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Takema Fukatsu - One of the best experts on this subject based on the ideXlab platform.
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understanding regulation of the host mediated gut symbiont population and the symbiont mediated host immunity in the riptortus burkholderia symbiosis system
Developmental and Comparative Immunology, 2016Co-Authors: Ho Am Jang, Takema FukatsuAbstract:Valuable insect models have tremendously contributed to our understanding of innate immunity and symbiosis. Bean bug, Riptortus pedestris, is a useful insect symbiosis model due to harboring cultivable monospecific gut symbiont, genus Burkholderia. Bean bug is a hemimetabolous insect whose immunity is not well-understood. However, we recently identified three major antimicrobial peptides of Riptortus and examined the relationship between gut symbiosis and host immunity. We found that the presence of Burkholderia gut symbiont positively affects Riptortus immunity. From studying host regulation mechanisms of symbiont population, we revealed that the symbiotic Burkholderia cells are much more susceptible to Riptortus immune responses than the cultured cells. We further elucidated that the immune-susceptibility of the Burkholderia gut Symbionts is due to the drastic change of bacterial cell envelope. Finally, we show that the immune-susceptible Burkholderia Symbionts are able to prosper in host owing to the suppression of immune responses of the symbiotic midgut.
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female specific specialization of a posterior end region of the midgut symbiotic organ in plautia splendens and allied stinkbugs
Applied and Environmental Microbiology, 2015Co-Authors: Takahiro Hosokawa, Xian-ying Meng, Takema Fukatsu, Ryuichi Koga, Toshinari HayashiAbstract:ABSTRACT Many stinkbugs (Insecta: Hemiptera: Heteroptera) are associated with bacterial Symbionts in a posterior region of the midgut. In these stinkbugs, adult females excrete symbiont-containing materials from the anus for transmission of the beneficial Symbionts to their offspring. For ensuring the vertical symbiont transmission, a variety of female-specific elaborate traits at the cellular, morphological, developmental, and behavioral levels have been reported from diverse stinkbugs of the families Plataspidae, Urostylididae, Parastrachiidae, etc. Meanwhile, such elaborate female-specific traits for vertical symbiont transmission have been poorly characterized for the largest and economically important stinkbug family Pentatomidae. Here, we investigated the midgut symbiotic system of a pentatomid stinkbug, Plautia splendens. A specific gammaproteobacterial symbiont was consistently present extracellularly in the cavity of numerous crypts arranged in four rows on the midgut fourth section. The symbiont was smeared on the egg surface upon oviposition by adult females, orally acquired by newborn nymphs, and thereby transmitted vertically to the next generation and important for growth and survival of the host insects. We found that, specifically in adult females, several rows of crypts at the posterior end region of the symbiotic midgut were morphologically differentiated and conspicuously enlarged, often discharging the symbiotic bacteria from the crypt cavity to the main tract of the symbiotic midgut. The female-specific enlarged end crypts were also found in other pentatomid stinkbugs Plautia stali and Carbula crassiventris. These results suggest that the enlarged end crypts represent a female-specific specialized morphological trait for vertical symbiont transmission commonly found among stinkbugs of the family Pentatomidae.
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Infection prevalence of Sodalis Symbionts among stinkbugs
Zoological letters, 2015Co-Authors: Takahiro Hosokawa, Nahomi Kaiwa, Yoshitomo Kikuchi, Yu Matsuura, Takema FukatsuAbstract:Diverse insects and other organisms are associated with microbial Symbionts, which often significantly contribute to growth and survival of their hosts and/or drastically affect phenotypes of their hosts in a variety of ways. Sodalis glossinidius was first identified as a facultative bacterial symbiont of tsetse flies, and recent studies revealed that Sodalis-allied bacteria encompass diverse ecological niches ranging from free-living bacteria through facultative Symbionts to obligate Symbionts associated with a diverse array of insects. Despite potential ecological and evolutionary relevance of the Sodalis Symbionts, their infection prevalence in natural insect populations has been poorly investigated. Here we surveyed diverse stinkbugs and allied terrestrial heteropteran bugs, which represented 17 families, 77 genera, 108 species, 310 populations and 960 individuals, for infection with the Sodalis Symbionts. Diagnostic PCR detected relatively low infection frequencies of the Sodalis Symbionts: 13.6% (14/103) of the species, 7.5% (22/295) of the populations, and 4.3% (35/822) of the individuals of the stinkbugs except for those belonging to the family Urostylididae. Among the urostylidid stinkbugs, strikingly, the Sodalis Symbionts exhibited very high infection frequencies: 100% (5/5) of the species, 100% (15/15) of the populations, and 94.2% (130/138) of the individuals we examined. Molecular phylogenetic analysis based on bacterial 16S rRNA gene sequences revealed that all the Symbionts were placed in the clade of Sodalis-allied bacteria while the symbiont phylogeny did not reflect the systematics of their stinkbug hosts. Notably, the Sodalis Symbionts of the urostylidid stinkbugs were not clustered with the Sodalis Symbionts of the other stinkbug groups on the phylogeny, suggesting their distinct evolutionary trajectories. The relatively low infection frequency and the overall host-symbiont phylogenetic incongruence suggest that the Sodalis Symbionts are, in general, facultative symbiotic associates in the majority of the stinkbug groups. On the other hand, it is conceivable, although speculative, that the Sodalis Symbionts may play some substantial biological roles for their host stinkbugs of the Urostylididae.
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Phylogenetic analysis of Symbionts in feather-feeding lice of the genus Columbicola: evidence for repeated symbiont replacements
BMC Evolutionary Biology, 2013Co-Authors: Wendy A. Smith, Takema Fukatsu, Ryuichi Koga, Kelly F. Oakeson, Kevin P. Johnson, David L. Reed, Tamar E. Carter, Kari Smith, Dale H. Clayton, Colin DaleAbstract:Background: Many groups of insects have obligate bacterial Symbionts that are vertically transmitted. Such associations are typically characterized by the presence of a monophyletic group of bacteria living in a well-defined host clade. In addition the phylogeny of the symbiotic bacteria is typically congruent with that of the host, signifying co-speciation. Here we show that bacteria living in a single genus of feather lice, Columbicola (Insecta: Phthiraptera), present an exception to this typical pattern. Results: The phylogeny of Columbicola spp. Symbionts revealed the presence of three candidate clades, with the most species-rich clade having a comb-like topology with very short internodes and long terminal branches. Evolutionary simulations indicate that this topology is characteristic of a process of repeated symbiont replacement over a brief time period. The two remaining candidate clades in our study exhibit high levels of nucleotide substitution, suggesting accelerated molecular evolution due to relaxed purifying selection or smaller effective population size, which is typical of many vertically transmitted insect Symbionts. Representatives of the fast-evolving and slow-evolving symbiont lineages exhibit the same localization, migration, and transmission patterns in their hosts, implying direct replacement. Conclusions: Our findings suggest that repeated, independent symbiont replacements have taken place over the course of the relatively recent radiation of Columbicola spp. These results are compatible with the notion that lice and other insects have the capability to acquire novel Symbionts through the domestication of progenitor strains residing in their local environment.
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Bacteriome-associated endoSymbionts of the green rice leafhopper Nephotettix cincticeps (Hemiptera: Cicadellidae)
Applied Entomology and Zoology, 2012Co-Authors: Hiroaki Noda, Naruo Nikoh, Kenji Watanabe, Sawako Kawai, Fumiko Yukuhiro, Takeharu Miyoshi, Makoto Tomizawa, Yoko Koizumi, Takema FukatsuAbstract:The green rice leafhopper Nephotettix cincticeps (Uhler) is a commonly distributed pest of rice in East Asia. Early histological studies describe the presence of two bacteriome-associated Symbionts and a rickettsial microorganism in N. cincticeps , but their microbiological affiliations have been elusive. We identified these bacterial Symbionts using modern microbiological techniques. Cloning and sequencing of the 16S ribosomal RNA gene from dissected bacteriomes yielded two major and a minor bacterial sequences: a major sequence was placed in the Bacteroidetes clade of Sulcia muelleri , an ancient symbiont lineage associated with diverse hemipteran insects; another major sequence was allied to a β-proteobacterial sequence from a leafhopper Matsumuratettix hiroglyphicus ; the minor sequence fell in the α-proteobacterial genus Rickettsia . In situ hybridization and transmission electron microscopy showed that the Sulcia symbiont and the β-proteobacterial symbiont are harbored within different types of bacteriocytes that constitute the outer and inner regions of the bacteriome, respectively. Oral administration of tetracycline to nymphal N. cincticeps resulted in retarded growth, high mortality rates, and failure in adult emergence, suggesting important biological roles of the Symbionts for the host insect. The designation Candidatus Nasuia deltocephalinicola is proposed for the β-proteobacterial symbiont clade associated with N. cincticeps and allied leafhoppers of the subfamily Deltocephalinae.
Nancy A Moran - One of the best experts on this subject based on the ideXlab platform.
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intraspecific genetic variation in hosts affects regulation of obligate heritable Symbionts
Proceedings of the National Academy of Sciences of the United States of America, 2016Co-Authors: Rebecca A Chong, Nancy A MoranAbstract:Abstract Symbiotic relationships promote biological diversification by unlocking new ecological niches. Over evolutionary time, hosts and Symbionts often enter intimate and permanent relationships, which must be maintained and regulated for both lineages to persist. Many insect species harbor obligate, heritable symbiotic bacteria that provision essential nutrients and enable hosts to exploit niches that would otherwise be unavailable. Hosts must regulate symbiont population sizes, but optimal regulation may be affected by the need to respond to the ongoing evolution of Symbionts, which experience high levels of genetic drift and potential selection for selfish traits. We address the extent of intraspecific variation in the regulation of a mutually obligate symbiosis, between the pea aphid (Acyrthosiphon pisum) and its maternally transmitted symbiont, Buchnera aphidicola. Using experimental crosses to identify effects of host genotypes, we measured symbiont titer, as the ratio of genomic copy numbers of symbiont and host, as well as developmental time and fecundity of hosts. We find a large (>10-fold) range in symbiont titer among genetically distinct aphid lines harboring the same Buchnera haplotype. Aphid clones also vary in fitness, measured as developmental time and fecundity, and genetically based variation in titer is correlated with host fitness, with higher titers corresponding to lower reproductive rates of hosts. Our work shows that obligate symbiosis is not static but instead is subject to short-term evolutionary dynamics, potentially reflecting coevolutionary interactions between host and symbiont.
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Swapping Symbionts in spittlebugs: evolutionary replacement of a reduced genome symbiont
The ISME Journal, 2014Co-Authors: Ryuichi Koga, Nancy A MoranAbstract:Bacterial Symbionts that undergo long-term maternal transmission experience elevated fixation of deleterious mutations, resulting in massive loss of genes and changes in gene sequences that appear to limit efficiency of gene products. Potentially, this dwindling of symbiont functionality impacts hosts that depend on these bacteria for nutrition. One evolutionary escape route is the acquisition of a novel symbiont with a robust genome and metabolic capabilities. Such an acquisition has occurred in an ancestor of Philaenus spumarius , the meadow spittlebug (Insecta: Cercopoidea), which has replaced its ancient association with the tiny genome symbiont Zinderia insecticola (Betaproteobacteria) with an association with a symbiont related to Sodalis glossinidius (Gammaproteobacteria). Spittlebugs feed exclusively on xylem sap, a diet that is low both in essential amino acids and in sugar or other substrates for energy production. The new symbiont genome has undergone proliferation of mobile elements resulting in many gene inactivations; nonetheless, it has selectively maintained genes replacing functions of its predecessor for amino-acid biosynthesis. Whereas ancient symbiont partners typically retain perfectly complementary sets of amino-acid biosynthetic pathways, the novel symbiont introduces some redundancy as it retains some pathways also present in the partner Symbionts ( Sulcia muelleri ). Strikingly, the newly acquired Sodalis -like symbiont retains genes underlying efficient routes of energy production, including a complete TCA cycle, potentially relaxing the severe energy limitations of the xylem-feeding hosts. Although evolutionary replacements of ancient Symbionts are infrequent, they potentially enable evolutionary and ecological novelty by conferring novel metabolic capabilities to host lineages.
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evolutionary replacement of obligate Symbionts in an ancient and diverse insect lineage
Environmental Microbiology, 2013Co-Authors: Ryuichi Koga, Gordon M Bennett, Jason R Cryan, Nancy A MoranAbstract:: Many insect groups depend on ancient obligate symbioses with bacteria that undergo long-term genomic degradation due to inactivation and loss of ancestral genes. Sap-feeding insects in the hemipteran suborder Auchenorrhyncha show complex symbioses with at least two obligate bacterial Symbionts, inhabiting specialized host cells (bacteriocytes). We explored the symbiotic relationships of the spittlebugs (Auchenorrhyncha: Cercopoidea) using phylogenetic and microscopy methods. Results show that most spittlebugs contain the Symbionts Sulcia muelleri (Bacteroidetes) and Zinderia insecticola (Betaproteobacteria) with each restricted to its own bacteriocyte type. However, the ancestral Zinderia symbiont has been replaced with a novel symbiont closely related to Sodalis glossinidius (Enterobacteriaceae) in members of the ecologically successful spittlebug tribe Philaenini. At least one spittlebug species retains Sulcia and Zinderia, but also has acquired a Sodalis-like symbiont, possibly representing a transitional stage in the evolutionary succession of symbioses. Phylogenetic analyses including Symbionts of other Auchenorrhyncha lineages suggest that Zinderia, like Sulcia, descends from an ancestral symbiont present in the common ancestor of Auchenorrhyncha. This betaproteobacterial symbiont has been repeatedly replaced by other Symbionts, such as the Sodalis-like symbiont of spittlebugs. Symbiont replacement may offer a route for hosts to escape dependence on an ancient, degraded and potentially inefficient symbiont.
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facultative Symbionts in aphids and the horizontal transfer of ecologically important traits
Annual Review of Entomology, 2010Co-Authors: Kerry M Oliver, Gaelen R Burke, Patrick H Degnan, Nancy A MoranAbstract:Aphids engage in symbiotic associations with a diverse assemblage of heritable bacteria. In addition to their obligate nutrient-provisioning symbiont, Buchnera aphidicola, aphids may also carry one or more facultative Symbionts. Unlike obligate Symbionts, facultative Symbionts are not generally required for survival or reproduction and can invade novel hosts, based on both phylogenetic analyses and transfection experiments. Facultative Symbionts are mutualistic in the context of various ecological interactions. Experiments on pea aphids (Acyrthosiphon pisum) have demonstrated that facultative Symbionts protect against entomopathogenic fungi and parasitoid wasps, ameliorate the detrimental effects of heat, and influence host plant suitability. The protective symbiont, Hamiltonella defensa, has a dynamic genome, exhibiting evidence of recombination, phage-mediated gene uptake, and horizontal gene transfer and containing virulence and toxin-encoding genes. Although transmitted maternally with high fidelity, ...
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sexual acquisition of beneficial Symbionts in aphids
Proceedings of the National Academy of Sciences of the United States of America, 2006Co-Authors: Nancy A Moran, Helen E DunbarAbstract:A noted cost of mating is the risk of acquiring sexually transmitted infections that are detrimental to the recipient. But many microbial associates of eukaryotes are mutualistic, raising the possibility that sexual contact provides the opportunity to acquire Symbionts that are beneficial. In aphids, facultative bacterial Symbionts, which benefit hosts by conferring resistance to natural enemies or to heat, are transmitted maternally with high fidelity and are maintained stably throughout hundreds of parthenogenetic generations in the laboratory. Data from field populations indicate that horizontal transfer of these facultative Symbionts is frequent, and transfections are readily achieved by microinjection or ingestion in artificial diet. However, no natural mechanism for the horizontal transfer of these Symbionts has been identified. Here we demonstrate that during sexual reproduction, male-borne Symbionts can be acquired by females and subsequently transferred to sexually and parthenogenetically produced progeny, establishing stable, maternally transmitted associations. In our experiments, sexually transmitted Symbionts resulted in (i) infection of previously uninfected matrilines, (ii) a double infection in a matriline already bearing a different symbiont, and (iii) replacement of the maternal symbiont. We also observed some cases in which maternal Symbionts failed to become established in sexually produced progeny. Microscopy indicated that Symbionts were abundant in the male reproductive system, which demonstrates a natural route of nonmaternal transfer of insect Symbionts. Because such transfer can generate coinfections, thereby creating opportunities for symbiont competition and recombination, paternal inheritance has major consequences for expectations regarding symbiont evolution.
Youjun Zhang - One of the best experts on this subject based on the ideXlab platform.
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location of Symbionts in the whitefly bemisia tabaci affects their densities during host development and environmental stress
PLOS ONE, 2014Co-Authors: Qi Su, Shaoli Wang, Qingjun Wu, Murad Ghanim, Youjun ZhangAbstract:Bacterial Symbionts often enhance the physiological capabilities of their arthropod hosts and enable their hosts to expand into formerly unavailable niches, thus leading to biological diversification. Many arthropods, including the worldwide invasive whitefly Bemisia tabaci, have individuals simultaneously infected with Symbionts of multiple genera that occur in different locations in the host. This study examined the population dynamics of Symbionts that are located in different areas within B. tabaci. While densities of Portiera and Hamiltonella (which are located in bacteriocytes) appeared to be well-regulated during host development, densities of Rickettsia (which are not located in bacteriocytes) were highly variable among individual hosts during host development. Host mating did not significantly affect symbiont densities. Infection by Tomato yellow leaf curl virus did not affect Portiera and Hamiltonella densities in either sex, but increased Rickettsia densities in females. High and low temperatures did not affect Portiera and Hamiltonella densities, but low temperature (15°C) significantly suppressed Rickettsia densities whereas high temperature (35°C) had little effect on Rickettsia densities. The results are consistent with the view that the population dynamics of bacterial Symbionts in B. tabaci are regulated by symbiont location within the host and that the regulation reflects adaptation between the bacteria and insect.
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factors affecting population dynamics of maternally transmitted endoSymbionts in bemisia tabaci
PLOS ONE, 2012Co-Authors: Xianchun Li, Daqing Ge, Shaoli Wang, Qingjun Wu, Xiaoguo Jiao, Baoyun Xu, Youjun ZhangAbstract:While every individual of Bemisia tabaci (Hemiptera: Aleyrodidae) harbors the primary symbiont (P-symbiont) Portiera, the infection frequencies of the six secondary Symbionts (S-Symbionts) including Hamiltonella, Arsenophonus, Cardinium, Wolbachia, Rickettsia and Fritschea vary greatly among different populations. To characterize the factors influencing the infection dynamics of the six S-Symbionts in B. tabaci, gene-specific PCR were conducted to screen for the presence of the P-symbiont Portiera and the six S-Symbionts in 61 (17 B and 44 Q biotypes) field populations collected from different plant species and locations in China. All individuals of the 61 populations hosted the P-symbiont Portiera, but none of them harbored Arsenophonus and Fritschea. The presence and infection rates of Hamiltonella, Cardinium, Rickettsia, Wolbachia and their co-infections Rickettsia + Hamiltonella (RH), Rickettsia + Cardinium (RC), Hamiltonella + Cardinium (HC) and Rickettsia + Hamiltonella + Cardinium (RHC) varied significantly among the 61 field populations; and the observed variations can be explained by biotypes, sexes, host plants and geographical locations of these field populations. Taken together, at least three factors including biotype, host plant and geographical location affect the infection dynamics of S-Symbionts in B. tabaci.
Takahiro Hosokawa - One of the best experts on this subject based on the ideXlab platform.
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female specific specialization of a posterior end region of the midgut symbiotic organ in plautia splendens and allied stinkbugs
Applied and Environmental Microbiology, 2015Co-Authors: Takahiro Hosokawa, Xian-ying Meng, Takema Fukatsu, Ryuichi Koga, Toshinari HayashiAbstract:ABSTRACT Many stinkbugs (Insecta: Hemiptera: Heteroptera) are associated with bacterial Symbionts in a posterior region of the midgut. In these stinkbugs, adult females excrete symbiont-containing materials from the anus for transmission of the beneficial Symbionts to their offspring. For ensuring the vertical symbiont transmission, a variety of female-specific elaborate traits at the cellular, morphological, developmental, and behavioral levels have been reported from diverse stinkbugs of the families Plataspidae, Urostylididae, Parastrachiidae, etc. Meanwhile, such elaborate female-specific traits for vertical symbiont transmission have been poorly characterized for the largest and economically important stinkbug family Pentatomidae. Here, we investigated the midgut symbiotic system of a pentatomid stinkbug, Plautia splendens. A specific gammaproteobacterial symbiont was consistently present extracellularly in the cavity of numerous crypts arranged in four rows on the midgut fourth section. The symbiont was smeared on the egg surface upon oviposition by adult females, orally acquired by newborn nymphs, and thereby transmitted vertically to the next generation and important for growth and survival of the host insects. We found that, specifically in adult females, several rows of crypts at the posterior end region of the symbiotic midgut were morphologically differentiated and conspicuously enlarged, often discharging the symbiotic bacteria from the crypt cavity to the main tract of the symbiotic midgut. The female-specific enlarged end crypts were also found in other pentatomid stinkbugs Plautia stali and Carbula crassiventris. These results suggest that the enlarged end crypts represent a female-specific specialized morphological trait for vertical symbiont transmission commonly found among stinkbugs of the family Pentatomidae.
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Infection prevalence of Sodalis Symbionts among stinkbugs
Zoological letters, 2015Co-Authors: Takahiro Hosokawa, Nahomi Kaiwa, Yoshitomo Kikuchi, Yu Matsuura, Takema FukatsuAbstract:Diverse insects and other organisms are associated with microbial Symbionts, which often significantly contribute to growth and survival of their hosts and/or drastically affect phenotypes of their hosts in a variety of ways. Sodalis glossinidius was first identified as a facultative bacterial symbiont of tsetse flies, and recent studies revealed that Sodalis-allied bacteria encompass diverse ecological niches ranging from free-living bacteria through facultative Symbionts to obligate Symbionts associated with a diverse array of insects. Despite potential ecological and evolutionary relevance of the Sodalis Symbionts, their infection prevalence in natural insect populations has been poorly investigated. Here we surveyed diverse stinkbugs and allied terrestrial heteropteran bugs, which represented 17 families, 77 genera, 108 species, 310 populations and 960 individuals, for infection with the Sodalis Symbionts. Diagnostic PCR detected relatively low infection frequencies of the Sodalis Symbionts: 13.6% (14/103) of the species, 7.5% (22/295) of the populations, and 4.3% (35/822) of the individuals of the stinkbugs except for those belonging to the family Urostylididae. Among the urostylidid stinkbugs, strikingly, the Sodalis Symbionts exhibited very high infection frequencies: 100% (5/5) of the species, 100% (15/15) of the populations, and 94.2% (130/138) of the individuals we examined. Molecular phylogenetic analysis based on bacterial 16S rRNA gene sequences revealed that all the Symbionts were placed in the clade of Sodalis-allied bacteria while the symbiont phylogeny did not reflect the systematics of their stinkbug hosts. Notably, the Sodalis Symbionts of the urostylidid stinkbugs were not clustered with the Sodalis Symbionts of the other stinkbug groups on the phylogeny, suggesting their distinct evolutionary trajectories. The relatively low infection frequency and the overall host-symbiont phylogenetic incongruence suggest that the Sodalis Symbionts are, in general, facultative symbiotic associates in the majority of the stinkbug groups. On the other hand, it is conceivable, although speculative, that the Sodalis Symbionts may play some substantial biological roles for their host stinkbugs of the Urostylididae.
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an ancient but promiscuous host symbiont association between burkholderia gut Symbionts and their heteropteran hosts
The ISME Journal, 2011Co-Authors: Yoshitomo Kikuchi, Takahiro Hosokawa, Takema FukatsuAbstract:Here, we investigated 124 stinkbug species representing 20 families and 5 superfamilies for their Burkholderia gut Symbionts, of which 39 species representing 6 families of the superfamilies Lygaeoidea and Coreoidea were Burkholderia-positive. Diagnostic PCR surveys revealed high frequencies of Burkholderia infection in natural populations of the stinkbugs, and substantial absence of vertical transmission of Burkholderia infection to their eggs. In situ hybridization confirmed localization of the Burkholderia in their midgut crypts. In the lygaeoid and coreoid stinkbugs, development of midgut crypts in their alimentary tract was coincident with the Burkholderia infection, suggesting that the specialized morphological configuration is pivotal for establishment and maintenance of the symbiotic association. The Burkholderia Symbionts were easily isolated as pure culture on standard microbiological media, indicating the ability of the gut Symbionts to survive outside the host insects. Molecular phylogenetic analysis showed that the gut Symbionts of the lygaeoid and coreoid stinkbugs belong to a β-proteobacterial clade together with Burkholderia isolates from soil environments and Burkholderia species that induce plant galls. On the phylogeny, the stinkbug-associated, environmental and gall-forming Burkholderia strains did not form coherent groups, indicating host–symbiont promiscuity among these stinkbugs. Symbiont culturing revealed that slightly different Burkholderia genotypes often coexist in the same insects, which is also suggestive of host–symbiont promiscuity. All these results strongly suggest an ancient but promiscuous host–symbiont relationship between the lygaeoid/coreoid stinkbugs and the Burkholderia gut Symbionts. Possible mechanisms as to how the environmentally transmitted promiscuous symbiotic association has been stably maintained in the evolutionary course are discussed.
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Bacterial Symbionts of the Giant Jewel Stinkbug Eucorysses grandis (Hemiptera: Scutelleridae)
Zoological Science, 2011Co-Authors: Nahomi Kaiwa, Motomi Ito, Yoshitomo Kikuchi, Takahiro Hosokawa, Xian-ying Meng, Nobutada Kimura, Naruo Nikoh, Takema FukatsuAbstract:Microbiological characterization of gut symbiotic bacteria in a limited number of stinkbugs of the families Acanthosomatidae, Plataspidae, Pentatomidae, Scutelleridae, Parastrachiidae, Alydidae and Pyrrhocoridae has shown symbiotic association with midgut bacteria to be common in phytophagous taxa of these heteropteran insects. Here we investigated the midgut bacterial symbiont of Eucorysses grandis, a stinkbug of the family Scutelleridae. A specific gammaproteobacterium was consistently identified in insects from five different geographic origins. The bacterium was detected in 64 of 64 insects sampled from three host populations. Phylogenetic analyses revealed that the bacterium constitutes a distinct lineage in the Gammaproteobacteria, neither closely related to the gut symbiont of another scutellerid stinkbug, Cantao ocellatus, nor to gut Symbionts of other stinkbugs. Diagnostic PCR, in situ hybridization and electron microscopy demonstrated that the bacterium is located extracelluarly, in the midgut fourth section, which possesses crypts. These results indicate that the primary gut Symbionts have multiple evolutionary origins in the Scutelleridae. A Sodalis-allied facultative symbiont was also identified in some insects from natural populations. Biological aspects of the primary gut symbiont and the secondary Sodalis-allied symbiont are discussed.
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Host-symbiont co-speciation and reductive genome evolution in gut symbiotic bacteria of acanthosomatid stinkbugs
BMC Biology, 2009Co-Authors: Yoshitomo Kikuchi, Takahiro Hosokawa, Xian-ying Meng, Naruo Nikoh, Yoichi Kamagata, Takema FukatsuAbstract:Background Host-symbiont co-speciation and reductive genome evolution have been commonly observed among obligate endocellular insect Symbionts, while such examples have rarely been identified among extracellular ones, the only case reported being from gut symbiotic bacteria of stinkbugs of the family Plataspidae. Considering that gut symbiotic communities are vulnerable to invasion of foreign microbes, gut symbiotic associations have been thought to be evolutionarily not stable. Stinkbugs of the family Acanthosomatidae harbor a bacterial symbiont in the midgut crypts, the lumen of which is completely sealed off from the midgut main tract, thereby retaining the symbiont in the isolated cryptic cavities. We investigated histological, ecological, phylogenetic, and genomic aspects of the unique gut symbiosis of the acanthosomatid stinkbugs. Results Phylogenetic analyses showed that the acanthosomatid Symbionts constitute a distinct clade in the γ- Proteobacteria , whose sister groups are the obligate endocellular Symbionts of aphids Buchnera and the obligate gut Symbionts of plataspid stinkbugs Ishikawaella . In addition to the midgut crypts, the Symbionts were located in a pair of peculiar lubricating organs associated with the female ovipositor, by which the Symbionts are vertically transmitted via egg surface contamination. The Symbionts were detected not from ovaries but from deposited eggs, and surface sterilization of eggs resulted in symbiont-free hatchlings. The symbiont-free insects suffered retarded growth, high mortality, and abnormal morphology, suggesting important biological roles of the symbiont for the host insects. The symbiont phylogeny was generally concordant with the host phylogeny, indicating host-symbiont co-speciation over evolutionary time despite the extracellular association. Meanwhile, some local host-symbiont phylogenetic discrepancies were found, suggesting occasional horizontal symbiont transfers across the host lineages. The Symbionts exhibited AT-biased nucleotide composition, accelerated molecular evolution, and reduced genome size, as has been observed in obligate endocellular insect Symbionts. Conclusion Comprehensive studies of the acanthosomatid bacterial symbiosis provide new insights into the genomic evolution of extracellular symbiotic bacteria: host-symbiont co-speciation and drastic genome reduction can occur not only in endocellular symbiotic associations but also in extracellular ones. We suggest that many more such cases might be discovered in future surveys.
Eleanor R. Haine - One of the best experts on this subject based on the ideXlab platform.
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Symbiont-mediated protection
Proceedings of the Royal Society B: Biological Sciences, 2008Co-Authors: Eleanor R. HaineAbstract:Despite the fact that all vertically transmitted Symbionts sequester resources from their hosts and are therefore costly to maintain, there is an extraordinary diversity of them in invertebrates. Some spread through host populations by providing their hosts with fitness benefits or by manipulating host sex ratio, but some do not: their maintenance in host lineages remains an enigma. In this review, I explore the evolutionary ecology of vertically transmitted Symbionts and their impact on host resistance, and provide an overview of the evidence for the three-way interactions between these Symbionts, natural enemies and invertebrate hosts. A number of recent empirical and theoretical studies suggest that vertically transmitted Symbionts may protect their hosts from pathogens. If this ‘symbiont-mediated protection’ is widespread, it is likely that vertically transmitted Symbionts contribute significantly to variation in measures of invertebrate resistance to natural enemies.
