Endosymbiotic Rickettsiella causes cytoplasmic incompatibility in a spider host

Abstract

14Many arthropod hosts are infected with bacterial endosymbionts that manipulate host 15 reproduction, but few bacterial taxa have been shown to cause such manipulations. Here we 16show that a bacterial strain in the genus Rickettsiella causes cytoplasmic incompatibility (CI) 17 between infected and uninfected hosts. We first surveyed the bacterial community of the 18 agricultural spider Mermessus fradeorum (Linyphiidae) using high throughput sequencing and 19found that individual spiders can be infected with up to five different strains of maternally-20 inherited symbiont from the genera Wolbachia, Rickettsia, and Rickettsiella. The Rickettsiella 21 strain was pervasive, found in all 23 tested spider matrilines. We used antibiotic curing to 22 generate uninfected matrilines that we reciprocally crossed with individuals infected only with 23Rickettsiella. We found that only 13% of eggs hatched when uninfected females were mated 24with Rickettsiella-infected males; in contrast, at least 83% of eggs hatched in the other cross 25 types. This is the first documentation of Rickettsiella, or any Gammaproteobacteria, causing CI. 26We speculate that induction of CI may be much more widespread among maternally-inherited 27 bacteria than previously appreciated. Further, our results reinforce the importance of thoroughly 28 characterizing and assessing the inherited microbiome before attributing observed host 29 phenotypes to well-characterized symbionts such as Wolbachia. 30 31

Symbiont-mediated cytoplasmic incompatibility: What have we learned in 50 years?

“…Since then, advances have significantly expanded our recognition of Wolbachia ’s incredible and complex toolset. In particular, biologists now appreciate CI as a common form of reproductive parasitism that symbionts, including Wolbachia and Cardinium , use to rapidly spread through populations ( Hunter et al, 2003 ; Rosenwald et al, 2020 ; Takano et al, 2017 ; Turelli, 1994 ; Weinert et al, 2015 ; Zug and Hammerstein, 2012 ). CI is associated with reproductive isolation ( Bordenstein et al, 2001 ; Gebiola et al, 2017 ; Jaenike et al, 2006 ) and is leveraged as a successful tool in the prevention of arboviral diseases that infect humans ( Crawford et al, 2020 ; O'Neill, 2018 ; Tantowijoyo et al, 2020 ).…”

“…Additionally, unknown symbionts of Brontispa longissimi coconut beetles and Lariophagus distinguendus parasitoid wasps cause CI, but they are not Wolbachia or Cardinium ( König et al, 2019 ; Takano et al, 2017 ). In addition, Gammaproteobacteria of the genus Rickettsiella cause CI in Mermessus fradeorum spiders ( Rosenwald et al, 2020 ). This review will focus primarily on Wolbachia -induced CI, but other symbionts will be discussed when information is available.…”

The Genetic Diversity of Rickettsiella Symbionts in Ixodes ricinus Throughout Europe

“…have been also associated with other arthropods, including insects, arachnids, and crustaceans [23][24][25][26][27][28][29]. Depending on the arthropod host, the infection by some Rickettsiella species was shownto hinder the hosts' development and survival [23], or manipulate host reproduction [30]. Other Rickettsiella spp.…”

Symbiont-Mediated Cytoplasmic Incompatibility: What have we Learned in 50 Years?

“…Since then, a century of advances have significantly expanded our recognition of Wolbachia's incredible and complex toolset. In particular, biologists now appreciate CI as a common form of reproductive parasitism that symbionts including Wolbachia and Cardinium use to rapidly spread through populations (Hunter et al, 2003;Rosenwald et al, 2020;Takano et al, 2017;Turelli, 1994;Weinert et al, 2015;Zug and Hammerstein, 2012). CI is associated with reproductive isolation (Bordenstein et al, 2001;Gebiola et al, 2017;Jaenike et al, 2006) and is leveraged as a successful tool in the prevention of arboviral diseases that infect humans (Crawford et al, 2020;O'Neill, 2018;Tantowijoyo et al, 2020).…”

“…Additionally, unknown symbionts of Brontispa longissimi coconut beetles and Lariophagus distinguendus parasitoid wasps cause CI, but they are not Wolbachia or Cardinium (König et al, 2019;Takano et al, 2017). In addition, Rickettsiella Gammaproteobacteria cause CI in Mermessus fradeorum spiders (Rosenwald et al, 2020). This review will focus primarily on Wolbachia-induced CI, but other symbionts will be discussed when information is available.…”