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Applied and Environmental Microbiology, November 2009, p. 7097-7106, Vol. 75, No. 22
0099-2240/09/$08.00+0     doi:10.1128/AEM.00778-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.

The Olive Fly Endosymbiont, "Candidatus Erwinia dacicola," Switches from an Intracellular Existence to an Extracellular Existence during Host Insect Development{triangledown} ,{dagger}

Anne M. Estes,1* David J. Hearn,1,§ Judith L. Bronstein,1 and Elizabeth A. Pierson2,{ddagger}

Department of Ecology and Evolutionary Biology,1 Division of Plant Pathology and Microbiology, Department of Plant Sciences, University of Arizona, Tucson, Arizona2

Received 6 April 2009/ Accepted 14 September 2009

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 plant-pathogenic 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).

* Corresponding author. Mailing address: Department of Ecology and Evolutionary Biology, University of Arizona, 310 BioSciences West, 1041 E. Lowell St., Tucson, AZ 85721. Phone: (520) 621-3792. Fax: (520) 621-9190. E-mail: anneestes{at}gmail.com

{triangledown} Published ahead of print on 18 September 2009.

{dagger} Supplemental material for this article may be found at http://www.aem.org/.

§ Present address: Department of Biological Sciences, Towson University, Smith Hall, 8000 York Rd., Baltimore, MD 21252.

{ddagger} Present address: Department of Horticultural Sciences, Texas A&M, College Station, TX 77843-2133.

Applied and Environmental Microbiology, November 2009, p. 7097-7106, Vol. 75, No. 22
0099-2240/09/$08.00+0     doi:10.1128/AEM.00778-09
Copyright © 2009, American Society for Microbiology. All Rights Reserved.





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