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.2005 Jul;71(7):4069-75.
doi: 10.1128/AEM.71.7.4069-4075.2005.

Rickettsia symbiont in the pea aphid Acyrthosiphon pisum: novel cellular tropism, effect on host fitness, and interaction with the essential symbiont Buchnera

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Rickettsia symbiont in the pea aphid Acyrthosiphon pisum: novel cellular tropism, effect on host fitness, and interaction with the essential symbiont Buchnera

Makiko Sakurai et al. Appl Environ Microbiol.2005 Jul.

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 mum long and 0.5 mum 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.

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Figures

FIG. 1.
FIG. 1.
Molecular phylogenetic analysis of theRickettsia symbiont fromA. pisum strain OY. (A) Neighbor-joining tree on the basis of 16S rRNA gene sequences. A total of 1,417 unambiguously aligned nucleotide sites were subjected to the analysis. (B) Neighbor-joining tree on the basis ofgltA gene sequences. A total of 353 unambiguously aligned nucleotide sites were subjected to the analysis. The percent bootstrap values are shown at the nodes, although values less than 70% are not indicated. The numbers in brackets are accession numbers. Three major groups in the genusRickettsia, “spotted fever group,” “typhus group,” and “bellii group,” are indicated on the right side.
FIG. 2.
FIG. 2.
Whole-mount in situ hybridization of aphid embryos targetingRickettsia (red) andBuchnera (green). (A) Mycetomes of an aphid embryo in which secondary mycetocytes and sheath cells harboringRickettsia are seen in addition to a number of primary mycetocytes harboringBuchnera. (B to D) Magnified images of mycetome. Arrows, secondary mycetocytes; arrowheads, sheath cells; bars, 50 μm.
FIG. 3.
FIG. 3.
Electron microscopy of theRickettsia symbiont. (A) A sheath cell harboring rod-shaped cells of theRickettsia symbiont (arrows) surrounded by primary mycetocytes harboringBuchnera (asterisks). (B) A magnified image of theRickettsia cells in a sheath cell. (C) Virus-like particles (arrowheads) in association with theRickettsia cells. Abbreviations: ShC, sheath cell; PM, primary mycetocyte.
FIG. 4.
FIG. 4.
Infection dynamics ofRickettsia andBuchnera in the developmental course of the host aphid. (A)Rickettsia titers in terms ofgltA gene copies per insect. (B)Rickettsia densities in terms ofgltA gene copies peref1α gene copy. (C)Buchnera titers in terms ofgroEL gene copies per insect. (D)Buchnera densities in terms ofgroEL gene copies peref1α gene copy. Open circles, theRickettsia-infected aphid strain OYdw; closed squares, theRickettsia-eliminated aphid strain OYamp. Means and standard deviations are shown (n = 12, respectively). Asterisks indicate statistically significant differences (Mann-Whitney U test; *,P < 0.05; **,P < 0.01; ***,P < 0.001). The measurements were conducted at 18 to 20 generations after the injection treatments.
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