4.6 Article

Male-killing mechanisms vary between Spiroplasma species

Journal

FRONTIERS IN MICROBIOLOGY
Volume 13, Issue -, Pages -

Publisher

FRONTIERS MEDIA SA
DOI: 10.3389/fmicb.2022.1075199

Keywords

Spiroplasma; male-killing; symbiosis; evolution; endosymbionts; Homona magnanima; spaid

Categories

Funding

  1. Japan Society for the Promotion of Science (JSPS) Research Fellowships for Young Scientists
  2. JSPS [19J13123, 21J00895]
  3. Cabinet Office, Government of Japan, Cross-ministerial Moonshot Agriculture, Forestry and Fisheries Research and Development Program [22K14902]
  4. [JPJ009237]

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This study analyzed the genome and characteristics of a male-killing S. ixodetis strain in a moth species. The strain showed different genetic features compared to other strains and distributed systemically within the host. Additionally, the strain could infect distantly related insects. These findings reveal distinct origins and characteristics of S. ixodetis- and S. poulsonii-induced male-killing.
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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