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Male-killing mechanisms vary between Spiroplasma species

Male-killing, a male-specific death of arthropod hosts during development, is induced by Spiroplasma (Mollicutes) endosymbionts of the Citri–Poulsonii and the Ixodetis groups, which are phylogenetically distant groups. Spiroplasma poulsonii induces male-killing in Drosophila melanogaster (Diptera) u...

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Autores principales: Arai, Hiroshi, Inoue, Maki N., Kageyama, Daisuke
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9742256/
https://www.ncbi.nlm.nih.gov/pubmed/36519169
http://dx.doi.org/10.3389/fmicb.2022.1075199
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author Arai, Hiroshi
Inoue, Maki N.
Kageyama, Daisuke
author_facet Arai, Hiroshi
Inoue, Maki N.
Kageyama, Daisuke
author_sort Arai, Hiroshi
collection PubMed
description Male-killing, a male-specific death of arthropod hosts during development, is induced by Spiroplasma (Mollicutes) endosymbionts of the Citri–Poulsonii and the Ixodetis groups, which are phylogenetically distant groups. Spiroplasma poulsonii induces male-killing in Drosophila melanogaster (Diptera) using the Spaid toxin that harbors ankyrin repeats, whereas little is known about the origin and mechanisms of male-killing induced by Spiroplasma ixodetis. Here, we analyzed the genome and the biological characteristics of a male-killing S. ixodetis strain sHm in the moth Homona magnanima (Tortricidae, Lepidoptera). Strain sHm harbored a 2.1 Mb chromosome and two potential plasmids encoding Type IV effectors, putatively involved in virulence and host–symbiont interactions. Moreover, sHm did not harbor the spaid gene but harbored 10 ankyrin genes that were homologous to those in other S. ixodetis strains. In contrast to the predominant existence of S. poulsonii in hemolymph, our quantitative PCR assays revealed a systemic distribution of strain sHm in H. magnanima, with particularly high titers in Malpighian tubules but low titers in hemolymph. Furthermore, transinfection assays confirmed that strain sHm can infect cultured cells derived from distantly related insects, namely Aedes albopictus (Diptera) and Bombyx mori (Lepidoptera). These results suggest different origins and characteristics of S. ixodetis- and S. poulsonii-induced male-killing.
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spelling pubmed-97422562022-12-13 Male-killing mechanisms vary between Spiroplasma species Arai, Hiroshi Inoue, Maki N. Kageyama, Daisuke Front Microbiol Microbiology Male-killing, a male-specific death of arthropod hosts during development, is induced by Spiroplasma (Mollicutes) endosymbionts of the Citri–Poulsonii and the Ixodetis groups, which are phylogenetically distant groups. Spiroplasma poulsonii induces male-killing in Drosophila melanogaster (Diptera) using the Spaid toxin that harbors ankyrin repeats, whereas little is known about the origin and mechanisms of male-killing induced by Spiroplasma ixodetis. Here, we analyzed the genome and the biological characteristics of a male-killing S. ixodetis strain sHm in the moth Homona magnanima (Tortricidae, Lepidoptera). Strain sHm harbored a 2.1 Mb chromosome and two potential plasmids encoding Type IV effectors, putatively involved in virulence and host–symbiont interactions. Moreover, sHm did not harbor the spaid gene but harbored 10 ankyrin genes that were homologous to those in other S. ixodetis strains. In contrast to the predominant existence of S. poulsonii in hemolymph, our quantitative PCR assays revealed a systemic distribution of strain sHm in H. magnanima, with particularly high titers in Malpighian tubules but low titers in hemolymph. Furthermore, transinfection assays confirmed that strain sHm can infect cultured cells derived from distantly related insects, namely Aedes albopictus (Diptera) and Bombyx mori (Lepidoptera). These results suggest different origins and characteristics of S. ixodetis- and S. poulsonii-induced male-killing. Frontiers Media S.A. 2022-11-28 /pmc/articles/PMC9742256/ /pubmed/36519169 http://dx.doi.org/10.3389/fmicb.2022.1075199 Text en Copyright © 2022 Arai, Inoue and Kageyama. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Arai, Hiroshi
Inoue, Maki N.
Kageyama, Daisuke
Male-killing mechanisms vary between Spiroplasma species
title Male-killing mechanisms vary between Spiroplasma species
title_full Male-killing mechanisms vary between Spiroplasma species
title_fullStr Male-killing mechanisms vary between Spiroplasma species
title_full_unstemmed Male-killing mechanisms vary between Spiroplasma species
title_short Male-killing mechanisms vary between Spiroplasma species
title_sort male-killing mechanisms vary between spiroplasma species
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9742256/
https://www.ncbi.nlm.nih.gov/pubmed/36519169
http://dx.doi.org/10.3389/fmicb.2022.1075199
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