Metagenome-Assembled Genomes of Bacterial Symbionts Associated with Insecticide-Resistant and -Susceptible Individuals of the Glassy-Winged Sharpshooter (Homalodisca vitripennis)

Ettinger, Cassandra L.; Byrne, Frank J.; Redak, Richard A.; Stajich, Jason E.

doi:10.1128/mra.00506-22

“…However, starting in 2012 the effectiveness of population control by these insecticides appeared substantially weakened ( 19 , 20 ), with documented instances of neonicotinoid applications leading to high levels of insecticide resistance in some Southern California populations resulting in GWSS population resurgence ( 21 , 22 ). Insecticide resistance usually involves multiple coexisting mechanisms spanning behavioral (e.g., avoidance) and physiological processes (e.g., cuticle modifications and detoxification) ( 23 – 25 ), and studies have proposed a novel role for symbionts and other associated microbes in detoxification of insecticides for their associated hosts ( 26 – 31 ). Recent studies on Southern California GWSS populations have identified both trade-offs in host reproductive fitness associated with resistance ( 32 ) as well as host genes that may play a role in conferring resistance ( 33 ).…”

Section: Introductionmentioning

confidence: 99%

Geographical survey of the mycobiome and microbiome of Southern California glassy-winged sharpshooters

Ettinger,

Wu-Woods,

Kurbessoian

et al. 2023

mSphere

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The glassy-winged sharpshooter, Homalodisca vitripennis Germar, is an invasive xylem-feeding leafhopper with a devastating economic impact on California agriculture through transmission of the plant pathogen, Xylella fastidiosa . While studies have focused on X. fastidiosa or known symbionts of H. vitripennis , little work has been done at the scale of the microbiome (the bacterial community) or mycobiome (the fungal community). Here, we characterize the mycobiome and the microbiome of H. vitripennis across Southern California and explore correlations with captivity and host insecticide resistance status. Using high-throughput sequencing of the ribosomal internal transcribed spacer 1 region and the 16S rRNA gene to profile the mycobiome and microbiome, respectively, we found that while the H. vitripennis mycobiome significantly varied across Southern California, the microbiome did not. We also observed a significant difference in both the mycobiome and microbiome between captive and wild H. vitripennis . Finally, we found that the mycobiome, but not the microbiome, was correlated with insecticide resistance status in wild H. vitripennis . This study serves as a foundational look at the H. vitripennis mycobiome and microbiome across Southern California. Future work should explore the putative link between microbes and insecticide resistance status and investigate whether microbial communities should be considered in H. vitripennis management practices. IMPORTANCE The glassy-winged sharpshooter is an invasive leafhopper that feeds on the xylem of plants and transmits the devastating pathogen, Xylella fastidiosa , resulting in significant economic damage to California’s agricultural system. While studies have focused on this pathogen or obligate symbionts of the glassy-winged sharpshooter, there is limited knowledge of the bacterial and fungal communities that make up its microbiome and mycobiome. To address this knowledge gap, we explored the composition of the mycobiome and the microbiome of the glassy-winged sharpshooter across Southern California and identified differences associated with geography, captivity, and host insecticide resistance status. Understanding sources of variation in the microbial communities associated with the glassy-winged sharpshooter is an important consideration for developing management strategies to control this invasive insect. This study is a first step toward understanding the role microbes may play in the glassy-winged sharpshooter’s resistance to insecticides.

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“…Additionally, future studies should also consider whether obligate and facultative microbial symbionts of GWSS are involved in conferring insecticide resistance (e.g. [ 61 ]). We believe that this work serves as a foundation for future studies of insecticide resistance in GWSS and other Hemipteran insects.…”

Section: Discussionmentioning

confidence: 99%

Transcriptome and population structure of glassy-winged sharpshooters (Homalodisca vitripennis) with varying insecticide resistance in southern California

Ettinger

¹

,

Byrne

²

,

Pacheco

³

et al. 2022

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Background Homalodisca vitripennis Germar, the glassy-winged sharpshooter, is an invasive insect in California and a critical threat to agriculture through its transmission of the plant pathogen, Xylella fastidiosa. Quarantine, broad-spectrum insecticides, and biological control have been used for population management of H. vitripennis since its invasion and subsequent proliferation throughout California. Recently wide-spread neonicotinoid resistance has been detected in populations of H. vitripennis in the southern portions of California’s Central Valley. In order to better understand potential mechanisms of H. vitripennis neonicotinoid resistance, we performed RNA sequencing on wild-caught insecticide-resistant and relatively susceptible sharpshooters to profile their transcriptome and population structure. Results We identified 81 differentially expressed genes with higher expression in resistant individuals. The significant largest differentially expressed candidate gene linked to resistance status was a cytochrome P450 gene with similarity to CYP6A9. Furthermore, we observed an over-enrichment of GO terms representing functions supportive of roles in resistance mechanisms (cytochrome P450s, M13 peptidases, and cuticle structural proteins). Finally, we saw no evidence of broad-scale population structure, perhaps due to H. vitripennis' relatively recent introduction to California or due to the relatively small geographic scale investigated here. Conclusions In this work, we characterized the transcriptome of insecticide-resistant and susceptible H. vitripennis and identified candidate genes that may be involved in resistance mechanisms for this species. Future work should seek to build on the transcriptome profiling performed here to confirm the role of the identified genes, particularly the cytochrome P450, in resistance in H. vitripennis. We hope this work helps aid future population management strategies for this and other species with growing insecticide resistance.

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“…avoidance) and physiological processes (e.g. cuticle modifications, detoxification) [23][24][25], and studies have proposed a novel role for symbionts and other associated microbes in detoxification of insecticides for their associated hosts [26][27][28][29][30][31]. Recent studies on Southern California GWSS populations have identified both trade-offs in host reproductive fitness associated with resistance [32] as well as host genes that may play a role in conferring resistance [33].…”

Section: Introductionmentioning

confidence: 99%

Geographical Survey of the Mycobiome and Microbiome of Southern California Glassy-winged Sharpshooters

Ettinger

¹

,

Wu-Woods

²

,

Kurbessoian

³

et al. 2023

Preprint

Self Cite

0

View full text Add to dashboard Cite

The glassy-winged sharpshooter, Homalodisca vitripennis Germar, is an invasive xylem-feeding leafhopper with a devastating economic impact on California agriculture through transmission of the plant pathogen, Xylella fastidiosa. While studies have focused on X. fastidiosa or known symbionts of H. vitripennis, little work has been done at the scale of the microbiome (the bacterial community) or mycobiome (the fungal community). Here we characterize the mycobiome and the microbiome of H. vitripennis across Southern California and explore correlations with captivity and host insecticide-resistance status. Using high-throughput sequencing of the ribosomal internal transcribed spacer (ITS1) region and the 16S rRNA gene to profile the mycobiome and microbiome, respectively, we found that while the H. vitripennis mycobiome significantly varied across Southern California, the microbiome did not. We also observed a significant difference in both the mycobiome and microbiome between captive and wild H. vitripennis. Finally, we found that the mycobiome, but not the microbiome, was correlated with insecticide-resistance status in wild H. vitripennis. This study serves as a foundational look at the H. vitripennis mycobiome and microbiome across Southern California. Future work should explore the putative link between microbes and insecticide-resistance status and investigate whether microbial communities should be considered in H. vitripennis management practices.

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Metagenome-Assembled Genomes of Bacterial Symbionts Associated with Insecticide-Resistant and -Susceptible Individuals of the Glassy-Winged Sharpshooter (Homalodisca vitripennis)

Abstract: The role of microbes in insecticide resistance is an emerging question. Here, we describe six metagenome-assembled genomes (MAGs) associated with the glassy-winged sharpshooter ( Homalodisca vitripennis [Germar, 1821]) (Hemiptera, Cicadellidae).

Cited by 4 publications

References 32 publications

Geographical survey of the mycobiome and microbiome of Southern California glassy-winged sharpshooters

Geographical survey of the mycobiome and microbiome of Southern California glassy-winged sharpshooters

Transcriptome and population structure of glassy-winged sharpshooters (Homalodisca vitripennis) with varying insecticide resistance in southern California

Geographical Survey of the Mycobiome and Microbiome of Southern California Glassy-winged Sharpshooters

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