Symbiont-mediated fly survival is independent of defensive symbiont genotype in the <i>Drosophila melanogaster-Spiroplasma</i>-wasp interaction

Jones, Jordan Elouise; Hurst, Gregory D. D.

doi:10.1101/2020.07.05.154906

Cited by 4 publications

(8 citation statements)

References 44 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Thus, the higher RIP2 copy numbers detected in MSRO-Br could reflect a higher number of chromosomal copies, or a higher abundance of extrachromosomal copies, which could be condition-dependent. If RIP2 gene copy numbers differ between MSRO-Br and MSRO-Ug, they could be related to the higher degree of overall protection against certain wasps reported for MSRO-Br (Jones and Hurst 2020).…”

Section: Discussionmentioning

confidence: 99%

Preliminary Characterization of Phage-like Particles from the Male-Killing MollicuteSpiroplasma poulsonii(an Endosymbiont ofDrosophila)

Ramirez

Leavitt

Gill

et al. 2021

Preprint

View full text Add to dashboard Cite

Viruses are vastly abundant and influential in all ecosystems, and are generally regarded as pathogens. Viruses of prokaryotes (themselves highly diverse and abundant) are known as bacteriophages or phages. Phages engage in diverse associations with their hosts, and contribute to regulation of biogeochemical processes, horizontal movement of genes, and control of bacterial populations. Recent studies have revealed the influential role of phage in the association of arthropods and their heritable endosymbiotic bacteria (e.g. the Proteobacteria genera Wolbachia and Hamiltonella). Despite prior studies (~30 years ago) documenting presence of phage in the mollicute Spiroplasma infecting Drosophila, genomic sequences of such phage are lacking, and their effects on the Spiroplasma-Drosophila interaction have not been comprehensively characterized. The present work isolated phage-like particles from the male-killing Spiroplasma poulsonii (strains NSRO and MSRO-Br) harbored by Drosophila melanogaster. Isolated particles were subjected to DNA sequencing, assembly, and annotation. Our results recovered three ~19 kb phage-like contigs (two in NSRO and one in MSRO-Br), and two smaller non-phage-like contigs encoding a known Spiroplasma toxin and an insertion element. Whole or parts of the particle-derived contigs were found in the genome assemblies of members of the Spiroplasma poulsonii clade. Although our results do not allow us to distinguish whether the contigs obtained represent infective phage-like particles capable of transmitting their DNA to new hosts, their encoding of several typical phage genes suggests that they are at least remnants of functional phage. We discuss potential implications of our findings and suggest future directions.

show abstract

Section: Discussionmentioning

confidence: 99%

Preliminary Characterization of Phage-like Particles from the Male-Killing MollicuteSpiroplasma poulsonii(an Endosymbiont ofDrosophila)

Ramirez

Leavitt

Gill

et al. 2021

Preprint

View full text Add to dashboard Cite

show abstract

“…Experimental over-expression of these, and the Group 2 “restored” genes, in the absence of Spiroplasma , could be used to test whether they influence the outcome of parasitism by L. heterotoma and other wasps, including those against which s Mel confers stronger rescue (e.g. L. boulardi or L. victoriae ; Mateos et al, 2016; Paredes et al, 2016; Jones and Hurst, 2020a)…”

Section: Discussionmentioning

confidence: 99%

“…Herein, we used an RNA-seq approach to evaluate the transcriptomic response of D. melanogaster during interactions involving Spiroplasma and two wasps that are generalists of the genus Drosophila : the Spiroplasma -susceptible L. heterotoma ; and the Spiroplasma -resistant Ganaspis hookeri . In addition, we evaluated the effect of wasp parasitism on the expression of Spiroplasma RIP genes in two closely related substrains of s Mel, which have similar genomes (Gerth et al, 2020) but confer different levels of protection against wasps, measured as fecundity of flies surviving a wasp attack (Jones and Hurst, 2020a).…”

Section: Introductionmentioning

confidence: 99%

Transcriptomic response during wasp parasitism in theDrosophila-Spiroplasmainteraction

Higareda‐Alvear¹,

Mateos²,

Cortez³

et al. 2020

Preprint

View full text Add to dashboard Cite

Several facultative bacterial symbionts of insects protect their hosts against natural enemies. Spiroplasma poulsonii strain sMel, a male-killing heritable symbiont of Drosophila melanogaster, confers protection against some species of parasitic wasps. Several lines of evidence suggest that Spiroplasma-encoded ribosome inactivating proteins (RIPs) are involved in the protection mechanism, but the potential contribution of the fly-encoded functions has not been deeply explored. Here we used RNA-seq to evaluate the response of D. melanogaster to infection by Spiroplasma and parasitism by the Spiroplasma-susceptible wasp Leptopilina heterotoma, and the Spiroplasma-resistant wasp Ganaspis hookeri. In the absence of Spiroplasma infection, we found evidence of Drosophila immune activation by G. hookeri, but not by L. heterotoma, which in turn negatively influenced functions associated with male gonad development. As expected for a symbiont that kills males, we detected extensive downregulation in the Spiroplasma-infected treatments of genes known to have male-biased expression. We detected very few genes whose expression was influenced by the Spiroplasma-L. heterotoma interaction, and they do not appear to be related to immune response. For most of them, parasitism by L. heterotoma (in the absence of Spiroplasma) caused an expression change that was at least partly reversed when Spiroplasma was also present. It is unclear whether such genes are involved in the Spiroplasma-mediated mechanism that leads to wasp death or fly rescue. Nonetheless, the expression pattern of some of these genes, which reportedly undergo expression shifts during the larva-to-pupa transition, is suggestive of an influence of Spiroplasma on the development time of L. heterotoma-parasitized flies. In addition, we used the RNAseq data and quantitative (q)PCR to evaluate the transcript levels of the Spiroplasma-encoded RIP genes. One of the five RIP genes (RIP2) was consistently highly expressed independently of wasp parasitism, in two substrains of sMel. Finally, the RNAseq data revealed evidence consistent with RIP-induced damage in the ribosomal (r)RNA of the Spiroplasma-susceptible, but not the Spiroplasma-resistant, wasp. We conclude that immune priming is unlikely to contribute to the Spiroplasma-mediated protection against wasps, and that the mechanism by which G. hookeri resists/tolerates Spiroplasma does not involve inhibition of RIP transcription.

show abstract

“…Experiments used the MSRO-Ug strain Spiroplasma strain originally collected from Namulonge, Uganda in 2005 (Pool et al ., 2006); this strain was transinfected onto a Canton-S background in 2020 (Jones and Hurst, 2020b). MSRO-Ug Canton-S stocks and Canton-S stocks lacking Spiroplasma were maintained on corn meal agar (10 g agarose, 85 g sugar, 60 g maize meal, 40 g autolysed yeast in a total volume of 1 L, to which 25 mL 10% Nipagin dissolved in 100% ethanol was added) at 25°C on a 12:12 light:dark cycle.…”

Section: Methodsmentioning

confidence: 99%

“…Spiroplasma is a facultative symbiont of Drosophila and has been shown to protect against parasitoid wasps and nematodes (Xie et al ., 2010; Jaenike et al ., 2010), and the strain in D. melanogaster combines protection phenotype with male-killing. Previous studies on this system have concluded that the strain of wasp and Spiroplasma are all important components for the outcome of Spiroplasma -mediated protection (Jones and Hurst, 2020a; Jones and Hurst, 2020b). Whilst influence of temperature on the protective phenotype have not been established, vertical transmission of Spiroplasma in D. melanogaster fails at 16.5°C, indicating cool sensitivity of the symbiosis (Montenegro and Klaczko, 2004).…”

Section: Introductionmentioning

confidence: 99%

History matters: thermal environment before, but not during wasp attack determines the efficiency of symbiont-mediated protection

Jones

Hurst

2022

Preprint

Self Cite

View full text Add to dashboard Cite

The outcome of natural enemy attack in insects is commonly impacted by the presence of defensive microbial symbionts residing within the host. Beyond their presence, the outcome of the interaction can also depend on genetic and environmental factors. The thermal environment is a key factor known to affect symbiont-mediated traits in insects, including their ability to defend against natural enemy attack. Cooler temperatures, for instance, have been previously shown to reduce Spiroplasma-mediated protection in Drosophila. Here, we dissect the effect of the thermal environment on Spiroplasma-mediated protection against Leptopilina boulardi in Drosophila melanogaster by examining the effect of temperature before, during and after wasp attack on fly survival and wasp success. We observed that the developmental temperature of the mothers' of attacked larvae, and not the temperature of the attacked larvae themselves during or after wasp attack, strongly determines the protective influence of Spiroplasma. Spiroplasma-mediated fly survival was found to be weaker when parental flies were reared at 21 C before their larvae were exposed to wasps compared to larvae derived from parental flies reared at 23 C or 25 C. Contrastingly, there was no effect of thermal environment on protection when mothers were reared at 25 C, and their progeny exposed to lower temperatures during and after wasp attack. The effect of developmental temperature on Spiroplasma-mediated protection is likely mediated by reduced Spiroplasma titre combined, at cooler temperatures, with segregation of infection. These results indicate the historical thermal environment is a stronger determinant of protection than current environment, and that protective capacity is partly an epigenetic trait.

show abstract

Symbiont-mediated fly survival is independent of defensive symbiont genotype in the Drosophila melanogaster-Spiroplasma-wasp interaction

Cited by 4 publications

References 44 publications

Preliminary Characterization of Phage-like Particles from the Male-Killing MollicuteSpiroplasma poulsonii(an Endosymbiont ofDrosophila)

Preliminary Characterization of Phage-like Particles from the Male-Killing MollicuteSpiroplasma poulsonii(an Endosymbiont ofDrosophila)

Transcriptomic response during wasp parasitism in theDrosophila-Spiroplasmainteraction

History matters: thermal environment before, but not during wasp attack determines the efficiency of symbiont-mediated protection

Contact Info

Product

Resources

About