Acetic acid bacteria, newly emerging symbionts of insects

Abstract

Recent research in microbe-insect symbiosis has shown that acetic acid bacteria (AAB) establish symbiotic relationships with several insects of the orders Diptera, Hymenoptera, Hemiptera, and Homoptera, all relying on sugar-based diets, such as nectars, fruit sugars, or phloem sap. To date, the fruit flies Drosophila melanogaster and Bactrocera oleae, mosquitoes of the genera Anopheles and Aedes, the honey bee Apis mellifera, the leafhopper Scaphoideus titanus, and the mealybug Saccharicoccus sacchari have been found to be associated with the bacterial genera Acetobacter, Gluconacetobacter, Gluconobacter, Asaia, and Saccharibacter and the novel genus Commensalibacter. AAB establish symbiotic associations with the insect midgut, a niche characterized by the availability of diet-derived carbohydrates and oxygen and by an acidic pH, selective factors that support AAB growth. AAB have been shown to actively colonize different insect tissues and organs, such as the epithelia of male and female reproductive organs, the Malpighian tubules, and the salivary glands. This complex topology of the symbiosis indicates that AAB possess the keys for passing through body barriers, allowing them to migrate to different organs of the host. Recently, AAB involvement in the regulation of innate immune system homeostasis of Drosophila has been shown, indicating a functional role in host survival. All of these lines of evidence indicate that AAB can play different roles in insect biology, not being restricted to the feeding habit of the host. The close association of AAB and their insect hosts has been confirmed by the demonstration of multiple modes of transmission between individuals and to their progeny that include vertical and horizontal transmission routes, comprising a venereal one. Taken together, the data indicate that AAB represent novel secondary symbionts of insects.

FIG. 1.

(A) Asaia sp. colonizes the gut epithelium of Anopheles sp., Ae. aegypti, and S. titanus, establishing a specific association with the insect epithelium mediated by an extracellular polysaccharidic matrix that surrounds Asaia sp. cells. Bar, 3.4 μm. (B) Asaia sp. produces a thick pellicle when cultured in a glass tube without shaking for 10 days. (C) Asaia sp. has been found to be strictly associated with the surface of immature eggs in S. titanus and An. gambiae, as shown by FISH with Asaia sp.-specific fluorescent probes (Asaia sp.-specific probes for S. titanus are shown in yellow), suggesting egg-smearing transmission of Asaia sp. in its hosts. Bar, 400 μm.

FIG. 2.

Phylogenetic positions of insect-associated AAB among the most representative members of family Acetobacteraceae. The tree shown is based on bacterial 16S rRNA gene sequences. AAB recovered from insects are in bold. Shaded species belong to clusters including environmental AAB, as well as those recovered from insects. Values at nodes are percentages of bootstrap replications calculated from 2,000 replicate trees. Accession numbers of reference sequences are in parentheses. The species used as the outgroup belongs to the Gammaproteobacteria taxon. The scale bar represents 10% sequence divergence.