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Microbiome analyses of 12 psyllid species of the family Psyllidae identified various bacteria including Fukatsuia and Serratia symbiotica, known as secondary symbionts of aphids

BACKGROUND: Psyllids (Hemiptera: Psylloidea) comprise a group of plant sap-sucking insects that includes important agricultural pests. They have close associations not only with plant pathogens, but also with various microbes, including obligate mutualists and facultative symbionts. Recent studies a...

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Autores principales: Nakabachi, Atsushi, Inoue, Hiromitsu, Hirose, Yuu
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8740488/
https://www.ncbi.nlm.nih.gov/pubmed/34996376
http://dx.doi.org/10.1186/s12866-021-02429-2
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author Nakabachi, Atsushi
Inoue, Hiromitsu
Hirose, Yuu
author_facet Nakabachi, Atsushi
Inoue, Hiromitsu
Hirose, Yuu
author_sort Nakabachi, Atsushi
collection PubMed
description BACKGROUND: Psyllids (Hemiptera: Psylloidea) comprise a group of plant sap-sucking insects that includes important agricultural pests. They have close associations not only with plant pathogens, but also with various microbes, including obligate mutualists and facultative symbionts. Recent studies are revealing that interactions among such bacterial populations are important for psyllid biology and host plant pathology. In the present study, to obtain further insight into the ecological and evolutionary behaviors of bacteria in Psylloidea, we analyzed the microbiomes of 12 psyllid species belonging to the family Psyllidae (11 from Psyllinae and one from Macrocorsinae), using high-throughput amplicon sequencing of the 16S rRNA gene. RESULTS: The analysis showed that all 12 psyllids have the primary symbiont, Candidatus Carsonella ruddii (Gammaproteobacteria: Oceanospirillales), and at least one secondary symbiont. The majority of the secondary symbionts were gammaproteobacteria, especially those of the family Enterobacteriaceae (order: Enterobacteriales). Among them, symbionts belonging to “endosymbionts3”, which is a genus-level monophyletic group assigned by the SILVA rRNA database, were the most prevalent and were found in 9 of 11 Psyllinae species. Ca. Fukatsuia symbiotica and Serratia symbiotica, which were recognized only as secondary symbionts of aphids, were also identified. In addition to other Enterobacteriaceae bacteria, including Arsenophonus, Sodalis, and “endosymbionts2”, which is another genus-level clade, Pseudomonas (Pseudomonadales: Pseudomonadaceae) and Diplorickettsia (Diplorickettsiales: Diplorickettsiaceae) were identified. Regarding Alphaproteobacteria, the potential plant pathogen Ca. Liberibacter europaeus (Rhizobiales: Rhizobiaceae) was detected for the first time in Anomoneura mori (Psyllinae), a mulberry pest. Wolbachia (Rickettsiales: Anaplasmataceae) and Rickettsia (Rickettsiales: Rickettsiaceae), plausible host reproduction manipulators that are potential tools to control pest insects, were also detected. CONCLUSIONS: The present study identified various bacterial symbionts including previously unexpected lineages in psyllids, suggesting considerable interspecific transfer of arthropod symbionts. The findings provide deeper insights into the evolution of interactions among insects, bacteria, and plants, which may be exploited to facilitate the control of pest psyllids in the future. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-021-02429-2.
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spelling pubmed-87404882022-01-07 Microbiome analyses of 12 psyllid species of the family Psyllidae identified various bacteria including Fukatsuia and Serratia symbiotica, known as secondary symbionts of aphids Nakabachi, Atsushi Inoue, Hiromitsu Hirose, Yuu BMC Microbiol Research BACKGROUND: Psyllids (Hemiptera: Psylloidea) comprise a group of plant sap-sucking insects that includes important agricultural pests. They have close associations not only with plant pathogens, but also with various microbes, including obligate mutualists and facultative symbionts. Recent studies are revealing that interactions among such bacterial populations are important for psyllid biology and host plant pathology. In the present study, to obtain further insight into the ecological and evolutionary behaviors of bacteria in Psylloidea, we analyzed the microbiomes of 12 psyllid species belonging to the family Psyllidae (11 from Psyllinae and one from Macrocorsinae), using high-throughput amplicon sequencing of the 16S rRNA gene. RESULTS: The analysis showed that all 12 psyllids have the primary symbiont, Candidatus Carsonella ruddii (Gammaproteobacteria: Oceanospirillales), and at least one secondary symbiont. The majority of the secondary symbionts were gammaproteobacteria, especially those of the family Enterobacteriaceae (order: Enterobacteriales). Among them, symbionts belonging to “endosymbionts3”, which is a genus-level monophyletic group assigned by the SILVA rRNA database, were the most prevalent and were found in 9 of 11 Psyllinae species. Ca. Fukatsuia symbiotica and Serratia symbiotica, which were recognized only as secondary symbionts of aphids, were also identified. In addition to other Enterobacteriaceae bacteria, including Arsenophonus, Sodalis, and “endosymbionts2”, which is another genus-level clade, Pseudomonas (Pseudomonadales: Pseudomonadaceae) and Diplorickettsia (Diplorickettsiales: Diplorickettsiaceae) were identified. Regarding Alphaproteobacteria, the potential plant pathogen Ca. Liberibacter europaeus (Rhizobiales: Rhizobiaceae) was detected for the first time in Anomoneura mori (Psyllinae), a mulberry pest. Wolbachia (Rickettsiales: Anaplasmataceae) and Rickettsia (Rickettsiales: Rickettsiaceae), plausible host reproduction manipulators that are potential tools to control pest insects, were also detected. CONCLUSIONS: The present study identified various bacterial symbionts including previously unexpected lineages in psyllids, suggesting considerable interspecific transfer of arthropod symbionts. The findings provide deeper insights into the evolution of interactions among insects, bacteria, and plants, which may be exploited to facilitate the control of pest psyllids in the future. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s12866-021-02429-2. BioMed Central 2022-01-07 /pmc/articles/PMC8740488/ /pubmed/34996376 http://dx.doi.org/10.1186/s12866-021-02429-2 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Nakabachi, Atsushi
Inoue, Hiromitsu
Hirose, Yuu
Microbiome analyses of 12 psyllid species of the family Psyllidae identified various bacteria including Fukatsuia and Serratia symbiotica, known as secondary symbionts of aphids
title Microbiome analyses of 12 psyllid species of the family Psyllidae identified various bacteria including Fukatsuia and Serratia symbiotica, known as secondary symbionts of aphids
title_full Microbiome analyses of 12 psyllid species of the family Psyllidae identified various bacteria including Fukatsuia and Serratia symbiotica, known as secondary symbionts of aphids
title_fullStr Microbiome analyses of 12 psyllid species of the family Psyllidae identified various bacteria including Fukatsuia and Serratia symbiotica, known as secondary symbionts of aphids
title_full_unstemmed Microbiome analyses of 12 psyllid species of the family Psyllidae identified various bacteria including Fukatsuia and Serratia symbiotica, known as secondary symbionts of aphids
title_short Microbiome analyses of 12 psyllid species of the family Psyllidae identified various bacteria including Fukatsuia and Serratia symbiotica, known as secondary symbionts of aphids
title_sort microbiome analyses of 12 psyllid species of the family psyllidae identified various bacteria including fukatsuia and serratia symbiotica, known as secondary symbionts of aphids
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8740488/
https://www.ncbi.nlm.nih.gov/pubmed/34996376
http://dx.doi.org/10.1186/s12866-021-02429-2
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