Highly transmissible cytoplasmic incompatibility by the extracellular insect symbiont Spiroplasma

Marie Pollmann; Logan D Moore; Elena Krimmer; Paul D'Alvise; Martin Hasselmann; Steve J Perlman; Matthew J Ballinger; Johannes L M Steidle; Yuval Gottlieb

doi:10.1016/j.isci.2022.104335

Highly transmissible cytoplasmic incompatibility by the extracellular insect symbiont Spiroplasma

iScience. 2022 Apr 29;25(5):104335. doi: 10.1016/j.isci.2022.104335. eCollection 2022 May 20.

Authors

Marie Pollmann¹, Logan D Moore², Elena Krimmer³, Paul D'Alvise⁴, Martin Hasselmann⁵, Steve J Perlman⁶, Matthew J Ballinger², Johannes L M Steidle^{1

7}, Yuval Gottlieb⁸

Affiliations

¹ Department of Chemical Ecology 190t, Institute of Biology, University of Hohenheim, 70599 Stuttgart, Germany.
² Department of Biological Sciences, Mississippi State University, Mississippi State, MS 39762, USA.
³ Department of Animal Ecology and Tropical Biology, Biocenter, University of Wuerzburg, 97074 Wuerzburg, Germany.
⁴ Institute of Medical Microbiology and Hygiene, University Hospital of Tuebingen, 72016 Tuebingen, Germany.
⁵ Department of Livestock Population Genomics 460h, Institute of Animal Science, University of Hohenheim, 70599 Stuttgart, Germany.
⁶ Department of Biology, University of Victoria, Victoria, BC V8W 3N5, Canada.
⁷ KomBioTa - Center of Biodiversity and Integrative Taxonomy, University of Hohenheim, 70599 Stuttgart, Germany.
⁸ Koret School of Veterinary Medicine, Robert H. Smith Faculty of Agriculture, Food and Environment, Hebrew University of Jerusalem, POB 12, Rehovot 76100, Israel.

Abstract

Cytoplasmic incompatibility (CI) is a form of reproductive manipulation caused by maternally inherited endosymbionts infecting arthropods, like Wolbachia, whereby matings between infected males and uninfected females produce few or no offspring. We report the discovery of a new CI symbiont, a strain of Spiroplasma causing CI in the parasitoid wasp Lariophagus distinguendus. Its extracellular occurrence enabled us to establish CI in uninfected adult insects by transferring Spiroplasma-infected hemolymph. We sequenced the CI-Spiroplasma genome and did not find any homologues of any of the cif genes discovered to cause CI in Wolbachia, suggesting independent evolution of CI. Instead, the genome contains other potential CI-causing candidate genes, such as homologues of high-mobility group (HMG) box proteins that are crucial in eukaryotic development but rare in bacterial genomes. Spiroplasma's extracellular nature and broad host range encompassing medically and agriculturally important arthropods make it a promising tool to study CI and its applications.

Keywords: Entomology; Microbiology; Microbiology parasite; Zoology.