Although previously examined for their...

Although previously examined for their roles in CI induction, our analysis of the Wolbachia TA modules indicates that they 1) are part of a large family of highly mosaic genes that are dispersed across a limited number of intracellular bacteria (and in some cases their host arthropod genomes), and 2) likely comprise only a subset of a large pool of mosaic genes with roles in other modes of RP, namely parthenogenesis, feminization and male killing. The latter is supported by the presence of pLbAR_38/36 (R. felis str. LSU-Lb) and nuclease TA modules (O. tsutsugamushi) in species known to strongly correlate with parthenogenesis in their respective hosts. We also found multiple CI-like TA module components in the genome of the Cardinium endosymbiont of the sweet potato whitefly Bemisia tabaci (hereafter cBtQ1) (table 1). This was surprising, as RP phenotypes have not previously been observed in B. tabaci despite other Cardinium strains being known to induce feminization, CI or parthenogenesis in various arthropod hosts (Hunter et al. 2003; Gotoh et al. 2007; White et al. 2011). The components we found in cBtQ1 may be decaying, consistent with elevated numbers of transposable elements, recently inactivated genes and chromosomal rearrangements in the cBtQ1 genome (Santos-Garcia et al. 2014). Conversely, we did not find evidence for CI-like TA modules in the genome of the CI-inducing Cardinium strain cEper1, an endoparasite of Encarsia wasps (Penz et al. 2012), although a recent report illuminated unrelated candidate CI-inducing proteins in this species (Mann et al. 2017). Importantly, some of the cBtQ1 CI-like TA module components are encoded on a plasmid (pcBtQ1), indicating that these elements are a part of the Cardinium mobilome and should not be overlooked as factors contributing to CI and other RP phenotypes in arthropod populations harboring these endoparasites. Whether different host cytological phenotypes caused by CI-inducing Cardinium and Wolbachia strains are underpinned by similar or unrelated molecular factors remains to be determined (Gebiola et al. 2017).

Table 1

Open in new tab

Obligate Intracellular Bacteria (Excluding Wolbachia Species) Containing Multiple Factors Potentially Associated with Host Reproductive Parasitism

Species	Host^a	DUB^b	NUC^c	Other^d	AT^e	RP^f
Rickettsia felis str. LSU-Lb	Liposcelis bostrychophila^B	OTU, CE, CE*	2*	Yes	Yes	PI
Orientia tsutsugamushi	Leptotrombidium mites	CE*	2	Yes	Yes*	PI
Cardinium endosymbiont cBtQ1	Bemisia tabaci^W	CA	1	Yes	No	?
“Cand. Rickettsiella isopodorum”	Terrestrial isopods	CE (2)	2	No	No	–
Diplorickettsia massiliensis	Ixodes ricinus^H	CE	–	Yes	No	–
Rickettsia gravesii	Amblyomma limbatum^S	CE, CE*	2*	Yes	Yes	–
Rickettsia amblyommatis	Amblyomma ticks^S	CE, CE*	2	No	Yes*	–
Rickettsia argasii	Argas dewae^H	CE*	1	Yes	Yes*	–
Rickettsia hoogstraalii	Carios capensis^S	CE*	3	Yes	Yes*	–
Rickettsia bellii	Many tick species^H,S	CE*, CE^	–	Yes	No	–
Occidentia massiliensis	Ornithodoros sonrai^S	–	–	Yes	Yes	–

Species	Host^a	DUB^b	NUC^c	Other^d	AT^e	RP^f
Rickettsia felis str. LSU-Lb	Liposcelis bostrychophila^B	OTU, CE, CE*	2*	Yes	Yes	PI
Orientia tsutsugamushi	Leptotrombidium mites	CE*	2	Yes	Yes*	PI
Cardinium endosymbiont cBtQ1	Bemisia tabaci^W	CA	1	Yes	No	?
“Cand. Rickettsiella isopodorum”	Terrestrial isopods	CE (2)	2	No	No	–
Diplorickettsia massiliensis	Ixodes ricinus^H	CE	–	Yes	No	–
Rickettsia gravesii	Amblyomma limbatum^S	CE, CE*	2*	Yes	Yes	–
Rickettsia amblyommatis	Amblyomma ticks^S	CE, CE*	2	No	Yes*	–
Rickettsia argasii	Argas dewae^H	CE*	1	Yes	Yes*	–
Rickettsia hoogstraalii	Carios capensis^S	CE*	3	Yes	Yes*	–
Rickettsia bellii	Many tick species^H,S	CE*, CE^	–	Yes	No	–
Occidentia massiliensis	Ornithodoros sonrai^S	–	–	Yes	Yes	–

B, booklouse; W, silverleaf whitefly; H, hard ticks (Ixodidae); S, soft ticks (Argasidae).

Deubiquitinases, or ubiquitin-like proteases (see figs. 2 and 3): OTU, ovarian tumor-like cysteine protease; CE, clan CE protease (similar to CidB and other Type I CI-inducing toxins); CE*, clan CE protease (RickCE-like); CE^, clan CE protease (Sca15 passenger domain); CA, clan CA protease (peptidase C19R subfamily, also found in Cardinium endosymbiont cEper1 of Encarsia pergandiella, GenBank acc. no. CCM09810).

PD-(D/E)XK nuclease (see fig. 4): similar to nucleases of CinB and Type II–IV CI-inducing toxins. Asterisks indicate domains occurring within the same protein as DUB domains.

Large region with unknown function (coordinates 1174-2813 of pLbAR_38); see fig. 1 and supplementary fig. S1, Supplementary Material online.

In silico identification of pLbAR_36/CidA/CinA antitoxins (see fig. 5). Asterisks depict multiple (some possibly degrading) genes per genome.

Predicted RP phenotype: PI, parthenogenesis induction; ?, other Cardinium strains induce RP phenotypes, but not strain cBtQ1.

This Feature Is Available To Subscribers Only