Community Structure of the Mediterranean Fruit Fly Microbiota: Seasonal and Spatial Sources of Variation

Abstract

Fruit flies (Diptera: Tephritidae) maintain diverse yet stable communities of Enterobacteriaceae that reside in their digestive system. Focusing on one species of this family, Ceratitis capitata, the Mediterranean fruit fly (medfly), we applied the PCR-DGGE approach to study the influence of temporal and spatial variations on the composition and diversity of the enterobacterial community associated with the medfly. Our results revealed that the Enterobacteriaceae constituted not only dominant, but also constant and stable populations in the medfly's gut. Nevertheless, changes in both time and space had an impact on the structure and diversity of these bacterial populations, and while some populations (e.g., Klebsiella spp.) were stable, others fluctuated. Whether the bacterial population fluctuated according to the ecological needs of the insect during different environmental conditions, or reflected opportunistic colonization abilities of some bacterial strains, remains to be determined.

Phylogenetic, Metabolic, and Taxonomic Diversities Shape Mediterranean Fruit Fly Microbiotas during Ontogeny

“…The phenotypic plasticity of the medfly's microbiota, as reflected in the variation of almost all phenotypic traits examined, may provide local adaptive advantages in changing environments, such as the extended array of fruits greatly varying in acidity and protein content in which it can feed and develop (53) and the different climates in which it is found (12). Whatever the environment, diazotrophy and pectinolysis may fill "core functions": they were found in almost all isolates, from all stages (92.6%), a figure nearly identical to that obtained from rotting fruits in a previous study (3), and are rendered essential for the maintenance of the holobiont by the medfly's diet, as they link carbon/energy sources to nitrogen acquisition in an insect that feeds on nitrogen-poor sources (9).…”

“…The very large majority of the symbionts composing this community is able to fix atmospheric nitrogen and to degrade pectin, thereby complementing the fly's nitrogen-deficient diet and possibly providing the necessary energy for nitrogenase activity (17). Nevertheless, alterations in the community structure occur within this functionally homogeneous population during ontogeny (3) and in response to seasonal or geographical changes (12). Despite these observations, albeit detailed, our knowledge of the dynamics of gut colonization during ontogeny is still fragmentary, lacking in both quantitative and qualitative information.…”

“…Butylene glycol fermentation (Voges-Proskauer [VP]) was determined by lysing cells in the remaining volume with 40% potassium hydroxide (Sigma-Aldrich) and reacting cytoplasmic contents with alpha naphthol amine (Sigma-Aldrich). All isolates were additionally streaked onto tryptic soy agar plates (Difco) and incubated at 10°C for 24 to 48 h. Diazotrophy (12) and pectinolysis (3)were detected on specific media as described previously by Behar et al…”

“…Previous explorations of the medfly's associated bacterial community revealed that the gut microbiota is dominated largely by free-living bacteria of the Enterobacteriaceae, notably by species of Enterobacter, Klebsiella, and Pectobacterium (3,(11)(12)(13)(14). These components of the bacterial community remain stable throughout the fly's life cycle and between geographical regions, and some are inherited vertically (3,12,(14)(15)(16).…”

“…These components of the bacterial community remain stable throughout the fly's life cycle and between geographical regions, and some are inherited vertically (3,12,(14)(15)(16). However, significant genotypic variation underlies this apparent taxonomic stability, as a large microdiversity of the 16S rRNA gene marker is observed at the strain level, and alterations in strain distribution are observed during ontogeny and between individuals (3,14).…”