Psyllids (Hemiptera: Sternorrhyncha: Psylloidea) are plant sap-sucking insects that include important agricultural pests. To obtain insights into the ecological and evolutionary behaviors of microbes, including plant pathogens, in Psylloidea, high-resolution analyses of the microbiomes of nine psyllid species belonging to the family Triozidae were performed using high-throughput amplicon sequencing of the 16S rRNA gene. Analyses identified various bacterial populations, showing that all nine psyllids have at least one secondary symbiont, along with the primary symbiont “Candidatus Carsonella ruddii” (Gammaproteobacteria: Oceanospirillales: Halomonadaceae). The majority of the secondary symbionts were gammaproteobacteria, particularly those of the order Enterobacterales, which included Arsenophonus and Serratia symbiotica, a bacterium formerly recognized only as a secondary symbiont of aphids (Hemiptera: Sternorrhyncha: Aphidoidea). The non-Enterobacterales gammaproteobacteria identified in the present study were Diplorickettsia (Diplorickettsiales: Diplorickettsiaceae), a potential human pathogen, and Carnimonas (Oceanospirillales: Halomonadaceae), a lineage detected for the first time in Psylloidea. Regarding alphaproteobacteria, the potential plant pathogen “Ca. Liberibacter europaeus” (Rhizobiales: Rhizobiaceae) was detected for the first time in Epitrioza yasumatsui, which feeds on the Japanese silverberry Elaeagnus umbellata (Elaeagnaceae), an aggressive invasive plant in the United States and Europe. Besides the detection of Wolbachia (Rickettsiales: Anaplasmataceae) of supergroup B in three psyllid species, a lineage belonging to supergroup O was identified for the first time in Psylloidea. These results suggest the rampant transfer of bacterial symbionts among animals and plants, thereby providing deeper insights into the evolution of interkingdom interactions among multicellular organisms and bacteria, which will facilitate the control of pest psyllids.
"}],"abstractLicenseFlag":"disallow"}],"creator":[{"@id":"https://cir.nii.ac.jp/crid/1420282801197065344","@type":"Researcher","personIdentifier":[{"@type":"KAKEN_RESEARCHERS","@value":"40332267"},{"@type":"NRID","@value":"1000040332267"},{"@type":"NRID","@value":"9000310314252"},{"@type":"NRID","@value":"9000310315297"},{"@type":"NRID","@value":"9000001904536"},{"@type":"NRID","@value":"9000310318278"},{"@type":"NRID","@value":"9000261656041"},{"@type":"NRID","@value":"9000345301366"},{"@type":"NRID","@value":"9000018910970"},{"@type":"NRID","@value":"9000310321045"},{"@type":"NRID","@value":"9000310314199"},{"@type":"NRID","@value":"9000310314219"},{"@type":"NRID","@value":"9000310320969"},{"@type":"NRID","@value":"9000310314201"},{"@type":"NRID","@value":"9000311771704"},{"@type":"NRID","@value":"9000310318799"},{"@type":"NRID","@value":"9000367031748"},{"@type":"RESEARCHMAP","@value":"https://researchmap.jp/CRDC_SSDC"}],"foaf:name":[{"@language":"en","@value":"Nakabachi Atsushi"}],"jpcoar:affiliationName":[{"@language":"en","@value":"Electronics-Inspired Interdisciplinary Research Institute (EIIRIS), Toyohashi University of Technology"},{"@language":"en","@value":"Department of Applied Chemistry and Life Sciences, Toyohashi University of Technology"}]},{"@id":"https://cir.nii.ac.jp/crid/1410294330154201600","@type":"Researcher","foaf:name":[{"@language":"en","@value":"Inoue Hiromitsu"}],"jpcoar:affiliationName":[{"@language":"en","@value":"Institute for Plant Protection, National Agriculture and Food Research Organization"}]},{"@id":"https://cir.nii.ac.jp/crid/1410294330154201601","@type":"Researcher","foaf:name":[{"@language":"en","@value":"Hirose Yuu"}],"jpcoar:affiliationName":[{"@language":"en","@value":"Department of Applied Chemistry and Life Sciences, Toyohashi University of Technology"}]}],"publication":{"publicationIdentifier":[{"@type":"PISSN","@value":"13426311"},{"@type":"LISSN","@value":"13426311"},{"@type":"EISSN","@value":"13474405"},{"@type":"NDL_BIB_ID","@value":"000000389713"},{"@type":"ISSN","@value":"13426311"},{"@type":"NCID","@value":"AA11551577"}],"prism:publicationName":[{"@language":"ja","@value":"Ｍｉｃｒｏｂｅｓ ａｎｄ ｅｎｖｉｒｏｎｍｅｎｔｓ"},{"@language":"en","@value":"Microbes and Environments"},{"@language":"en","@value":"Microb. Environ."},{"@language":"en","@value":"Microbes Environ."},{"@language":"en","@value":"Microbes and environments"},{"@language":"ja","@value":"Ｍｉｃｒｏｂｅｓ ａｎｄ ｅｎｖｉｒｏｎｍｅｎｔｓ"}],"dc:publisher":[{"@language":"en","@value":"Japanese Society of Microbial Ecology / Japanese Society of Soil Microbiology / Taiwan Society of Microbial Ecology / Japanese Society of Plant Microbe Interactions / Japanese Society for Extremophiles"},{"@language":"ja","@value":"日本微生物生態学会 / 日本土壌微生物学会 / Taiwan Society of Microbial Ecology / 植物微生物研究会 / 極限環境生物学会"}],"prism:publicationDate":"2022","prism:volume":"37","prism:number":"4","prism:startingPage":"n/a"},"reviewed":"false","dcterms:accessRights":"http://purl.org/coar/access_right/c_abf2","url":[{"@id":"http://id.ndl.go.jp/bib/032628872"},{"@id":"https://ndlsearch.ndl.go.jp/books/R000000004-I032628872"},{"@id":"https://www.jstage.jst.go.jp/article/jsme2/37/4/37_ME22078/_pdf"}],"availableAt":"2022","foaf:topic":[{"@id":"https://cir.nii.ac.jp/all?q=%3Ci%3ELiberibacter%3C/i%3E","dc:title":"Liberibacter"},{"@id":"https://cir.nii.ac.jp/all?q=%3Ci%3EWolbachia%3C/i%3E%20supergroup%20O","dc:title":"Wolbachia supergroup O"},{"@id":"https://cir.nii.ac.jp/all?q=%3Ci%3EDiplorickettsia%3C/i%3E","dc:title":"Diplorickettsia"},{"@id":"https://cir.nii.ac.jp/all?q=%3Ci%3ESerratia%20symbiotica%3C/i%3E","dc:title":"Serratia symbiotica"},{"@id":"https://cir.nii.ac.jp/all?q=%3Ci%3ECarnimonas%3C/i%3E","dc:title":"Carnimonas"}],"project":[{"@id":"https://cir.nii.ac.jp/crid/1040003825719103104","@type":"Project","projectIdentifier":[{"@type":"KAKEN","@value":"20H02998"},{"@type":"JGN","@value":"JP20H02998"},{"@type":"URI","@value":"https://kaken.nii.ac.jp/grant/KAKENHI-PROJECT-20H02998/"}],"notation":[{"@language":"ja","@value":"「オルガネラ様防衛共生体」の基盤解析から応用展開へ"},{"@language":"en","@value":"From the fundamental analysis to the application development of \"organelle-like defensive symbionts\""}]}],"relatedProduct":[{"@id":"https://cir.nii.ac.jp/crid/1360011142936348672","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies"}]},{"@id":"https://cir.nii.ac.jp/crid/1360011143863432960","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Extraordinary proliferation of microorganisms in aposymbiotic pea aphids, Acyrthosiphon pisum"}]},{"@id":"https://cir.nii.ac.jp/crid/1360011146038879360","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Wolbachia: master manipulators of invertebrate biology"}]},{"@id":"https://cir.nii.ac.jp/crid/1360013170666269440","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Controlling for Contaminants in Low-Biomass 16S rRNA Gene Sequencing Experiments"}]},{"@id":"https://cir.nii.ac.jp/crid/1360013172710740864","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Uncovering Symbionts Across the Psyllid Tree of Life and the Discovery of a New Liberibacter Species, “Candidatus” Liberibacter capsica"}]},{"@id":"https://cir.nii.ac.jp/crid/1360283690861640064","@type":"Article","resourceType":"学術雑誌論文(journal article)","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Defensive Bacteriome Symbiont with a Drastically Reduced Genome"}]},{"@id":"https://cir.nii.ac.jp/crid/1360283692578587264","@type":"Article","resourceType":"学術雑誌論文(journal article)","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Parallel Histories of Horizontal Gene Transfer Facilitated Extreme Reduction of Endosymbiont Genomes in Sap-Feeding Insects"}]},{"@id":"https://cir.nii.ac.jp/crid/1360285710548677888","@type":"Article","resourceType":"学術雑誌論文(journal article)","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"A full‐length cDNA resource for the pea aphid,\n Acyrthosiphon pisum"}]},{"@id":"https://cir.nii.ac.jp/crid/1360285712513020800","@type":"Article","resourceType":"学術雑誌論文(journal article)","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Horizontal Gene Acquisition of Liberibacter Plant Pathogens from a Bacteriome-Confined Endosymbiont of Their Psyllid Vector"}]},{"@id":"https://cir.nii.ac.jp/crid/1360292617908774656","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"DADA2: High-resolution sample inference from Illumina amplicon data"}]},{"@id":"https://cir.nii.ac.jp/crid/1360292617917314944","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"BLAST+: architecture and applications"}]},{"@id":"https://cir.nii.ac.jp/crid/1360292618594650752","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"First report of ‘Candidatus Liberibacter europaeus’ in the United Kingdom"}]},{"@id":"https://cir.nii.ac.jp/crid/1360292619918993536","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Cospeciation of Psyllids and Their Primary Prokaryotic Endosymbionts"}]},{"@id":"https://cir.nii.ac.jp/crid/1360292621169692544","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"A Small\n Wolbachia\n Protein Directly Represses Phage Lytic Cycle Genes in “\n Candidatus\n Liberibacter asiaticus” within Psyllids"}]},{"@id":"https://cir.nii.ac.jp/crid/1360292621387717376","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Differential Display of mRNAs Related to Amino Acid Metabolism in the Endosymbiotic System of Aphids"}]},{"@id":"https://cir.nii.ac.jp/crid/1360298341433460992","@type":"Article","resourceType":"学術雑誌論文(journal article)","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Diaphorin, a Polyketide Produced by a Bacterial Symbiont of the Asian Citrus Psyllid, Inhibits the Growth and Cell Division of Bacillus subtilis but Promotes the Growth and Metabolic Activity of Escherichia coli"}]},{"@id":"https://cir.nii.ac.jp/crid/1360298343110260608","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Potato Zebra Chip: An Overview of the Disease, Control Strategies, and Prospects"}]},{"@id":"https://cir.nii.ac.jp/crid/1360298343141006336","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Molecular detection and phylogenetic analyses of Wolbachia in natural populations of nine galling Aphid species"}]},{"@id":"https://cir.nii.ac.jp/crid/1360298345074891136","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Made for Each Other: Vector–Pathogen Interfaces in the Huanglongbing Pathosystem"}]},{"@id":"https://cir.nii.ac.jp/crid/1360301785962921984","@type":"Article","resourceType":"学術雑誌論文(journal article)","relationType":["isReferencedBy"],"jpcoar:relatedTitle":[{"@value":"Ultrastructure of the bacteriome and bacterial symbionts in the Asian citrus psyllid,\n Diaphorina citri"}]},{"@id":"https://cir.nii.ac.jp/crid/1360567182022865664","@type":"Article","resourceType":"学術雑誌論文(journal article)","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Horizontal gene transfers in insects"}]},{"@id":"https://cir.nii.ac.jp/crid/1360568466980268800","@type":"Article","resourceType":"学術雑誌論文(journal article)","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Concentration and distribution of diaphorin, and expression of diaphorin synthesis genes during Asian citrus psyllid development"}]},{"@id":"https://cir.nii.ac.jp/crid/1360574093480472576","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Arsenophonus, an emerging clade of intracellular symbionts with a broad host distribution"}]},{"@id":"https://cir.nii.ac.jp/crid/1360574093981395968","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Diplorickettsia massiliensis as a human pathogen"}]},{"@id":"https://cir.nii.ac.jp/crid/1360574095506645888","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Combining 'omics and microscopy to visualize interactions between the Asian citrus psyllid vector and the Huanglongbing pathogen Candidatus Liberibacter asiaticus in the insect gut"}]},{"@id":"https://cir.nii.ac.jp/crid/1360574095575910400","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Deep Characterization of the Microbiomes of Calophya spp. (Hemiptera: Calophyidae) Gall-Inducing Psyllids Reveals the Absence of Plant Pathogenic Bacteria and Three Dominant Endosymbionts"}]},{"@id":"https://cir.nii.ac.jp/crid/1360574095732593664","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Aphids acquired symbiotic genes via lateral gene transfer"}]},{"@id":"https://cir.nii.ac.jp/crid/1360574096445010176","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Genomics and Evolution of Heritable Bacterial Symbionts"}]},{"@id":"https://cir.nii.ac.jp/crid/1360576118786415872","@type":"Article","resourceType":"学術雑誌論文(journal article)","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Comparative Genomics Underlines Multiple Roles of Profftella, an Obligate Symbiont of Psyllids: Providing Toxins, Vitamins, and Carotenoids"}]},{"@id":"https://cir.nii.ac.jp/crid/1360576118786659840","@type":"Article","resourceType":"学術雑誌論文(journal article)","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Microbiome analyses of 12 psyllid species of the family Psyllidae identified various bacteria including Fukatsuia and Serratia symbiotica, known as secondary symbionts of aphids"}]},{"@id":"https://cir.nii.ac.jp/crid/1360576122222323712","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"An updated classification of the jumping plant-lice (Hemiptera: Psylloidea) integrating molecular and morphological evidence"}]},{"@id":"https://cir.nii.ac.jp/crid/1360576122344360832","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Vertical Transmission at the Pathogen-Symbiont Interface: Serratia symbiotica and Aphids"}]},{"@id":"https://cir.nii.ac.jp/crid/1360579820498099200","@type":"Article","resourceType":"学術雑誌論文(journal article)","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Extreme Polyploidy of\n Carsonella\n , an Organelle-Like Bacterium with a Drastically Reduced Genome"}]},{"@id":"https://cir.nii.ac.jp/crid/1360846640815110784","@type":"Article","resourceType":"学術雑誌論文(journal article)","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Aphid gene of bacterial origin encodes a protein transported to an obligate endosymbiont"}]},{"@id":"https://cir.nii.ac.jp/crid/1360846644420191488","@type":"Article","resourceType":"学術雑誌論文(journal article)","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Behavior of bacteriome symbionts during transovarial transmission and development of the Asian citrus psyllid"}]},{"@id":"https://cir.nii.ac.jp/crid/1360848657942908928","@type":"Article","resourceType":"学術雑誌論文(journal article)","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Genome size ofPachypsylla venusta(Hemiptera: Psyllidae) and the ploidy of its bacteriocyte, the symbiotic host cell that harbors intracellular mutualistic bacteria with the smallest cellular genome"}]},{"@id":"https://cir.nii.ac.jp/crid/1360848660897689472","@type":"Article","resourceType":"学術雑誌論文(journal article)","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Diversity of Bacterial Endosymbionts Associated with Macrosteles Leafhoppers Vectoring Phytopathogenic Phytoplasmas"}]},{"@id":"https://cir.nii.ac.jp/crid/1360850167420518912","@type":"Article","resourceType":"学術雑誌論文(journal article)","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Diaphorin, a polyketide synthesized by an intracellular symbiont of the Asian citrus psyllid, is potentially harmful for biological control agents"}]},{"@id":"https://cir.nii.ac.jp/crid/1360855567863055360","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2"}]},{"@id":"https://cir.nii.ac.jp/crid/1360855569087445760","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"SINA: Accurate high-throughput multiple sequence alignment of ribosomal RNA genes"}]},{"@id":"https://cir.nii.ac.jp/crid/1360855570772632448","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"A Genus Definition for\n Bacteria\n and\n Archaea\n Based on a Standard Genome Relatedness Index"}]},{"@id":"https://cir.nii.ac.jp/crid/1361131415710349056","@type":"Article","resourceType":"学術雑誌論文(journal article)","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"16S rRNA Sequencing Detected Profftella, Liberibacter, Wolbachia, and Diplorickettsia from Relatives of the Asian Citrus Psyllid"}]},{"@id":"https://cir.nii.ac.jp/crid/1361137044079488768","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin"}]},{"@id":"https://cir.nii.ac.jp/crid/1361137044901079296","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Genetic variation and potential coinfection of Wolbachia among widespread Asian citrus psyllid (Diaphorina citri Kuwayama) populations"}]},{"@id":"https://cir.nii.ac.jp/crid/1361137045538570240","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences"}]},{"@id":"https://cir.nii.ac.jp/crid/1361137045619236608","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Secondary Endosymbionts of Psyllids Have Been Acquired Multiple Times"}]},{"@id":"https://cir.nii.ac.jp/crid/1361413117375405824","@type":"Article","resourceType":"学術雑誌論文(journal article)","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Diaphorin, a polyketide produced by a bacterial symbiont of the Asian citrus psyllid, kills various human cancer cells"}]},{"@id":"https://cir.nii.ac.jp/crid/1361699994167766272","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Transcriptome analysis of the aphid bacteriocyte, the symbiotic host cell that harbors an endocellular mutualistic bacterium,\n Buchnera"}]},{"@id":"https://cir.nii.ac.jp/crid/1361699994826349184","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Symbiotic bacteria motivate the foraging decision and promote fecundity and survival of Bactrocera dorsalis (Diptera: Tephritidae)"}]},{"@id":"https://cir.nii.ac.jp/crid/1361699995136630272","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Provision of riboflavin to the host aphid, Acyrthosiphon pisum, by endosymbiotic bacteria, Buchnera"}]},{"@id":"https://cir.nii.ac.jp/crid/1361699996273744000","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"25 years of serving the community with ribosomal RNA gene reference databases and tools"}]},{"@id":"https://cir.nii.ac.jp/crid/1361981468551605888","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Biology and Management of Asian Citrus Psyllid, Vector of the Huanglongbing Pathogens"}]},{"@id":"https://cir.nii.ac.jp/crid/1361981469573195648","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"A genomic analysis of transcytosis in the pea aphid,\n Acyrthosiphon pisum\n , a mechanism involved in virus transmission"}]},{"@id":"https://cir.nii.ac.jp/crid/1361981470741003776","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"A standardized bacterial taxonomy based on genome phylogeny substantially revises the tree of life"}]},{"@id":"https://cir.nii.ac.jp/crid/1362544420431944960","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Symbionts in waiting: the dynamics of incipient endosymbiont complementation and replacement in minimal bacterial communities of psyllids"}]},{"@id":"https://cir.nii.ac.jp/crid/1362825893408966016","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Wolbachia pipientis should not be split into multiple species: A response to Ramírez-Puebla et al., “Species in Wolbachia? Proposal for the designation of ‘Candidatus Wolbachia bourtzisii’, ‘Candidatus Wolbachia onchocercicola’, ‘Candidatus Wolbachia blaxteri’, ‘Candidatus Wolbachia brugii’, ‘Candidatus Wolbachia taylori’, ‘Candidatus Wolbachia collembolicola’ and ‘Candidatus Wolbachia multihospitum’ for the different species within Wolbachia supergroups”"}]},{"@id":"https://cir.nii.ac.jp/crid/1362825893629386624","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Inter-Population Variability of Endosymbiont Densities in the Asian Citrus Psyllid (Diaphorina citri Kuwayama)"}]},{"@id":"https://cir.nii.ac.jp/crid/1362825894855800960","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"The bacterial communities in plant phloem‐sap‐feeding insects"}]},{"@id":"https://cir.nii.ac.jp/crid/1362825895440080512","@type":"Article","relationType":["references"],"jpcoar:relatedTitle":[{"@value":"Uncovering symbiont‐driven genetic diversity across