Abstract
ABSTRACTThe oxidation of alcohols and aldehydes is crucial for detoxification and efficient catabolism of various volatile organic compounds (VOCs). Thus, many Gram-negative bacteria have evolved periplasmic oxidation systems based on pyrroloquinoline quinone-dependent alcohol dehydrogenases (PQQ-ADHs) that are often functionally redundant. Here we report the first description and characterization of a lanthanide-dependent PQQ-ADH (PedH) in a nonmethylotrophic bacterium based on the use of purified enzymes from the soil-dwelling model organism Pseudomonas putida KT2440. PedH (PP_2679) exhibits enzyme activity on a range of substrates similar to that of its Ca2+-dependent counterpart PedE (PP_2674), including linear and aromatic primary and secondary alcohols, as well as aldehydes, but only in the presence of lanthanide ions, including La3+, Ce3+, Pr3+, Sm3+, or Nd3+. Reporter assays revealed that PedH not only has a catalytic function but is also involved in the transcriptional regulation of pedE and pedH, most likely acting as a sensory module. Notably, the underlying regulatory network is responsive to as little as 1 to 10 nM lanthanum, a concentration assumed to be of ecological relevance. The present study further demonstrates that the PQQ-dependent oxidation system is crucial for efficient growth with a variety of volatile alcohols. From these results, we conclude that functional redundancy and inverse regulation of PedE and PedH represent an adaptive strategy of P. putida KT2440 to optimize growth with volatile alcohols in response to the availability of different lanthanides.
Highlights
The oxidation of alcohols and aldehydes is crucial for detoxification and efficient catabolism of various volatile organic compounds (VOCs)
The present study reveals that one of the two PQQADHs produced by the model organism P. putida KT2440 utilizes lanthanides as a cofactor, expanding the scope of lanthanide-employing bacteria beyond the methylotrophs
Similar to the system described in methylotrophic bacteria, a complex regulatory network is involved in lanthanide-responsive switching between the two PQQ-ADHs encoded by P. putida KT2440
Summary
The oxidation of alcohols and aldehydes is crucial for detoxification and efficient catabolism of various volatile organic compounds (VOCs). VOCs include cyclic, acyclic, aromatic, and terpenoid structures with alcohol and aldehyde moieties, which are derived mainly from the metabolism of bacterial, yeast, fungal, or plant species Beside their specific molecular function, they can serve as carbon and energy sources for a wide range of microorganisms. ExaA and homologs thereof accept a wide variety of substrates and rely on a Ca2ϩ ion in the active site, in addition to the PQQ cofactor, for the oxidation of primary and secondary alcohols, as well as aldehydes [18, 24] Despite their broad substrate range, ExaA-like enzymes show only very poor conversion of methanol. Lanthanide-dependent PQQ-ADHs have been limited to methano- and methylotrophic bacteria
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