Abstract
Several insect taxa are associated with intracellular symbionts that provision limiting nutrients to their hosts. Such tightly integrated symbioses are especially common in insects feeding on nutritionally challenging diets like phloem sap or vertebrate blood, but also occur in seed-eating and omnivorous taxa. Here, we characterize an intracellular symbiosis in pollen-feeding beetles of the genus Dasytes (Coleoptera, Dasytidae). High-throughput tag-encoded 16S amplicon pyrosequencing of adult D. plumbeus and D. virens revealed a single gamma-proteobacterial symbiont (‘Candidatus Dasytiphilus stammeri’) that amounts to 52.4–98.7% of the adult beetles’ entire microbial community. Almost complete 16S rRNA sequences phylogenetically placed the symbiont into a clade comprising Buchnera and other insect endosymbionts, but sequence similarities to these closest relatives were surprisingly low (83.4–87.4%). Using histological examination, three-dimensional reconstructions, and fluorescence in situ hybridization, we localized the symbionts in three mulberry-shaped bacteriomes that are associated with the mid- to hind-gut transition in adult male and female beetles. Given the specialized pollen-feeding habits of the adults that contrasts with the larvae’s carnivorous lifestyle, the symbionts may provision limiting essential amino acids or vitamins as in other intracellular symbioses, or they might produce digestive enzymes that break up the fastidious pollen walls and thereby contribute to the host’s nutrition. In either case, the presence of gamma-proteobacterial symbionts in pollen-feeding beetles indicates that intracellular mutualists are more widely distributed across insects with diverse feeding habits than previously recognized.
Highlights
Many insects are associated with mutualistic microbes that represent major sources of evolutionary innovation by conveying novel ecological traits to their hosts (Douglas, 2009; Feldhaar, 2011; McFall-Ngai et al, 2013)
Samples of both species consistently yielded gamma-proteobacterial sequences that were related to other intracellular symbionts in insects
Phylogenetic analyses using almost complete 16S rRNA gene sequences placed the symbionts of D. plumbeus and D. virens in a monophyletic clade most closely related to ‘Candidatus Annandia pinicola,’ ‘Candidatus Purcelliella pentastirinorum,’ and ‘Candidatus Buchnera aphidicola,’ the intracellular symbionts of adelgids, fulgoroid planthoppers, and aphids, respectively (Figure 1)
Summary
Many insects are associated with mutualistic microbes that represent major sources of evolutionary innovation by conveying novel ecological traits to their hosts (Douglas, 2009; Feldhaar, 2011; McFall-Ngai et al, 2013). Intracellular Symbionts in Pollen-Feeding Beetles plants (Tsuchida et al, 2004; Hosokawa et al, 2007), by allowing the insect host to specialize on nutritional resources that would otherwise be inaccessible, e.g., phloem or xylem sap or wood (Moran, 2007). A particular feature of many obligate insect-associated symbionts is the intracellular localization within specialized organs, the so-called bacteriomes. Such structures occur across at least six different insect orders (Hemiptera, Dictyoptera, Coleoptera, Diptera, Hymenoptera, and Phthiraptera; Douglas, 1989), mostly in taxa with nutritionally challenging diets (Buchner, 1965). A defensive function has recently been described for a bacteriome-localized mutualist (Nakabachi et al, 2013), such symbionts usually supplement limiting nutrients to the host (essential amino acids, B-vitamins). Even though extracellular gut bacteria appear to be predisposed toward involvement in digestion and detoxification, contributions from bacteriome-associated primary mutualists are conceivable
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