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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Published in:PLoS pathogens Vol. 13; no. 7; p. e1006431
Main Authors: Ballinger, Matthew J., Perlman, Steve J.
Format: Journal Article
Language:English
Published: United States Public Library of Science 06.07.2017
Public Library of Science (PLoS)
Subjects:
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
Online Access:Get full text
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Summary: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.
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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