Tags

Type your tag names separated by a space and hit enter

Generality of toxins in defensive symbiosis: Ribosome-inactivating proteins and defense against parasitic wasps in Drosophila.
PLoS Pathog 2017; 13(7):e1006431PP

Abstract

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.

Authors+Show Affiliations

Department of Biology, University of Victoria, Victoria, BC, Canada.Department of Biology, University of Victoria, Victoria, BC, Canada. Integrated Microbial Biodiversity Program, Canadian Institute for Advanced Research, Toronto, ON, Canada.

Pub Type(s)

Journal Article

Language

eng

PubMed ID

28683136

Citation

Ballinger, Matthew J., and Steve J. Perlman. "Generality of Toxins in Defensive Symbiosis: Ribosome-inactivating Proteins and Defense Against Parasitic Wasps in Drosophila." PLoS Pathogens, vol. 13, no. 7, 2017, pp. e1006431.
Ballinger MJ, Perlman SJ. Generality of toxins in defensive symbiosis: Ribosome-inactivating proteins and defense against parasitic wasps in Drosophila. PLoS Pathog. 2017;13(7):e1006431.
Ballinger, M. J., & Perlman, S. J. (2017). Generality of toxins in defensive symbiosis: Ribosome-inactivating proteins and defense against parasitic wasps in Drosophila. PLoS Pathogens, 13(7), pp. e1006431. doi:10.1371/journal.ppat.1006431.
Ballinger MJ, Perlman SJ. Generality of Toxins in Defensive Symbiosis: Ribosome-inactivating Proteins and Defense Against Parasitic Wasps in Drosophila. PLoS Pathog. 2017;13(7):e1006431. PubMed PMID: 28683136.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Generality of toxins in defensive symbiosis: Ribosome-inactivating proteins and defense against parasitic wasps in Drosophila. AU - Ballinger,Matthew J, AU - Perlman,Steve J, Y1 - 2017/07/06/ PY - 2017/04/18/received PY - 2017/05/23/accepted PY - 2017/7/7/entrez PY - 2017/7/7/pubmed PY - 2017/12/20/medline SP - e1006431 EP - e1006431 JF - PLoS pathogens JO - PLoS Pathog. VL - 13 IS - 7 N2 - 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. SN - 1553-7374 UR - https://www.unboundmedicine.com/medline/citation/28683136/Generality_of_toxins_in_defensive_symbiosis:_Ribosome_inactivating_proteins_and_defense_against_parasitic_wasps_in_Drosophila_ L2 - http://dx.plos.org/10.1371/journal.ppat.1006431 DB - PRIME DP - Unbound Medicine ER -