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

Abstract

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.

Gut bacterial population and community dynamics following adult emergence in pest tephritid fruit flies

“…Klebsiella and other Enterobacteriaceae are often detected in sequencing and culturing efforts of tephritid fruit fly pests 21 , 41 , 46 , 56 , 57 , 59 , 60 , but how they are retained between lifestages, fluctuate in abundance relative to other microbial taxa, exhibit taxonomic and functional resiliency, and vary between insect populations and across timepoints are not well-resolved. Specifically, the amount of variation in specific isolates and strains, and how that might impact fly performance is unknown.…”

“…As is the case with many holometabolous insects, tephritids consume divergent diets as adults and larvae, and their gut microbiomes can reflect these substantial changes 6 , 19 . Understanding the establishment and flexibility of gut microbiome dynamics would help inform sources of variation that are often observed in natural populations of males 20 as well as how host-microbe respond to different environments 21 . Additionally, while determining microbial dynamics of flies in natural settings can uncover fundamental physiological functioning, elucidating how microbial establishment occurs in insectary-maintained populations is especially important for tephritid fruit flies.…”

Effect of Wolbachia Infection and Adult Food on the Sexual Signaling of Males of the Mediterranean Fruit Fly Ceratitis capitata

“…Similarly, Ben Yosef and colleagues (2008) reported that antibiotic-treated males needed longer time to achieve mating compared to the untreated ones [ 145 ]. Several studies have also demonstrated the dominance and stability of Klebsiella abundance across different wild populations and laboratory strains of medfly [ 146 , 147 , 148 ] and the presence of genes in Klebsiella genome that play a potential role in the acquisition and metabolism of nutrients that are vital for insect fitness and reproductive success [ 148 ]. Therefore, Wolbachia might have an impact on nutrient utilization either by directly affecting metabolic functions of its host or through the perturbation of the host symbiotic microbiota, and this impact might lead to changes in the sexual behavior and performance of the host.…”

Probiotics as a Beneficial Modulator of Gut Microbiota and Environmental Stress for Sustainable Mass-Reared Ceratitis capitata

“…As a result, dysbiosis of the gut microbiota has recently emerged as the cause of the sterile medfly males' low fitness. Indeed, these males face a variety of constraints during mass-rearing, treatment with ionizing radiation, and release conditions that favor minor bacterial genera such as Providencia and Pseudomonas, which are considered potential pathogens for the fly [16,20]. The reduced fitness of released sterile males usually means that they are less competitive [21][22][23].…”