein families, cytosolic abundant heat-soluble (CAHS) proteins, have been identified, which are postulated to be integral parts of the tardigrades’ response to desiccation. In this study, to elucidate these protein functions, we performed in vitro and in vivo characterizations of the reversible self-assembling property of CAHS1 protein, a major isoform of CAHS proteins from Ramazzottius varieornatus, using a series of spectroscopic and microscopic techniques. We found that CAHS1 proteins homo-oligomerized via the C-terminal α-helical region and formed a hydrogel as their concentration increased. We also demonstrated that the overexpressed CAHS1 proteins formed condensates under desiccation-mimicking conditions. These data strongly suggested that, upon drying, the CAHS1 proteins form oligomers and eventually underwent sol–gel transition in tardigrade cytosols. Thus, it is proposed that the CAHS1 proteins form the cytosolic fibrous condensates, which presumably have variable mechanisms for the desiccation tolerance of tardigrades. These findings provide insights into molecular strategies of organisms to adapt to extreme environments.

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Shifts in morphology, gene expression, and selection underlie web loss in Hawaiian Tetragnatha spiders

Berger C.A., Brewer M.S., Kono N., Nakamura H., Arakawa K., Kennedy S.R., Wood H.M., Adams S.A., Gillespie R.G.

BMC Ecology and Evolution 21 ( 1 ) 2021.12

Background: A striking aspect of evolution is that it often converges on similar trajectories. Evolutionary convergence can occur in deep time or over short time scales, and is associated with the imposition of similar selective pressures. Repeated convergent events provide a framework to infer the genetic basis of adaptive traits. The current study examines the genetic basis of secondary web loss within web-building spiders (Araneoidea). Specifically, we use a lineage of spiders in the genus Tetragnatha (Tetragnathidae) that has diverged into two clades associated with the relatively recent (5 mya) colonization of, and subsequent adaptive radiation within, the Hawaiian Islands. One clade has adopted a cursorial lifestyle, and the other has retained the ancestral behavior of capturing prey with sticky orb webs. We explore how these behavioral phenotypes are reflected in the morphology of the spinning apparatus and internal silk glands, and the expression of silk genes. Several sister families to the Tetragnathidae have undergone similar web loss, so we also ask whether convergent patterns of selection can be detected in these lineages. Results: The cursorial clade has lost spigots associated with the sticky spiral of the orb web. This appears to have been accompanied by loss of silk glands themselves. We generated phylogenies of silk proteins (spidroins), which showed that the transcriptomes of cursorial Tetragnatha contain all major spidroins except for flagelliform. We also found an uncharacterized spidroin that has higher expression in cursorial species. We found evidence for convergent selection acting on this spidroin, as well as genes involved in protein metabolism, in the cursorial Tetragnatha and divergent cursorial lineages in the families Malkaridae and Mimetidae. Conclusions: Our results provide strong evidence that independent web loss events and the associated adoption of a cursorial lifestyle are based on similar genetic mechanisms. Many genes we identified as having evolved convergently are associated with protein synthesis, degradation, and processing, which are processes that play important roles in silk production. This study demonstrates, in the case of independent evolution of web loss, that similar selective pressures act on many of the same genes to produce the same phenotypes and behaviors.

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Multiomics study of a heterotardigrade, Echinisicus testudo, suggests the possibility of convergent evolution of abundant heat-soluble proteins in Tardigrada

Murai Y., Yagi-Utsumi M., Fujiwara M., Tanaka S., Tomita M., Kato K., Arakawa K.

BMC Genomics 22 ( 1 ) 2021.12

Background: Many limno-terrestrial tardigrades can enter an ametabolic state, known as anhydrobiosis, upon desiccation, in which the animals can withstand extreme environments. Through genomics studies, molecular components of anhydrobiosis are beginning to be elucidated, such as the expansion of oxidative stress response genes, loss of stress signaling pathways, and gain of tardigrade-specific heat-soluble protein families designated CAHS and SAHS. However, to date, studies have predominantly investigated the class Eutardigrada, and molecular mechanisms in the remaining class, Heterotardigrada, still remains elusive. To address this gap in the research, we report a multiomics study of the heterotardigrade Echiniscus testudo, one of the most desiccation-tolerant species which is not yet culturable in laboratory conditions. Results: In order to elucidate the molecular basis of anhydrobiosis in E. testudo, we employed a multi-omics strategy encompassing genome sequencing, differential transcriptomics, and proteomics. Using ultra-low input library sequencing protocol from a single specimen, we sequenced and assembled the 153.7 Mbp genome annotated using RNA-Seq data. None of the previously identified tardigrade-specific abundant heat-soluble genes was conserved, while the loss and expansion of existing pathways were partly shared. Furthermore, we identified two families novel abundant heat-soluble proteins, which we named E. testudo Abundant Heat Soluble (EtAHS), that are predicted to contain large stretches of disordered regions. Likewise the AHS families in eutardigrada, EtAHS shows structural changes from random coil to alphahelix as the water content was decreased in vitro. These characteristics of EtAHS proteins are analogous to those of CAHS in eutardigrades, while there is no conservation at the sequence level. Conclusions: Our results suggest that Heterotardigrada have partly shared but distinct anhydrobiosis machinery compared with Eutardigrada, possibly due to convergent evolution within Tardigrada. (276/350).

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The balance of crystalline and amorphous regions in the fibroin structure underpins the tensile strength of bagworm silk

Kono N., Nakamura H., Tateishi A., Numata K., Arakawa K.

Zoological Letters 7 ( 1 ) 2021.12

Protein-based materials are considered versatile biomaterials, and their biodegradability is an advantage for sustainable development. Bagworm produces strong silk for use in unique situations throughout its life stages. Rigorous molecular analyses of Eumeta variegata suggested that the particular mechanical properties of its silk are due to the coexistence of poly-A and GA motifs. However, little molecular information on closely related species is available, and it is not understood how these properties were acquired evolutionarily or whether the motif combination is a conserved trait in other bagworms. Here, we performed a transcriptome analysis of two other bagworm species (Canephora pungelerii and Bambalina sp.) belonging to the family Psychidae to elucidate the relationship between the fibroin gene and silk properties. The obtained transcriptome assemblies and tensile tests indicated that the motif combination and silk properties were conserved among the bagworms. Furthermore, our analysis showed that C. pungelerii produces extraordinarily strong silk (breaking strength of 1.4 GPa) and indicated that the cause may be the C. pungelerii -specific balance of crystalline/amorphous regions in the H-fibroin repetitive domain. This particular H-fibroin architecture may have been evolutionarily acquired to produce strong thread to maintain bag stability during the relatively long development period of Canephora species relative to other bagworms.

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The evidence of temporary social parasitism by Polyrhachis lamellidens (Hymenoptera, Formicidae) in a Camponotus obscuripes colony (Hymenoptera, Formicidae)

Iwai H., Kurihara Y., Kono N., Tomita M., Arakawa K.

Insectes Sociaux 68 ( 4 ) 375 - 382 2021.11

ISSN 00201812

Polyrhachis lamellidens is a temporary socially parasitic ant whose new queen utilizes other ant species in the early stages of colony foundation. Field observations and rearing experiments suggest that Camponotus japonicus is a host species of P. lamellidens. It is presumed that Camponotus obscuripes is also a host of P. lamellidens by rearing experiments and field observations; however, there are no records of P. lamellidens workers or brood coexisting in C. obscuripes colonies in field observations, and there is no clear evidence that C. obscuripes is a natural host of P. lamellidens. We conducted detailed field observations, behavioral tests, and rearing experiments to show that C. obscuripes is a host of temporary social parasites. We found colonies with P. lamellidens queens, workers, and larvae intermixed with C. obscuripes workers in the field. Behavioral tests showed that workers of both species in mixed colonies did not attack each other and maintained nestmate recognition ability, which suggests a collaborative nestmate relationship. Furthermore, a rearing experiment confirmed social parasitism by P. lamellidens among C. obscuripes by producing a mixed brood-producing colony. These are the first field and laboratory records of temporary social parasitism involving P. lamellidens and C. obscuripes.

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Tardigrade Secretory-Abundant Heat-Soluble Protein Has a Flexible β-Barrel Structure in Solution and Keeps This Structure in Dehydration

Miyazawa K., Itoh S.G., Watanabe H., Uchihashi T., Yanaka S., Yagi-Utsumi M., Kato K., Arakawa K., Okumura H.

Journal of Physical Chemistry B 125 ( 32 ) 9145 - 9154 2021.08

ISSN 15206106

Secretory-abundant heat-soluble (SAHS) proteins are unique heat-soluble proteins of Tardigrada and are believed to play an essential role in anhydrobiosis, a latent state of life induced by desiccation. To investigate the dynamic properties, molecular dynamics (MD) simulations of a SAHS protein, RvSAHS1, were performed in solution and under dehydrating conditions. For comparison purposes, MD simulations of a human liver-type fatty-acid binding protein (LFABP) were performed in solution. Furthermore, high-speed atomic force microscopy observations were conducted to ascertain the results of the MD simulations. Three properties of RvSAHS1 were found as follows. (1) The entrance region of RvSAHS1 is more flexible and can be more extensive in solutions compared with that of a human LFABP because there is no salt bridge between the βD and βE strands. (2) The intrinsically disordered domain in the N-terminal region significantly fluctuates and can form an amphiphilic α-helix. (3) The size of the entrance region gets smaller along with dehydration, keeping the β-barrel structure. Overall, the obtained results provide atomic-level dynamics of SAHS proteins.

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Multicomponent nature underlies the extraordinary mechanical properties of spider dragline silk

Kono N., Nakamura H., Mori M., Yoshida Y., Ohtoshi R., Malay A.D., Pedrazzoli Moran D.A., Tomita M., Numata K., Arakawa K.

Proceedings of the National Academy of Sciences of the United States of America 118 ( 31 ) 2021.08

ISSN 00278424

Dragline silk of golden orb-weaver spiders (Nephilinae) is noted for its unsurpassed toughness, combining extraordinary extensibility and tensile strength, suggesting industrial application as a sustainable biopolymer material. To pinpoint the molecular composition of dragline silk and the roles of its constituents in achieving its mechanical properties, we report a multiomics approach, combining highquality genome sequencing and assembly, silk gland transcriptomics, and dragline silk proteomics of four Nephilinae spiders.We observed the consistent presence of the MaSp3B spidroin unique to this subfamily as well as several nonspidroin SpiCE proteins. Artificial synthesis and the combination of these components in vitro showed that the multicomponent nature of dragline silk, including MaSp3B and SpiCE, along with MaSp1 and MaSp2, is essential to realize the mechanical properties of spider dragline silk.

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New Tardigrade Opsins and Differential Expression Analyses Show Ontogenic Variation in Light Perception

Fleming J.F., Pisani D., Arakawa K.

Genome Biology and Evolution 13 ( 8 ) 2021.08

Opsins are light-sensitive proteins involved in many photoreceptive processes, including, but not limited to, vision and regulation of circadian rhythms. Arthropod (e.g., insects, spiders, centipedes, and crabs) opsins have been extensively researched, but the relationships and function of opsins found in lineages that are evolutionarily closely related to the arthropods remains unclear. Multiple, independent, opsin duplications are known in Tardigrada (the water bears), evidencing that protostome opsin duplications are not limited to the Arthropoda. However, the relationships, function, and expression of these new opsins are still unknown. Here, we use two tardigrade transcriptomes with deep coverage to greatly expand our knowledge of the diversity of tardigrade opsins. We reconstruct the phylogenetic relationships of the tardigrade opsins and investigate their ontogenetic expression. We found that while tardigrades have multiple opsins that evolved from lineage-specific duplications of well-understood arthropod opsins, their expression levels change during ontogeny such that most of these opsins are not co-temporally expressed. Co-temporal expression of multiple opsins underpins color vision in Arthropoda and Vertebrata. Our results clearly show duplications of both rhabdomeric and ciliary opsins within Tardigrada, forming clades specific to both the Heterotardigrada and Eutardigrada in addition to multiple independent duplications within genera. However, lack of co-temporal, ontogenetic, expression suggests that while tardigrades possess multiple opsins, they are unlikely to be able to distinguish color.

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Complete genome sequence of atopobiaceae bacterium strain p1, isolated from mouse feces

Watanabe Y., Takeuchi N., Yang J., Obana N., Morinaga K., Kusada H., Tamaki H., Fukuda S., Arakawa K.

Microbiology Resource Announcements 10 ( 28 ) 2021.07

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Complete genome sequences of two lysobacter strains, isolated from seawater (lysobacter caseinilyticus) and soil (lysobacter helvus) in south korea

Watanabe Y., Arakawa K.

Microbiology Resource Announcements 10 ( 28 ) 2021.07

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Proteomic evidence for the silk fibroin genes of spider mites (Order Trombidiformes: Family Tetranychidae)

Arakawa K., Mori M., Kono N., Suzuki T., Gotoh T., Shimano S.

Journal of Proteomics 239 2021.05

ISSN 18743919

Spider mites are a group of arachnids belonging to Acari (mites and ticks), family Tetranychidae, known to produce nanoscale silk fibers characterized by a high Young's modulus. The silk fibroin gene of spider mites has been computationally predicted through genomic analysis of Tetranychus urticae Koch, but it has yet to be confirmed by proteomic evidence. In this work, we sequenced and assembled the transcriptome from two genera of spider mites, Tetranychus kanzawai Kishida and Panonychus citri (McGregor), and combined it with silk proteomics of T. urticae and P. citri to characterize the fibroin genes through comparative genomics and multiomics analysis. As a result, two fibroins were identified, which were different genes than those previously predicted by computational methods. The amino acid composition and secondary structure suggest similarity to aciniform or cylindrical spidroins of spider silk, which partly mirrors their mechanical properties, exhibiting a high Young's modulus. The availability of full-length fibroin sequences of spider mites facilitates the study of the evolution of silk genes that sometimes emerge in multiple lineages in a convergent manner and in the industrial application of artificial protein fibers through the study of the amino acid sequence and the resulting mechanical properties of these silks. Significance: Here we sequenced and assembled the transcriptome from two genera of spider mites, T. kanzawai and P. citri, and combined it with silk proteomics of T. urticae and P. citri to characterize the fibroin genes through comparative genomics and multiomics analysis. Spider mite silk is especially characterized by its extremely fine nano-scale diameter and high Young's modulus, even exceeding those of spider silks. The availability of full-length fibroin sequences of spider mites facilitates the study of the evolution of silk genes, which independently evolved in mites, insects, and spiders but yet show sequence convergence, and in the industrial application of artificial protein fibers through the study of the amino acid sequence and the resulting mechanical properties of these silks.

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Systematics of tardigrada: A reanalysis of tardigrade taxonomy with specific reference to Guil et al. (2019)

Fleming J.F., Arakawa K.

Zoologica Scripta 50 ( 3 ) 376 - 382 2021.05

ISSN 03003256

The Tardigrada are a clade with a disputed and complex taxonomy. The three traditional tardigrade classes are the Heterotardigrada, Eutardigrada and the dubious, monotypic Mesotardigrada. A recent molecular study by Guil et al (Zoologica Scripta, 48, 2019, 120) suggested that the Apochela, previously considered an order of Eutardigrada, should become a new class, Apotardigrada, with the Parachela becoming THE new Eutardigrada. This new diagnosis was presented alongside compelling morphological evidence. Here, we test the assumptions of the molecular evidence for Apotardigrada by analysing tardigrade 18S and 28S data under four separate conditions, along with new BUSCO data, across both Bayesian- and maximum-likelihood phylogenetic approaches. We found variable conclusions regarding the status of Apotardigrada could be drawn by comparing the ribosomal RNA and BUSCO results, and caution against using branch length data to determine taxonomic hierarchy.

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Complete genome sequence of adlercreutzia equolifaciens subsp. celatus DSM 18785

Takahashi H., Yang J., Yamamoto H., Fukuda S., Arakawa K.

Microbiology Resource Announcements 10 ( 19 ) 2021.05

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