Mountain Pine Beetles Colonizing Historical and Naïve Host Trees Are Associated with a Bacterial Community Highly Enriched in Genes Contributing to Terpene Metabolism

Abstract

eThe mountain pine beetle, Dendroctonus ponderosae, is a subcortical herbivore native to western North America that can kill healthy conifers by overcoming host tree defenses, which consist largely of high terpene concentrations. The mechanisms by which these beetles contend with toxic compounds are not well understood. Here, we explore a component of the hypothesis that beetle-associated bacterial symbionts contribute to the ability of D. ponderosae to overcome tree defenses by assisting with terpene detoxification. Such symbionts may facilitate host tree transitions during range expansions currently being driven by climate change. For example, this insect has recently breached the historical geophysical barrier of the Canadian Rocky Mountains, providing access to näive tree hosts and unprecedented connectivity to eastern forests. We use culture-independent techniques to describe the bacterial community associated with D. ponderosae beetles and their galleries from their historical host, Pinus contorta, and their more recent host, hybrid P. contorta-Pinus banksiana. We show that these communities are enriched with genes involved in terpene degradation compared with other plant biomass-processing microbial communities. These pine beetle microbial communities are dominated by members of the genera Pseudomonas, Rahnella, Serratia, and Burkholderia, and the majority of genes involved in terpene degradation belong to these genera. Our work provides the first metagenome of bacterial communities associated with a bark beetle and is consistent with a potential microbial contribution to detoxification of tree defenses needed to survive the subcortical environment.

Influence of Starvation on the Structure of Gut-Associated Bacterial Communities in the Chinese White Pine Beetle (Dendroctonus armandi)

“…The molecular analysis indicated that the predominant species in the D. armandi bacterial community formed a low complexity group with a different structure after starvation. Low-complexity gut microbial communities have been reported for D. rhizophagus, D. valens and D. ponderosae [31][32][33]. Additionally, as found in all of the D. armandi developmental stages, some taxa were shared among the bacterial communities [12].…”

Symbiosis as a General Principle in Eukaryotic Evolution

“…Plant allelochemical detoxification has also been implicated in certain insect symbioses, notably bark-feeding beetles and leaf-cutting ants. The gut microbiota of the mountain pine beetle Dendroctonus ponderosae include bacteria of the genera Pseudomonas, Serratia, Rahnella, and Burkholderia that bear genes involved in the degradation of terpenes, the principal defensive compounds of the trees infested by these beetles (Adams et al 2013). The leaf-cutting ant Acromyrmex echinatior maintains, and feeds on, the symbiotic fungus Leucocoprinus gongylophorus in its nest.…”

Cellulolytic Streptomyces Strains Associated with Herbivorous Insects Share a Phylogenetically Linked Capacity To Degrade Lignocellulose

“…A fourth Streptomyces strain, DpondAA-B6 (SDPB6), was isolated from a surface-sterilized adult mountain pine beetle collected from a naturally attacked Pinus contorta tree near Mackenzie, British Columbia, Canada (Fig. 1A) (27). Cellulolytic activities were significantly different among these four strains (Fig.…”

“…Streptomyces sp. DpondAA-B6 (SDPB6; NCBI Taxonomy ID 682311) was isolated from samples of D. ponderosae adults collected from naturally attacked P. contorta trees near Mackenzie, British Columbia, Canada (27). Adult insects were surface sterilized in 95% ethanol for 1 min, rinsed twice in sterile phosphate-buffered solution (PBS), and homogenized in PBS, and dilutions were spread onto agar plates supplemented with chitin.…”