Abstract
The involvement of bacterial aromatic ring-hydroxylating dioxygenases (ARHDs) in the degradation of aromatic pollutants, such as polychlorinated biphenyls (PCBs), has been well studied. However, there is considerable speculation as to the origin of this ability. One hypothesis is centered on a connection between the ability to degrade aromatic pollutants and the necessity of soil bacteria to cope with and/or utilize secondary plant metabolites (SPMs). To investigate this connection, we researched the involvement of biphenyl 2,3-dioxygenase (BPDO), an ARHD essential for the degradation of PCBs, in the metabolism of SPMs in the soil bacterium Pseudomonas alcaliphila JAB1, a versatile degrader of PCBs. We demonstrated the ability of the strain JAB1 to transform a variety of SPMs, namely the flavonoids apigenin, flavone, flavanone, naringenin, fisetin, quercetin, morin, and catechin, caffeic acid, trans-cinnamic acid, and the monoterpenes (S)-limonene and (R)-carvone. Of those, the transformation of flavone, flavanone, and (S)-limonene was conditioned by the activity of JAB1-borne BPDO and thus was researched in more detail, and we found evidence for the limonene monooxygenase activity of the BPDO. Furthermore, the bphA gene in the strain JAB1 was demonstrated to be induced by a wide range of SPMs, with monoterpenes being the strongest inducers of the SPMs tested. Thus, our findings contribute to the growing body of evidence that ARHDs not only play a role in the catabolism of aromatic pollutants, but also of natural plant-derived aromatics, and this study supports the hypothesis that ARHDs participate in ecological processes mediated by SPMs.
Highlights
Secondary plant metabolites (SPMs) are a highly diverse group of compounds of plant origin with numerous functions in ecological processes
With the example of biphenyl 2,3-dioxygenase (BPDO) from the soil polychlorinated biphenyls (PCBs)-degrader Pseudomonas alcaliphila JAB1 (Ryslava et al, 2003; Ridl et al, 2018), we provide a complex investigation of how a wide variety of secondary plant metabolites (SPMs), including flavonoids, phenolic acids, coumarins, and monoterpenes, induce the expression of this BPDO, and that this BPDO is involved in the degradation of some of these SPMs
In order to be able to distinguish the involvement of the JAB1borne BPDO in the transformation of SPMs, the strain JAB1ΔbphA was employed alongside the wild-type strain
Summary
Secondary plant metabolites (SPMs) are a highly diverse group of compounds of plant origin with numerous functions in ecological processes. SPMs have a wide range of both positive and negative effects on soil microbial communities (reviewed by Musilova et al, 2016). They can serve as growth substrates for many bacteria (Donnelly et al, 1994; Fraraccio et al, 2017) or are involved in plant-microbe crosstalk during the establishment of mutualistic symbiosis (Liu and Murray, 2016). To deal with the selective pressure resulting from the detrimental effect of SPMs, soil microbiota responds with two mechanisms of resistance. One group of enzymes involved in the bacterial transformation of aromatic compounds is aromatic ringhydroxylating dioxygenases (ARHDs), multicomponent non-heme oxidoreductases that usually exhibit broad substrate specificity (Baldwin et al, 2000). ARHDs have been mostly described in connection with the degradation of aromatic pollutants, including polychlorinated biphenyls (PCBs), under aerobic conditions (Eltis and Bolin, 1996; Vezina et al, 2008); they attack aromatic compounds, which are usually inert and stable, and activate the substrate for subsequent reactions leading to the cleavage of the aromatic ring (Parales and Resnick, 2006)
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