Symbiotic streptomycetes in antennal glands of the South American digger wasp genus Trachypus (Hymenoptera, Crabronidae)

Abstract

Several insect taxa have evolved symbioses with actinobacteria that protect the host or its nutritional resources against pathogens. Digger wasps of the genus Philanthus (‘beewolves’; Hymenoptera, Crabronidae) cultivate ‘Candidatus Streptomyces philanthi’ (Ca. S. philanthi) in specialized antennal glands and transfer them to subterranean brood cells, where the symbionts provide protection for the beewolf larva against pathogens by producing a cocktail of antibiotic substances. The present study investigates the occurrence of antennal symbionts in two species of the genus Trachypus, which is the closest relative to Philanthus. Cross sections of the antennae from females of both Trachypus denticollis and Trachypus boharti reveal bacteria‐containing gland reservoirs that are morphologically very similar to those found in Philanthus spp. Polymerase chain reaction‐based screens with specific primers, sequencing of the partial 16S rRNA gene, and fluorescence in situ hybridization confirm the presence of close relatives of ‘Ca. S. philanthi’ in T. denticollis and T. boharti. However, 16S rRNA sequence divergence between Trachypus spp. and Philanthus spp. symbionts is much higher for T. boharti than for T. denticollis, suggesting that horizontal transmission and/or de novo uptake of symbionts from the environment occurs occasionally. The results obtained indicate that the protective symbiosis with antennal actinobacteria is older and more widespread than previously recognized and occurs in at least two genera of digger wasps that comprise approximately 170 species.

Refining the Roots of the Beewolf-Streptomyces Symbiosis: Antennal Symbionts in the Rare Genus Philanthinus (Hymenoptera, Crabronidae)

“…Streptomyces philanthi," a basal placement of the symbionts would have been expected under the assumption of an ancient infection event and subsequent codiversification of hosts and symbionts. Since this is not the case, the observed phylogenetic pattern is indicative of occasional horizontal transfer of symbionts as has been suggested earlier for the symbionts of Trachypus (17). It has to be noted, however, that the high similarities in 16S rRNA sequences among the symbionts severely limit the ability to draw conclusions on the evolutionary history of the symbiosis.…”

“…FISH was done with the "Ca. Streptomyces philanthi"-specific oligonucleotide probe Cy3-SPT177 (14,15) or the general eubacterial probe Cy3-EUB338 (2) as described previously (17). In both cases, the eubacterial probe FAM-EUB784 was used as a positive control, and the sections were counterstained with DAPI (4=,6-diamidino-2-phenylindole).…”

“…Subsequently, the primers fD1 and Spa-2R were used for amplification of about 2060 bp of the 16S rRNA gene, including parts of the 16S-23S intergenic spacer region (12,30). The amplicon was purified, and 1,490 bp were sequenced bidirectionally with primers fD1 and rP2 (14,17,30). PCRs were performed on a VWR thermocycler in total reaction volumes of 12.5 l containing 1 l of template, 1ϫ PCR buffer (10 mM Tris-HCl, 50 mM KCl, 0.1% Triton X-100), 2.5 mM MgCl 2 , 240 M deoxynucleoside triphosphates, 20 pmol of each primer, and 1 U of Taq DNA polymerase (VWR).…”

“…The antennal Streptomyces symbionts have been described for the genera Philanthus (14,15) and Trachypus (17), while other genera of the subfamily Philanthinae (Cerceris, Aphilanthops, and Clypeadon) apparently lack the symbionts (14). The rare genera Philanthinus and Pseudoscolia, however, have not yet been investigated.…”

“…Solitary digger wasps of the genera Philanthus and Trachypus (Hymenoptera, Crabronidae), the so-called beewolves, have been shown to engage in a highly specialized symbiotic association with actinobacteria of the genus Streptomyces ("Candidatus Streptomyces philanthi") (14,15,17). The symbionts are cultivated in unique antennal gland reservoirs that constitute invaginations of the outer antennal cuticle (9).…”