Interactions between Bacteria And Aspen Defense Chemicals at the Phyllosphere – Herbivore Interface
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Plant- and insect-associated microorganisms encounter a diversity of allelochemicals, and require mechanisms for contending with these often deleterious and broadly-acting compounds. Trembling aspen, Populus tremuloides, contains two principal groups of defenses, phenolic glycosides (salicinoids) and condensed tannins, which differentially affect the folivorous gypsy moth, Lymantria dispar, and its gut symbionts. The bacteria genus Acinetobacter is frequently associated with both aspen foliage and gypsy moth consuming that tissue, and one isolate, Acinetobacter sp. R7-1, previously has been shown to metabolize phenolic glycosides. In this study, we aimed to characterize further interactions between this Acinetobacter isolate and aspen secondary metabolites. We assessed bacterial carbon utilization and growth in response to different concentrations of phenolic glycosides and condensed tannins. We also tested if enzyme inhibitors reduce bacterial growth and catabolism of phenolic glycosides. Acinetobacter sp. R7-1 utilized condensed tannins but not phenolic glycosides or glucose as carbon sources. Growth in nutrient-rich medium was increased by condensed tannins, but reduced by phenolic glycosides. Addition of the P450 enzyme inhibitor piperonyl butoxide increased the effects of phenolic glycosides on Acinetobacter sp. R7-1. In contrast, the esterase inhibitor S,S,S,-tributyl-phosphorotrithioate did not affect phenolic glycoside inhibition of bacterial growth. Degradation of phenolic glycosides by Acinetobacter sp. R7-1 appears to alleviate the cytotoxicity of these compounds, rather than provide an energy source. Our results further suggest this bacterium utilizes additional, complementary mechanisms to degrade antimicrobial phytochemicals. Collectively, these results provide insight into mechanisms by which microorganisms contend with their environment within the context of plant-herbivore interactions.
KeywordsAcinetobacter Lymantria dispar Condensed tannins Detoxification Gypsy moth P450 Phenolic glycosides
This research was funded in part by UW-Madison College of Agricultural and Life Sciences, USDA Hatch #WIS01598 awarded to Kenneth Raffa, and USDA NIFA AFRI Grant No. 2011-67013-30147 awarded to Richard Lindroth and Kenneth Raffa. Tiffany Lowe is funded in part by NIH National Research Service Award T32 GM07215 and by USDA NIFA AFRI Grant No. 2015-67011-22799. Critical comments by three anonymous reviewers improved the quality of the manuscript.
- Adams AS, Aylward FO, Adams SM, Erbilgin N, Aukema BH, Currie CR, Suen G, Raffa KF (2013) Mountain pine beetles colonizing historical and naive host trees are associated with a bacterial community highly enriched in genes contributing to terpene metabolism. Appl Environ Microbiol 79:3468–3475CrossRefPubMedPubMedCentralGoogle Scholar
- Boucher C, Barberis P, Trigalet A, Demery D (1985) Transposon mutagenesis of Pseudomonas solanacearum: isolation of Tn5-induced avirulent mutants. J Gen Microbiol 131:2449–2457Google Scholar
- Martin MM, Rockholm DC, Martin JS (1985) Effects of surfactants, pH, and certain cations on precipitation of proteins by tannins. J. Chem. Ecol 11:485–494Google Scholar
- Nemec A, Krizova L, Maixnerova M, Der Reijden TJK V, Deschaght P, Passet V, Vaneechoutte M, Brisse S, Dijkshoorn L (2011) Genotypic and phenotypic characterization of the Acinetobacter calcoaceticus-Acinetobacter baumannii complex with the proposal of Acinetobacter pittii sp. nov. (formerly Acinetobacter genomic species 3) and Acinetobacter nosocomialis sp. nov. (formerly Acinetobacter. sp 13TU). Res Microbiol 162:393–404CrossRefPubMedGoogle Scholar
- Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proceedings of the National Academy of Sciences of the United States of America, 100:1803–1807Google Scholar
- Oliver KM, Martinez AJ (2014) How resident microbes modulate ecologically-important traits of insects. Current Opinion in Insect Science, 4:1–7Google Scholar
- Schweitzer JA, Madritch MD, Bailey JK, Leroy CJ, Fischer G, Rehill BJ, Lindroth RL, Hagerman AE, Wooley SC, Stephen C, Whitham TG, Schweitzer A, Bailey K, Fischer DG, Hart SC (2008) From genes to ecosystems: the genetic basis of condensed tannins and their role in nutrient regulation in a Populus model system. Ecosystems 11:1005–1020CrossRefGoogle Scholar
- Scully ED, Geib SM, Carlson JE, Tien M, Mckenna D, Hoover K (2014) Functional genomics and microbiome profiling of the Asian longhorned beetle (Anoplophora glabripennis) reveal insights into the digestive physiology and nutritional ecology of wood feeding beetles. BMC Genomics 15:1096CrossRefPubMedPubMedCentralGoogle Scholar
- Welte CU, de Graaf RM, van den Bosch TJM, den Camp HJMO, van Dam NM, Jetten MSM (2015) Plasmids from the gut microbiome of cabbage root fly larvae encode SaxA that catalyses the conversion of the plant toxin 2-phenylethyl isothiocyanate. Env Microbiol DOI. doi: 10.1111/1462-2920.12997 Google Scholar