Mountain pine beetles colonizing historical and naive host trees are associated with a bacterial community highly enriched in genes contributing to terpene metabolism

Abstract

The 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.

Fig 1

Outbreak and spread of D. ponderosae in western Canada from 1999 to 2010 (A) and sampling locations of beetles and galleries from lodgepole (LP) and hybrid (HY) pines (B). (The map in panel A is a copy of an official work published by Natural Resources Canada but has not been produced in affiliation with, or with the endorsement of, the Government of Canada.)

Fig 2

Results of genus-level phylogenetic binning of the four beetle-associated community metagenome assemblies (A). Phylogenetic binning of only contigs containing genes annotated in the KEGG limonene and pinene degradation pathway or dit cluster of Pseudomonas abietaniphila BKME-9 (B). Only those genera with greater than 1% representation are shown.

Fig 3

Representation of genes involved in diterpene degradation in mountain pine beetle-associated metagenomes. (A) In the diterpene degradation gene cluster dit, each gene is colored according to its representation within the four mountain pine beetle metagenomes. (B) Total copy numbers for each gene are shown, with those in blue enriched (Fisher's exact test, P < 0.05) relative to other plant biomass-degrading metagenomes.