Manipulation of Gut Symbionts for Improving the Sterile Insect Technique: Quality Parameters of <i>Bactrocera dorsalis</i> (Diptera: Tephritidae) Genetic Sexing Strain Males After Feeding on Bacteria-Enriched Diets

Zhang, Qiwen; Cai, Pumo; Wang, Bo; Liu, Xuxiang; Lin, Jia; Hua, Ruohan; Zhang, Hehe; Yi, Chen; Song, Xuesen; Ji, Qinge; Yang, Jing; CHEN, SHI

doi:10.1093/jee/toaa294

Cited by 14 publications

(7 citation statements)

References 72 publications

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“…longicaudata , so it was perhaps transferred from the parasitoid female into the host larvae during parasitization. Morganella morganii is an opportunistic bacterium linked to pathogenicity in tephritids [ 60 , 61 ] and may have an immune-suppressing function in B . dorsalis .…”

Section: Discussionmentioning

confidence: 99%

Shaping the Microbial Landscape: Parasitoid-Driven Modifications of Bactrocera dorsalis Microbiota

Gwokyalya,

Herren,

Weldon

et al. 2024

Microb Ecol

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Koinobiont endoparasitoids regulate the physiology of their hosts through altering host immuno-metabolic responses, processes which function in tandem to shape the composition of the microbiota of these hosts. Here, we employed 16S rRNA and ITS amplicon sequencing to investigate whether parasitization by the parasitoid wasps, Diachasmimorpha longicaudata (Ashmaed) (Hymenoptera: Braconidae) and Psyttalia cosyrae (Wilkinson) (Hymenoptera: Braconidae), induces gut dysbiosis and differentially alter the gut microbial (bacteria and fungi) communities of an important horticultural pest, Bactrocera dorsalis (Hendel) (Diptera: Tephritidae). We further investigated the composition of bacterial communities of adult D. longicaudata and P. cosyrae to ascertain whether the adult parasitoids and parasitized host larvae share microbial taxa through transmission. We demonstrated that parasitism by D. longicaudata induced significant gut perturbations, resulting in the colonization and increased relative abundance of pathogenic gut bacteria. Some pathogenic bacteria like Stenotrophomonas and Morganella were detected in both the guts of D. longicaudata-parasitized B. dorsalis larvae and adult D. longicaudata wasps, suggesting a horizontal transfer of microbes from the parasitoid to the host. The bacterial community of P. cosyrae adult wasps was dominated by Arsenophonus nasoniae, whereas that of D. longicaudata adults was dominated by Paucibater spp. and Pseudomonas spp. Parasitization by either parasitoid wasp was associated with an overall reduction in fungal diversity and evenness. These findings indicate that unlike P. cosyrae which is avirulent to B. dorsalis, parasitization by D. longicaudata induces shifts in the gut bacteriome of B. dorsalis larvae to a pathobiont-dominated community. This mechanism possibly enhances its virulence against the pest, further supporting its candidacy as an effective biocontrol agent of this frugivorous tephritid fruit fly pest.

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Section: Discussionmentioning

confidence: 99%

Shaping the Microbial Landscape: Parasitoid-Driven Modifications of Bactrocera dorsalis Microbiota

Gwokyalya,

Herren,

Weldon

et al. 2024

Microb Ecol

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“…Providencia and Morganella are widespread in the gut of Bactrocera sp. (Gujjar et al, 2017;Rashid et al, 2018;Zhang et al, 2021). Two genera of Enterobacteriaceae, Providencia and Morganella, were stably present in different host populations with high relative abundances.…”

Section: Discussionmentioning

confidence: 99%

Effect of host shift on the gut microbes of Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae)

Tian,

Chen,

Chen

et al. 2023

Front. Microbiol.

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BackgroundGut microbes play an important role in the adaptation of insects. Polyphagous insects usually undergo changes in gut microbiota after host shift. The Bactrocera cucurbitae have a wide range of hosts, but the dynamic of gut microorganisms during host shift have not been thoroughly investigated. To understand the role of gut microbes in insect adaptation, it is necessary to study the dynamics of insect gut microorganisms during host transfer.MethodsUsing Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae) and its four hosts as study subjects, we investigated the dynamics of gut microbes during host transfer and the effects of different hosts on the gut microbial composition of B. cucurbitae.ResultsThe results showed that the Chao1 index of B. cucurbitae decreased significantly during host transfer, and the intestinal microorganisms were significantly affected by the original host, host, and generations. Furthermore, predicated changes in the abundance of secondary metabolite pathways after host transfer suggested that microorganisms may play an important role in the degradation of secondary metabolites, among which Providencia and Morganella have important functions in the gut of B. cucurbitae.ConclusionThis implied that microorganisms play a function in the host transfer process of B. cucurbitae and may be an important cofactor in the adaptation of B. cucurbitae to different hosts and environments, providing new research ideas for the future control of B. cucurbitae.

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“…In addition to the members of the Enterobactericeae family, Enterococcus sp. ( Enterococcaceae ) was also reported to be a beneficial species for B. dorsalis GSS populations, where the flies fed on diets enriched with this bacterium had a reduced larval developmental duration and higher pupal weight and percentage of survival (Khaeso et al, 2018 ; Zhang et al, 2021 ). Correspondently, Enterococcus were broadly present mainly in teneral and adults of Vienna 8 FD-GSS population across all the generations, while they were acquired at F7 in larval stage.…”

Section: Discussionmentioning

confidence: 99%

Dynamics of the Gut Bacteriome During a Laboratory Adaptation Process of the Mediterranean Fruit Fly, Ceratitis capitata

Mokhtar

Catalá-Oltra²,

Stathopoulou

et al. 2022

Front. Microbiol.

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Laboratory adaptation process used in sterile insect technique (SIT) programs can exert a significant impact on the insect-gut microbiome relationship, which may negatively impact the quality and performance of the fly. In the present study, changes in the gut microbiota that occur through laboratory adaptation of two Ceratitis capitata populations were investigated: Vienna 8 genetic sexing strain (GSS), a long-established control line, and a wild population recently introduced to laboratory conditions. The bacterial profiles were studied for both strains using amplicon sequencing of the 16S rRNA V3-V4 hypervariable region in larvae and in the gastrointestinal tract of teneral (1 day) and adults (5 and 15 days) reared under laboratory conditions for 14 generations (F0–F13). Findings demonstrated the development of distinct bacterial communities across the generations with differences in the bacterial composition, suggesting a strong impact of laboratory adaptation on the fly bacteriome. Moreover, different bacterial profiles were observed between wild and Vienna 8 FD-GSS displaying different patterns between the developmental stages. Proteobacteria, mainly members of the Enterobacteriaceae family, represented the major component of the bacterial community followed by Firmicutes (mainly in Vienna 8 FD-GSS adults) and Chlamydiae. The distribution of these communities is dynamic across the generations and seems to be strain- and age-specific. In the Vienna 8 FD-GSS population, Providencia exhibited high relative abundance in the first three generations and decreased significantly later, while Klebsiella was relatively stable. In the wild population, Klebsiella was dominant across most of the generations, indicating that the wild population was more resistant to artificial rearing conditions compared with the Vienna 8 FD-GSS colony. Analysis of the core bacteriome revealed the presence of nine shared taxa between most of the examined medfly samples including Klebsiella, Providencia, Pantoea, and Pseudomonas. In addition, the operational taxonomic unit co-occurrence and mutual exclusion networks of the wild population indicated that most of the interactions were classified as co-presence, while in the Vienna 8 FD-GSS population, the number of mutual exclusions and co-presence interactions was equally distributed. Obtained results provided a thorough study of the dynamics of gut-associated bacteria during the laboratory adaptation of different Ceratitis capitata populations, serving as guidance for the design of colonization protocols, improving the effectiveness of artificial rearing and the SIT application.

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Manipulation of Gut Symbionts for Improving the Sterile Insect Technique: Quality Parameters of Bactrocera dorsalis (Diptera: Tephritidae) Genetic Sexing Strain Males After Feeding on Bacteria-Enriched Diets

Cited by 14 publications

References 72 publications

Shaping the Microbial Landscape: Parasitoid-Driven Modifications of Bactrocera dorsalis Microbiota

Shaping the Microbial Landscape: Parasitoid-Driven Modifications of Bactrocera dorsalis Microbiota

Effect of host shift on the gut microbes of Bactrocera cucurbitae (Coquillett) (Diptera: Tephritidae)

Dynamics of the Gut Bacteriome During a Laboratory Adaptation Process of the Mediterranean Fruit Fly, Ceratitis capitata

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