Bacteria Associated with a Tree-Killing Insect Reduce Concentrations of Plant Defense Compounds

Abstract

Bark beetles encounter a diverse array of constitutive and rapidly induced terpenes when attempting to colonize living conifers. Concentrations of these compounds at entry sites can rapidly reach levels toxic to beetles, their brood, and fungal symbionts. Large numbers of beetles can overwhelm tree defenses via pheromone-mediated mass attacks, but the mechanisms are poorly understood. We show that bacteria associated with mountain pine beetles can metabolize monoterpenes and diterpene acids. The abilities of different symbionts to reduce concentrations of different terpenes appear complementary. Serratia reduced concentrations of all monoterpenes applied to media by 55-75 %, except for α-pinene. Beetle-associated Rahnella reduced (-)- and (+)-α-pinene by 40 % and 45 %, respectively. Serratia and Brevundimonas reduced diterpene abietic acid levels by 100 % at low concentrations. However, high concentrations exhausted this ability, suggesting that opposing rates of bacterial metabolism and plant induction of terpenes are critical. The two major fungal symbionts of mountain pine beetle, Grosmannia clavigera and Ophiostoma montium were highly susceptible to abietic acid. Grosmannia clavigera did not reduce total monoterpene concentrations in lodgepole pine turpentine. We propose the ability of bark beetles to exert landscape-scale impacts may arise partly from micro-scale processes driven by bacterial symbionts.

Gut-Associated Bacteria of Dendroctonus valens and their Involvement in Verbenone Production

“…aquatilis and bacteria in the genera Bacillus and Delftia were also detected in D. valens from America [1]. Many of them can metabolize monoterpenes of host pines [4,6,45], and the abilities of different microorganisms to reduce concentrations of different terpenes appear complementary to each other. For example, Rahnella reduced α-pinene by more than 40 %, and Serratia reduced by 55-75 % the concentrations of many monoterpenes applied to media with the exception of α-pinene [4,45].…”

Review of the Gross Anatomy and Microbiology of the Phasmatodea Digestive Tract

“…com.). in particular, the finding of Serratia marcescens, a monoterpene-degrading bacteria (Boone et al 2013), in all phasmids fed monoterpene-rich Eucalyptus suggests the microbe may function in these species to reduce the toxicity of the diet: a hypothesis that would explain how such phasmids can consume as many leaves as they do during outbreak years in Australia, where they are a significant cause of defoliation and eucalypt dieback (Jurskis & turner 2002). however, this bacteria species is cosmopolitan and was also found in the guts of blackberry-feeding Phyllium, so it is not exclusive to Eucalyptus feeders.…”

“…While cellulolytic gut symbionts would certainly facilitate digestion of the phasmids' leafy diets (Watanabe & tokuda 2010), the acidic and moderately oxidizing phasmid digestive tract is not conducive to fermentative digestion (Caarels 2011), and its straight and simple shape suggests it is more likely to be inhabited by transient microbes passing with the diet (douglas & Beard 1996(douglas & Beard , lacey et al 2007) than symbionts (dillon & dillon 2004(dillon & dillon , Watanabe & tokuda 2010. Recent transcriptomic assays confirmed that phasmatodea produce their own plant cell wall degrading enzymes (Shelomi et al 2014a) in certain sections of the gut, theoretically enabling symbiont independent digestion of compounds like cellulose (Shelomi et al 2013), but this finding is controversial (Moran et al 2008, Caarels 2011) and does not address other potential functions of the microbiome, such as in defending against plant secondary toxins (Boone et al 2013).…”

Symbiosis—Evolution’s Co-Author

“…While gut microbes are in low diversity in bark beetles likely due to the more sugar centered as opposed to cellulose diet within the phloem, the nitrogen-fixing bacterium Rahnella aquatilis is consistently found in all stages of the beetle life cycle (Six 2013). Tree defense compounds and toxins may be degraded by bacterial symbionts within some beetle species (Boone et al 2013).…”

“…For example, the mountain pine beetle expansion in western Canada has expanded over the past 40 years into more northerly latitudes and higher altitudes with a 1 °C increase. Because bark beetle bacterial symbionts are known to detoxify tree defense chemicals Boone et al 2013), evolving research is focusing on some manipulation of the bacterial community to alleviate the growing invasive strength of the beetles, especially with increasingly alarming data on anthropogenic climate change.…”