Hydrolysis of aromatic β-glucosides by non-pathogenic bacteria confers a chemical weapon against predators

Abstract

Bacteria present in natural environments such as soil have evolved multiple strategies to escape predation. We report that natural isolates of Enterobacteriaceae that actively hydrolyze plant-derived aromatic b-glucosides such as salicin, arbutin and esculin, are able to avoid predation by the bacteriovorous amoeba Dictyostelium discoideum and nematodes of multiple genera belonging to the family Rhabditidae. This advantage can be observed under laboratory culture conditions as well as in the soil environment. The aglycone moiety released by the hydrolysis of b-glucosides is toxic to predators and acts via the dopaminergic receptor Dop-1 in the case of Caenorhabditis elegans. While soil isolates of nematodes belonging to the family Rhabditidae are repelled by the aglycone, laboratory strains and natural isolates of Caenorhabditis sp. are attracted to the compound, mediated by receptors that are independent of Dop-1, leading to their death. The b-glucosides-positive (Bgl þ ) bacteria that are otherwise non-pathogenic can obtain additional nutrients from the dead predators, thereby switching their role from prey to predator. This study also offers an evolutionary explanation for the retention by bacteria of 'cryptic' or 'silent' genetic systems such as the bgl operon.

Effects of Global and Specific DNA-Binding Proteins on Transcriptional Regulation of the E. coli bgl Operon

“…Further studies will be required to establish the detailed repressive mechanism of this unusual operon, as well as that responsible for the very interesting process by which IS elements activate it. This class of mutations grants wild type E. coli cells the capacity to switch the expression of the operon using insertion sequence (IS) elements as triggers, thereby enabling the protection of the cell from toxic β-glucosides while benefiting from the presence of nutritious β-glucosides [ 71 ]. It seems likely that this is another example in which small bacterial transposons have been used to allow directed mutation to occur only under appropriate environmental stress conditions, as discussed previously [ 23 , 72 , 73 , 74 , 75 , 76 , 77 , 78 , 79 , 80 ].…”

Uncovering carbohydrate metabolism through a genotype-phenotype association study of 56 lactic acid bacteria genomes

“…Following carbohydrate uptake by PTS proteins, transcriptional regulators modulate the degradation of β-glucosides like d -cellobiose, as well as aromatic β-glucosides, such as salicin and arbutin (Bardowski et al 1994 ; Sonowal et al 2013 ). All three carbohydrates, d -cellobiose, salicin, and arbutin, were shown in this study to be significantly associated with transcriptional regulators, supporting their role in the degradation of these β-glucosides (Fig.…”

Metabolism of poplar salicinoids by the generalist herbivore Lymantria dispar (Lepidoptera)

“…Salicinoids have been suggested to be activated by degradation to the toxic metabolite saligenin (reviewed in Pentzold et al, 2014) or catechol, which may oxidize to form reactive quinones (Ruuhola et al, 2001). These reactions were proposed based on the results of in vitro experiments (Clausen et al, 1990;Julkunen-Tiitto and Meier, 1992;Ruuhola et al, 2003) and studies with bacteria (Sonowal et al, 2013;Zhu et al, 1998) or vertebrates (Knuth et al, 2013;McLean et al, 2001), but the pathways of salicinoid metabolism in poplar-feeding arthropods are still not elucidated.…”