The Olive Fly Endosymbiont, “CandidatusErwinia dacicola,” Switches from an Intracellular Existence to an Extracellular Existence during Host Insect Development

Abstract

As polyphagous, holometabolous insects, tephritid fruit flies (Diptera: Tephritidae) provide a unique habitat for endosymbiotic bacteria, especially those microbes associated with the digestive system. Here we examine the endosymbiont of the olive fly [Bactrocera oleae (Rossi) (Diptera: Tephritidae)], a tephritid of great economic importance. "Candidatus Erwinia dacicola" was found in the digestive systems of all life stages of wild olive flies from the southwestern United States. PCR and microscopy demonstrated that "Ca. Erwinia dacicola" resided intracellularly in the gastric ceca of the larval midgut but extracellularly in the lumen of the foregut and ovipositor diverticulum of adult flies. "Ca. Erwinia dacicola" is one of the few nonpathogenic endosymbionts that transitions between intracellular and extracellular lifestyles during specific stages of the host's life cycle. Another unique feature of the olive fly endosymbiont is that unlike obligate endosymbionts of monophagous insects, "Ca. Erwinia dacicola" has a G؉C nucleotide composition similar to those of closely related plantpathogenic and free-living bacteria. These two characteristics of "Ca. Erwinia dacicola," the ability to transition between intracellular and extracellular lifestyles and a G؉C nucleotide composition similar to those of free-living relatives, may facilitate survival in a changing environment during the development of a polyphagous, holometabolous host. We propose that insect-bacterial symbioses should be classified based on the environment that the host provides to the endosymbiont (the endosymbiont environment).

Experimental Manipulation Shows a Greater Influence of Population than Dietary Perturbation on the Microbiome of Tyrophagus putrescentiae

“…Previously, we observed sequences with 99% similarity to Xenorhabdus cabanillasii among clones from L. destructor and A. siro (10), whereas sequences similar to those of Erwinia bacteria comprised the majority of the microbiome of Blomia tropicalis (9). "Candidatus Erwinia dacicola" resides intracellularly in the gastric ceca of the larval midgut but extracellularly in the lumen of the foregut and the ovipositor diverticulum in adult flies (27). Moran et al (28) described three symbiotic Enterobacteriaceae species, "Candidatus Serratia symbiotica," "Candidatus Hamiltonella defensa," and "Candidatus Regiella insecticola," as sister groups to one another; moreover, they revealed a relationship to a species of Photorhabdus.…”

Characterization of an Obligate Intracellular Bacterium in the Midgut Epithelium of the Bulrush Bug Chilacis typhae (Heteroptera, Lygaeidae, Artheneinae)

“…Another relationship of Erwinia-related symbiotic bacteria was described in fruit flies (Diptera: Tephritidae). Here, the bacteria reside intracellularly in the epithelial cells of digestive tissue in larval stages, as in Chilacis, but also extracellularly in the midgut lumen between the peritrophic tube and the midgut epithelium in adults (15,42). In the olive fly Bactrocera oleae the symbionts were additionally localized in a special cephalic organ (esophageal bulb or pharyngeal bulb) connected to the pharynx (9,10).…”

Evidence of two lineages of the symbiont ‘Candidatus Erwinia dacicola’ in Italian populations of Bactrocera oleae (Rossi) based on 16S rRNA gene sequences

“…The lack of an association between the symbiont and host lineages could be at least partly explained assuming the horizontal transfer of the symbiont. Even though Estes et al (2009) have recently hypothesized an intracellular existence for 'Ca. E. dacicola' at the larval stage, the olive fly symbiont can, at present, according to Petri (1909), be considered to be extracellular.…”