Defensive endosymbionts: a cryptic trophic level in community ecology

Jaenike, John; Brekke, Thomas D.

doi:10.1111/j.1461-0248.2010.01564.x

Cited by 56 publications

(52 citation statements)

References 37 publications

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“…In D. neotestacea, we have observed no fitness costs associated with Spiroplasma (e.g., ref. 21), and population cage experiments also suggest that direct costs of Spiroplasma-toxin-induced or otherwise-are negligible or context-dependent in this symbiosis (47).…”

Section: Discussionmentioning

confidence: 83%

A ribosome-inactivating protein in a Drosophila defensive symbiont

Hamilton

Peng

Boulanger

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

117

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Vertically transmitted symbionts that protect their hosts against parasites and pathogens are well known from insects, yet the underlying mechanisms of symbiont-mediated defense are largely unclear. A striking example of an ecologically important defensive symbiosis involves the woodland fly Drosophila neotestacea, which is protected by the bacterial endosymbiont Spiroplasma when parasitized by the nematode Howardula aoronymphium. The benefit of this defense strategy has led to the rapid spread of Spiroplasma throughout the range of D. neotestacea, although the molecular basis for this protection has been unresolved. Here, we show that Spiroplasma encodes a ribosome-inactivating protein (RIP) related to Shiga-like toxins from enterohemorrhagic Escherichia coli and that Howardula ribosomal RNA (rRNA) is depurinated during Spiroplasma-mediated protection of D. neotestacea. First, we show that recombinant Spiroplasma RIP catalyzes depurination of 28S rRNAs in a cell-free assay, as well as Howardula rRNA in vitro at the canonical RIP target site within the α-sarcin/ricin loop (SRL) of 28S rRNA. We then show that Howardula parasites in Spiroplasma-infected flies show a strong signal of rRNA depurination consistent with RIP-dependent modification and large decreases in the proportion of 28S rRNA intact at the α-sarcin/ricin loop. Notably, host 28S rRNA is largely unaffected, suggesting targeted specificity. Collectively, our study identifies a novel RIP in an insect defensive symbiont and suggests an underlying RIP-dependent mechanism in Spiroplasma-mediated defense.symbiosis | male-killing | Spiroplasma | Shiga toxin | nematode

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Section: Discussionmentioning

confidence: 83%

A ribosome-inactivating protein in a Drosophila defensive symbiont

Hamilton

Peng

Boulanger

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

117

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“…Mutualistic effects may prove more common and/or more important for Wolbachia prevalence than reproductive manipulation (cf. Jaenike & Brekke 2011). …”

Section: Discussionmentioning

confidence: 99%

Wolbachiado not live by reproductive manipulation alone: infection polymorphism inDrosophila suzukiiandD. subpulchrella

et al. 2014

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Drosophila suzukii recently invaded North America and Europe. Populations in Hawaii, California, New York and Nova Scotia are polymorphic for Wolbachia, typically with <20% infection frequency. The Wolbachia in D. suzukii, denoted wSuz, is closely related to wRi, the variant prevalent in continental populations of D. simulans. wSuz is also nearly identical to Wolbachia found in D. subpulchrella, plausibly D. suzukii's sister species. This suggests vertical Wolbachia transmission through cladogenesis (“cladogenic transmission”). The widespread occurrence of 7-20% infection frequencies indicates a stable polymorphism. wSuz is imperfectly maternally transmitted, with wild infected females producing on average 5-10% uninfected progeny. As expected from its low frequency, wSuz produces no cytoplasmic incompatibility (CI), i.e., no elevated embryo mortality when infected males mate with uninfected females, and no appreciable sex-ratio distortion. The persistence of wSuz despite imperfect maternal transmission suggests positive fitness effects. Assuming a balance between selection and imperfect transmission, we expect a fitness advantage on the order of 20%. Unexpectedly, Wolbachia-infected females produce fewer progeny than do uninfected females. We do not yet understand the maintenance of wSuz in D. suzukii. The absence of detectable CI in D. suzukii and D. subpulchrella makes it unlikely that CI-based mechanisms could be used to control this species without transinfection using novel Wolbachia. Contrary to their reputation as horizontally transmitted reproductive parasites, many Wolbachia infections are acquired through introgression or cladogenesis and many cause no appreciable reproductive manipulation. Such infections, likely to be mutualistic, may be central to understanding the pervasiveness of Wolbachia among arthropods.

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“…chinensis sand flies. Endosymbionts have complex interactions with their hosts, such as parthenogenesis, male killing, cytoplasm incompatibility, and host defence4150515253. Although most of Rickettsiella spp.…”

Section: Discussionmentioning

confidence: 99%

Diversity of bacteriome associated with Phlebotomus chinensis (Diptera: Psychodidae) sand flies in two wild populations from China

Chen

Jiang

et al. 2016

Sci Rep

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Sand fly Phlebotomus chinensis is a primary vector of transmission of visceral leishmaniasis in China. The sand flies have adapted to various ecological niches in distinct ecosystems. Characterization of the microbial structure and function will greatly facilitate the understanding of the sand fly ecology, which would provide critical information for developing intervention strategy for sand fly control. In this study we compared the bacterial composition between two populations of Ph. chinensis from Henan and Sichuan, China. The phylotypes were taxonomically assigned to 29 genera of 19 families in 9 classes of 5 phyla. The core bacteria include Pseudomonas and enterobacteria, both are shared in the sand flies in the two regions. Interestingly, the endosymbionts Wolbachia and Rickettsia were detected only in Henan, while the Rickettsiella and Diplorickettsia only in Sichuan. The intracellular bacteria Rickettsia, Rickettsiella and Diplorickettsia were reported for the first time in sand flies. The influence of sex and feeding status on the microbial structure was also detected in the two populations. The findings suggest that the ecological diversity of sand fly in Sichuan and Henan may contribute to shaping the structure of associated microbiota. The structural classification paves the way to function characterization of the sand fly associated microbiome.

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Defensive endosymbionts: a cryptic trophic level in community ecology

Cited by 56 publications

References 37 publications

A ribosome-inactivating protein in a Drosophila defensive symbiont

A ribosome-inactivating protein in a Drosophila defensive symbiont

Wolbachiado not live by reproductive manipulation alone: infection polymorphism inDrosophila suzukiiandD. subpulchrella

Diversity of bacteriome associated with Phlebotomus chinensis (Diptera: Psychodidae) sand flies in two wild populations from China

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