Rickettsia Symbiont in the Pea Aphid Acyrthosiphon pisum : Novel Cellular Tropism, Effect on Host Fitness, and Interaction with the Essential Symbiont Buchnera

Abstract

In natural populations of the pea aphid Acyrthosiphon pisum, a facultative bacterial symbiont of the genus Rickettsia has been detected at considerable infection frequencies worldwide. We investigated the effects of the Rickettsia symbiont on the host aphid and also on the coexisting essential symbiont Buchnera. In situ hybridization revealed that the Rickettsia symbiont was specifically localized in two types of host cells specialized for endosymbiosis: secondary mycetocytes and sheath cells. Electron microscopy identified bacterial rods, about 2 m long and 0.5 m thick, in sheath cells of Rickettsia-infected aphids. Virus-like particles were sometimes observed in association with the bacterial cells. By an antibiotic treatment, we generated Rickettsia-infected and Rickettsia-eliminated aphid strains with an identical genetic background. Comparison of these strains revealed that Rickettsia infection negatively affected some components of the host fitness. Quantitative PCR analysis of the bacterial population dynamics identified a remarkable interaction between the coexisting symbionts: Buchnera population was significantly suppressed in the presence of Rickettsia, particularly at the young adult stage, when the aphid most actively reproduces. On the basis of these results, we discussed the possible mechanisms that enable the prevalence of Rickettsia infection in natural host populations in spite of the negative fitness effects observed in the laboratory.

Bacterial symbionts in insects or the story of communities affecting communities

“…In such circumstances, symbionts monopolizing resources should be selected for at the within-host level, if this increases the efficiency of their own vertical transmission. Examples of such competitive interactions have been illustrated between secondary symbionts [6,102], but also in situations of co-infections between primary and secondary symbionts [103,104]. If symbionts evolve higher competitive ability, this may further limit the maintenance of multiple infections.…”

Acquisition ofRickettsia felisby Cat Fleas During Feeding

“…Arthropods are the primary host of all rickettsial species and many rickettsial species are inherited and maintained via transovarial and transstadial transmission within arthropods (Sakurai et al 2005). Vertical transmission of R. felis has been described in detail and is the primary transmission strategy in the LSU cat flea colony (Wedincamp and Foil 2002).…”

Purine biosynthesis-deficient Burkholderia mutants are incapable of symbiotic accommodation in the stinkbug

“…Previous studies on symbiont infection density have been conducted on whole insects without symbiont cultivation: different combinations of host and symbiont genotypes were experimentally generated by microinjection, antibiotic therapy and/or introgression, and infection densities of the symbionts in the different host-symbiont combinations were evaluated by quantitative PCR. These studies have demonstrated that symbiont infection dynamics are significantly affected by the symbiont genotype (McGraw et al, 2002;Ikeda et al, 2003;Mouton et al, 2003Mouton et al, , 2004, host genotype (Kondo et al, 2005;Mouton et al, 2007), interactions between co-infecting symbionts (Koga et al, 2003;Kondo et al, 2005;Sakurai et al, 2005;Goto et al, 2006) and/or other environmental factors (Mouton et al, 2007;Anbutsu et al, 2008). However, it is not clear which symbiont genes are involved in the infection dynamics and regulation of symbiont density.…”

“…Previous studies have shown that the infection density of the symbiont can affect the fidelity of vertical transmission, the degree of reproductive aberrations and the level of fitness consequences as indicated by body size, growth, survival and/or fecundity (McGraw et al, 2002;Koga et al, 2003;Mouton et al, 2004;Sakurai et al, 2005;Kikuchi et al, 2007;Kim et al, 2013b). The mechanisms underlying the infection, proliferation and maintenance of symbionts within their host organisms are therefore of ecological and evolutionary importance (Kondo et al, 2005;Engelstadter et al, 2006;Vautrin and Vavre, 2009).…”