Biology subjects

Fukatsu, T.

Publications and source records attributed to Fukatsu, T..

4 recordsLinked to original sources

bioRxiv2023

Mechanisms underpinning morphogenesis of symbiotic organ specialized for hosting indispensable microbial symbiont in stinkbug

Microbial mutualists are pivotal for insect adaptation, which often entails the evolution of elaborate organs for symbiosis. Addressing what mechanisms underpin the development of such organs is of evolutionary interest. Here we investigated the stinkbug Plautia stali whose posterior midgut is transformed into a specialized symbiotic organ. Despite being a simple tube in newborns, it developed numerous crypts in four rows, whose inner cavity hosts a specific bacterial symbiont, during 1st to 2nd nymphal instar. Visualization of dividing cells revealed that active cell proliferation was coincident with the crypt formation, although spatial patterns of the proliferating cells did not reflect the crypt arrangement. Visualization of visceral muscles in the midgut, consisting of circular muscles and longitudinal muscles, uncovered that, strikingly, circular muscles exhibited a characteristic arrangement running between the crypts specifically in the symbiotic organ. Even in early 1st instar when no crypts were seen, two rows of epithelial areas delineated by bifurcated circular muscles were identified. In 2nd instar, crossing muscle fibers newly appeared and connected the adjacent circular muscles, whereby the midgut epithelium was divided into four rows of crypt-to-be areas. The crypt formation proceeded even in aposymbiotic nymphs, uncovering autonomous nature of the crypt development. We propose a mechanistic model of crypt formation wherein the spatial arrangement of muscle fibers and the proliferation of epithelial cells underpin the formation of crypts as midgut evaginations. IMPORTANCEDiverse organisms are associated with microbial mutualists, in which specialized host organs often develop for retaining the microbial partners. In the light of the origin of evolutionary novelties, it is important to understand what mechanisms underpin the elaborate morphogenesis of such symbiotic organs, which must have been shaped through interactions with the microbial symbionts. Using the stinkbug Plautia stali as a model, we demonstrated that visceral muscular patterning and proliferation of intestinal epithelial cells during early nymphal stages are involved in the formation of numerous symbiont-harboring crypts arranged in four rows in the posterior midgut to constitute the symbiotic organ. Strikingly, the crypt formation occurred normally even in symbiont-free nymphs, uncovering that the crypt development proceeds autonomously. These findings suggest that the crypt formation is deeply implemented into the normal development of P. stali, which must reflect the considerably ancient evolutionary origin of the midgut symbiotic organ in stinkbugs.

microbiology↗

bioRxiv2022

Cuticle supplementation and nitrogen recycling by a dual bacterial symbiosis in a family of xylophagous beetles (Coleoptera: Bostrichidae)

Many insects engage in stable nutritional symbioses with bacteria that supplement limiting essential nutrients to their host. While several plant sap-feeding Hemipteran lineages are known to be simultaneously associated with two or more endosymbionts with complementary biosynthetic pathways to synthesize amino acids or vitamins, such co-obligate symbioses have not been functionally characterized in other insect orders. Here, we report on the characterization of a dual co-obligate, bacteriome-localized symbiosis in a family of xylophagous beetles using comparative genomics, fluorescence microscopy, and phylogenetic analyses. Across the beetle family Bostrichidae, all investigated species harbored the Bacteroidota symbiont Shikimatogenerans bostrichidophilus that encodes the shikimate pathway to produce tyrosine precursors in its severely reduced genome, likely supplementing the beetles cuticle biosynthesis, sclerotisation, and melanisation. One clade of Bostrichid beetles additionally housed the co-obligate symbiont Bostrichicola ureolyticus that is inferred to complement the function of Shikimatogenerans by recycling urea and provisioning the essential amino acid lysine, thereby providing additional benefits on nitrogen-poor diets. Both symbionts represent ancient associations within the Bostrichidae that have subsequently experienced genome erosion and co-speciation with their hosts. While Bostrichicola was repeatedly lost, Shikimatogenerans has been retained throughout the family and exhibits a perfect pattern of co-speciation. Our results reveal that co-obligate symbioses with complementary metabolic capabilities occur beyond the well-known sap-feeding Hemiptera and highlight the importance of symbiont-mediated cuticle supplementation and nitrogen recycling for herbivorous beetles. Significance statementNutritional symbioses evolved frequently in insects and contribute diverse metabolites to their hosts physiology. Associations with dual symbionts providing complementary nutrients evolved in multiple Hemiptera lineages, compensating eroded biosynthetic capabilities of primary symbionts. Bostrichidae, a family of xylophagous beetles, harbor consistently a Flavobacterial symbiont encoding exclusively the Shikimate pathway to synthesis precursors of tyrosine. However, in two families a second, closely Flavobacterial symbiont capable of recycling urea and synthesizing lysine was retained. Both symbionts exhibit high genomic syntheny and tight co-cladogenesis with the host phylogeny, indicating ancestral, ecological highly beneficial symbioses.

evolutionary biology↗

bioRxiv2022

Seasonal polyphenism underlies the origin of a sterile caste in aphids

The origin of a sterile caste among eusocial animals has been a fundamental but still unresolved problem in understanding the evolution of biological complexity. At the origin of a sterile caste, recruitment of pre-existing plasticity may lead to produce physiologically, morphologically and behaviorally distinct caste phenotypes. Here, we provide convincing evidence that preexisting seasonal polyphenism has been recruited to generate a sterile soldier caste in host-alternating social aphids. We demonstrate that sterile soldier nymphs of Colophina aphids resemble those of monomorphic defensive nymphs produced in a different host-plant generation. Notably, the two morphs in the basal species show the closest similarity in morphology and gene expression among all morph pairs. Moreover, their evolutionary phenotypic changes along the phylogeny of four Colophina species are significantly correlated positively. These results suggest that they may share the common regulatory mechanisms of development, which underpin the heterochronic expression of monomorphic defenders on the different host plant leading to the evolution of a novel soldier phenotype. We further demonstrate that the monomorphic defenders can increase their inclusive fitness by killing predators eggs on a seasonally different host plant. Taken together, our findings suggest that preexisting plasticity that can gain indirect fitness benefits facilitates the early evolution of a sterile caste.

evolutionary biology↗

bioRxiv2022

Single mutation makes Escherichia coli an insect mutualist

We report an experimental system in which Escherichia coli evolves into an insect mutualist. When the essential gut symbiont of the stinkbug Plautia stali was replaced by E. coli, a few survivor insects exhibited specific localization and vertical transmission of E. coli. Through trans-generational maintenance with P. stali, several hyper-mutating E. coli lines independently evolved hosts high adult emergence and improved body color. Such "mutualistic" E. coli lines exhibited independent mutations disrupting the carbon catabolite repression (CCR) global transcriptional regulator. Each of the mutations reproduced the mutualistic phenotypes when introduced into wild-type E. coli, confirming that the single CCR mutations instantly make E. coli an insect mutualist. Our discovery uncovers that evolution of elaborate mutualism can proceed more easily and rapidly than conventionally envisaged.

evolutionary biology↗