Ancient symbiosis confers desiccation resistance to stored grain pest beetles

Abstract

Microbial symbionts of insects provide a range of ecological traits to their hosts that are beneficial in the context of biotic interactions. However, little is known about insect symbiont-mediated adaptation to the abiotic environment, for example, temperature and humidity. Here, we report on an ancient clade of intracellular, bacteriome-located Bacteroidetes symbionts that are associated with grain and wood pest beetles of the phylogenetically distant families Silvanidae and Bostrichidae. In the saw-toothed grain beetle Oryzaephilus surinamensis, we demonstrate that the symbionts affect cuticle thickness, melanization and hydrocarbon profile, enhancing desiccation resistance and thereby strongly improving fitness under dry conditions. Together with earlier observations on symbiont contributions to cuticle biosynthesis in weevils, our findings indicate that convergent acquisitions of bacterial mutualists represented key adaptations enabling diverse pest beetle groups to survive and proliferate under the low ambient humidity that characterizes dry grain storage facilities.

Metabolic Cost of a Nutritional Symbiont Manifests in Delayed Reproduction in a Grain Pest Beetle

“…Few model systems have so far been established in which microbial symbionts provide nutrients, but are not obligate for their host, either in laboratory conditions or, in some cases, where natural aposymbiotic host populations have been reported [ 23 , 24 , 41 ]. We recently demonstrated that a grain pest beetle, the sawtoothed grain beetle Oryzaephilus surinamensis , harbors Bacteroidetes symbionts that support their host by hardening the cuticle [ 42 , 43 , 44 ]. O. surinamensis is able to survive and reproduce in a quite broad range of environmental humidity conditions (at least from 12% to 90%) [ 45 , 46 ], partially supported by this mutualistic association—symbiotic beetles exhibited a humidity-dependent benefit in terms of lower larval mortality and stronger population growth compared to aposymbiotic beetles [ 44 ].…”

“…We recently demonstrated that a grain pest beetle, the sawtoothed grain beetle Oryzaephilus surinamensis , harbors Bacteroidetes symbionts that support their host by hardening the cuticle [ 42 , 43 , 44 ]. O. surinamensis is able to survive and reproduce in a quite broad range of environmental humidity conditions (at least from 12% to 90%) [ 45 , 46 ], partially supported by this mutualistic association—symbiotic beetles exhibited a humidity-dependent benefit in terms of lower larval mortality and stronger population growth compared to aposymbiotic beetles [ 44 ]. While the beetles could still survive and reproduce without their symbionts under low humidity (30% RH), they suffered a 50–70% fitness reduction.…”

Editorial 2019

“…The third section probed the evolution of symbiotic relationships and how they shape host adaptation (Engl et al, 2018;Gauthier et al., 2018;Vanderpool, Bracewell, & McCutcheon, 2018) and the fourth section looked into the resilience of these relationships in the changing environment of the Anthropocene (Deveautour, Donn, Power, Bennett, & Powell, 2018;Doremus et al, 2018;Ramsby, Hoogenboom, Whalan, & Webster, 2018).…”

Introduction: The host‐associated microbiome: Pattern, process and function

“…Engl and colleagues use 16S rRNA sequencing, microscopy and experimental manipulation to investigate the identity of bacterial endosymbionts of grain beetles—major stored grain pests worldwide—further assessing the adaptive significance of these faithfully transmitted, bacteriocyte‐dwelling microbes (Engl et al., ). They first find that the endosymbionts are from the Bacteroidetes phylum and related to well‐known insect symbionts Sulcia (cicadas) and Blattabacterium (cockroaches), which are both obligate nutritional symbionts (Moran et al., ).…”