Host adaptation protects a defensive symbiont during vertical transmission in beewolf wasps (Hymenoptera: Crabronidae)
Loading...
Date issued
Authors
Editors
Journal Title
Journal ISSN
Volume Title
Publisher
Reuse License
Abstract
Microbial symbioses are ubiquitous in insects, and present key drivers of evolutionary innovation. To
stabilize a symbiosis over long evolutionary timescales, the symbiont must be reliably transmitted to
the next host generation. Vertically transmitted extracellular symbionts commonly face prolonged
periods outside of the stable host environment during transmission, entailing exposure to diverse
biotic and abiotic threats. These threats should be exacerbated in insect symbionts of evolutionary
ancient associations, which generally possess eroded genomes with reduced genetic inventories.
While external transmission is widespread among the Hemiptera, Hymenoptera, Coleoptera and
Diptera, the mechanism protecting the symbionts from environmental threats during transmission
remain poorly studied.
In this dissertation, I employ the defensive symbiosis of the European beewolf Philanthus triangulum
(Hymneoptera: Crabronidae) and the Actinobacterium ‘Candidatus Streptomyces philanthi’
(henceforth S. philanthi) to investigate how a symbiont with an eroded genome copes with a host-derived exogenous challenge during vertical transmission in an evolutionary ancient symbiosis. Female
beewolves provide their brood cells with a symbiont-containing secretion, from which S. philanthi is
later transferred to the cocoon to protect the offspring from microbial opportunists by producing
antibiotics. In the brood cell, this secretion is exposed to extremely high concentrations of toxic nitric
oxide (NO) emitted by the beewolf egg, which effectively kills antagonistic microbes. How S. philanthi
withstands the lethal burst of NO remained unknown.
I show that the symbiont’s global stress response to NO is not sufficient to survive NO concentrations
mimicking brood cell-level concentrations in vitro. Instead, I demonstrate that the symbiont-
containing secretion consisting of long-chain hydrocarbons (HCs) forms an effective NO diffusion
barrier around S. philanthi, and additionally contains host-derived protective enzymes. While different
functions of an insect’s HC profile can exert conflicting selection pressures on its composition, in vitro
assays with beewolf-derived and synthetic HCs reveal that the NO diffusion barrier function of HCs in
P. triangulum does not constrain the insect’s multifunctional HC profile. My comparisons of HC profiles
across different beewolf hosts suggest their suitability for NO protection, and in vitro assays with their
respective symbionts indicate a widespread NO sensitivity. Given the shared ecology among
beewolves, as well as additional reports on NO defense in P. gibbosus and P. basilaris, NO fumigation
and the concomitant HC-mediated protection of the symbiont from NO is likely crucial across
beewolves.
My findings add a novel dimension to the plethora of functions of insect HCs, and constitute one of
the few examples of a host adaptation protecting a symbiont from a lethal threat during external
vertical transmission. I therefore illustrate a mechanism by which a symbiotic association can be
stabilized over long evolutionary timescales, an aspect essential to our general understanding of
microbial symbiosis.