Phenotypic Effect of “Candidatus Rickettsiella viridis,” a Facultative Symbiont of the Pea Aphid (Acyrthosiphon pisum), and Its Interaction with a Coexisting Symbiont

Abstract

A gammaproteobacterial facultative symbiont of the genus Rickettsiella was recently identified in the pea aphid, Acyrthosiphon pisum. Infection with this symbiont altered the color of the aphid body from red to green, potentially affecting the host's ecological characteristics, such as attractiveness to different natural enemies. In European populations of A. pisum, the majority of Rickettsiella-infected aphids also harbor another facultative symbiont, of the genus Hamiltonella. We investigated this Rickettsiella symbiont for its interactions with the coinfecting Hamiltonella symbiont, its phenotypic effects on A. pisum with and without Hamiltonella coinfection, and its infection prevalence in A. pisum populations. Histological analyses revealed that coinfecting Rickettsiella and Hamiltonella exhibited overlapping localizations in secondary bacteriocytes, sheath cells, and hemolymph, while Rickettsiella-specific localization was found in oenocytes. Rickettsiella infections consistently altered hosts' body color from red to green, where the greenish hue was affected by both host and symbiont genotypes. Rickettsiella-Hamiltonella coinfections also changed red aphids to green; this greenish hue tended to be enhanced by Hamiltonella coinfection. With different host genotypes, Rickettsiella infection exhibited either weakly beneficial or nearly neutral effects on host fitness, whereas Hamiltonella infection and Rickettsiella-Hamiltonella coinfection had negative effects. Despite considerable frequencies of Rickettsiella infection in European and North American A. pisum populations, no Rickettsiella infection was detected among 1,093 insects collected from 14 sites in Japan. On the basis of these results, we discuss possible mechanisms for the interaction of Rickettsiella with other facultative symbionts, their effects on their hosts' phenotypes, and their persistence in natural host populations. We propose the designation "Candidatus Rickettsiella viridis" for the symbiont.

Consequences of coinfection with protective symbionts on the host phenotype and symbiont titres in the pea aphid system

“…96 generations. These 8 aphid lineages have already been studied for body color changes (summarized in Table ) and presented in recent publications where elimination/transfection symbiont procedures are reported with further details (Tsuchida et al ., ; Tsuchida et al ., ).…”

Happens in the best of subfamilies: establishment and repeated replacements of co‐obligate secondary endosymbionts within Lachninae aphids

“…Buchnera, as other 'ancient' obligate endosymbionts, underwent a rapid genome erosion early in its evolutionary history with aphids, resulting in a high degree of synteny among distantly related Buchnera (Tamas et al, 2002;van Ham et al, 2003), and since then, lineages of both partners have been co-diverging. To date, various secondary facultative bacterial endosymbionts have been identified, primarily in the pea aphid Acyrthosiphon pisum (Aphidinae subfamily) (Fukatsu et al, 2000(Fukatsu et al, , 2001Sakurai et al, 2005;Degnan et al, 2009a,b;Guay et al, 2009;Tsuchida et al, 2014). Besides Buchnera, aphids can also harbour secondary endosymbionts (in addition to the primary symbiont), these being of facultative or obligate nature in some lineages.…”

Candidate pathogenicity islands in the genome of ‘CandidatusRickettsiella isopodorum’, an intracellular bacterium infecting terrestrial isopod crustaceans

“…Unlike R. isopodorum , its DNA was found at a low density in our sequencing data, suggesting it did not proliferate as strongly within its host, although it could have just been in the early stages of infection. Although Rickettsiella is traditionally described as a potent pathogen (Dutky & Gooden, 1952; Hall & Badgley, 1957; Kleespies, Federici & Leclerque, 2014), recently, benign or even beneficial Rickettsiella endosymbionts have been found in other arthropod lineages (Tsuchida et al, 2010; Tsuchida et al, 2014; Iasur-Kruh et al, 2013), and some evidence suggests some forms of Rickettsiella may also be capable of vertical transmission (Iasur-Kruh et al, 2013). Consistent with this hypothesis, Dittmer et al (2016) report that Rickettsiella was detected even in some isopods that did not show symptoms.…”

“…However, based on 16S rRNA gene sequence analyses, this genus has been recently reclassified to the order Legionellales in the Gammaproteobacteria, which also includes human pathogens such as Coxiella and Legionella (Roux et al, 1997; Cordaux et al, 2007; Leclerque, 2008; Leclerque & Kleespies, 2008b; Leclerque & Kleespies, 2008c). There are several described species in the genus Rickettsiella : R. popilliae  (Dutky & Gooden, 1952), R. grylli  (Vago & Martoja, 1963), R. chironomi (Weiser & Žižka, 1968), R. stethorae  (Hall & Badgley, 1957), plus the recently described ‘ Candidatus Rickettsiella isopodorum’ (Kleespies, Federici & Leclerque, 2014) and ‘ Candidatus Rickettsiella viridis’ (Tsuchida et al, 2014). There are also several additional pathotypes thought to be synonyms of the previously recognized species, including R. tipulae  (Leclerque & Kleespies, 2008a), R. agriotidis  (Leclerque et al, 2011a), R. pyronotae  (Kleespies et al, 2011), and R. costelytrae  (Leclerque et al, 2012).…”

“…is correlated with the intensity of green coloration, potentially helping evade predators (Tsuchida et al, 2010). In another study on pea aphids, Rickettsiella was shown to have neutral or positive effects on host fitness, depending on host genotype and whether the host was coinfected with Hamiltonella  (Tsuchida et al, 2014). …”