Generality of toxins in defensive symbiosis: Ribosome-inactivating proteins and defense against parasitic wasps in Drosophila

While it has become increasingly clear that multicellular organisms often harbor microbial symbionts that protect their hosts against natural enemies, the mechanistic underpinnings underlying most defensive symbioses are largely unknown. Spiroplasma bacteria are widespread associates of terrestrial...

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Vydané v:	PLoS pathogens Ročník 13; číslo 7; s. e1006431
Hlavní autori:	Ballinger, Matthew J., Perlman, Steve J.
Médium:	Journal Article
Jazyk:	English
Vydavateľské údaje:	United States Public Library of Science 06.07.2017 Public Library of Science (PLoS)
Predmet:	Abundance Animal defenses Animals Arthropods Bacteria Bacterial Proteins - genetics Bacterial Proteins - metabolism Bacterial Proteins - toxicity Bacterial Toxins - genetics Bacterial Toxins - metabolism Bacterial Toxins - toxicity Biological Evolution Biology Biology and Life Sciences Cellular proteins Defensive behavior Drosophila - genetics Drosophila - microbiology Drosophila - parasitology Drosophila - physiology E coli Ectoparasites Eggs Evolution Flies Genetic aspects Genomes Host-parasite relationships Insects Larva - genetics Larva - microbiology Larva - parasitology Larva - physiology Larvae Low density lipoprotein receptors Medicine and Health Sciences Microorganisms Natural enemies Nematodes Parasites Properties Proteins Research and Analysis Methods Ribonucleic acid Ribosome Inactivating Proteins - genetics Ribosome Inactivating Proteins - metabolism Ribosome Inactivating Proteins - toxicity Ribosome-inactivating protein Ribosomes Ricin RNA rRNA 28S Spiroplasma - genetics Spiroplasma - metabolism Symbionts Symbiosis Terrestrial environments Toxins Wasps - drug effects Wasps - physiology Woodlands
ISSN:	1553-7374, 1553-7366, 1553-7374
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Shrnutí:	While it has become increasingly clear that multicellular organisms often harbor microbial symbionts that protect their hosts against natural enemies, the mechanistic underpinnings underlying most defensive symbioses are largely unknown. Spiroplasma bacteria are widespread associates of terrestrial arthropods, and include strains that protect diverse Drosophila flies against parasitic wasps and nematodes. Recent work implicated a ribosome-inactivating protein (RIP) encoded by Spiroplasma, and related to Shiga-like toxins in enterohemorrhagic Escherichia coli, in defense against a virulent parasitic nematode in the woodland fly, Drosophila neotestacea. Here we test the generality of RIP-mediated protection by examining whether Spiroplasma RIPs also play a role in wasp protection, in D. melanogaster and D. neotestacea. We find strong evidence for a major role of RIPs, with ribosomal RNA (rRNA) from the larval endoparasitic wasps, Leptopilina heterotoma and Leptopilina boulardi, exhibiting the hallmarks of RIP activity. In Spiroplasma-containing hosts, parasitic wasp ribosomes show abundant site-specific depurination in the α-sarcin/ricin loop of the 28S rRNA, with depurination occurring soon after wasp eggs hatch inside fly larvae. Interestingly, we found that the pupal ectoparasitic wasp, Pachycrepoideus vindemmiae, escapes protection by Spiroplasma, and its ribosomes do not show high levels of depurination. We also show that fly ribosomes show little evidence of targeting by RIPs. Finally, we find that the genome of D. neotestacea's defensive Spiroplasma encodes a diverse repertoire of RIP genes, which are differ in abundance. This work suggests that specificity of defensive symbionts against different natural enemies may be driven by the evolution of toxin repertoires, and that toxin diversity may play a role in shaping host-symbiont-enemy interactions.
Bibliografia:	ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Conceptualization: MJB SJP.Data curation: MJB.Formal analysis: MJB.Funding acquisition: SJP.Investigation: MJB.Methodology: MJB SJP.Project administration: MJB SJP.Resources: SJP.Supervision: SJP.Validation: MJB SJP.Visualization: MJB.Writing – original draft: MJB SJP.Writing – review & editing: MJB SJP. The authors have declared that no competing interests exist.
ISSN:	1553-7374 1553-7366 1553-7374
DOI:	10.1371/journal.ppat.1006431