The Symbiotic Organ of <i>Xyleborus</i> Ambrosia Beetles: Cell Structure of the Preoral Mycangia Housing Partner Symbiotic Microbes

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Abstract

Ambrosia beetles have evolved specialized structures termed &ldquo;mycangia&rdquo;, which are used to house and transport partner symbiotic microbes. Microbial partners include at least one obligate mutualistic filamentous fungus used as food for larvae and adults and potentially secondary filamentous fungi, yeasts, and bacteria, although the roles of these secondary partners remain poorly understood. Beetles in the genus Xyleborus possess a set of two pre-oral mycangial structures located within the head on either side of the mouth parts/mandibles. These mycangia develop in pupae, with newly emerged adults acquiring partners from the environment. However, information concerning the cellular structure and function of the Xyleborus mycangia remains limited. We show that the mycangia are lined with a thick layer of striated dense material, followed by layers of insect epithelial cells, with different types of spine-like structures directed into the mycangia. Larger (5-10 mm) Ross projections were concentrated within and near the entrance of the mycangia, with smaller tubules and filaments (4-8 mm) within the mycangia itself. In addition, rows of &ldquo;eyelash&rdquo; structures were seen lining the inside of mycangia, with the fungal cells apparently free-floating within the mycangial enclosure or in close association with projections. Serial sections revealed nearby mandible articulations, eyes and antennae, and mandibular, pharyngeal, and labial muscles, along with the mycangial entry/exit channel leading into the pre-oral cavity. Sheets of comb-like large spines at the mycangial entrance and opposite the mycangia attached to the roof of the labrum or epipharynx were noted that may serve as an interlocking mechanism for opening/closing the mycangia and for guiding fungal cells into entry/exit channels. In addition, mandibular fibra (muscle tissue) potentially enervating and affecting the mechanism of mycangial functioning, i.e., acting to fill/empty the mycangia were noted. These data support the hypothesis that the twin pre-oral mycangia in Xyleborus beetles are dynamic organs with evolved specialized cellular structures that mediate their function in housing and dispensing partner microbial symbionts.

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