Concurrent Haloalkanoate Degradation and Chlorate Reduction by Pseudomonas chloritidismutans AW-1T
Authors: Peng Peng , Zheng Ying , Koehorst Jasper J. , Schaap Peter J. , Stams Alfons J. M. , Smidt Hauke , Atashgahi Siavash 
Published: April 2017

Haloalkanoates are environmental pollutants that can be degraded aerobically by microorganisms producing hydrolytic dehalogenases. However, there is a lack of information about the anaerobic degradation of haloalkanoates. Genome analysis ofPseudomonas chloritidismutansAW-1T, a facultative anaerobic chlorate-reducing bacterium, showed the presence of two putative haloacid dehalogenase genes, thel-DEX gene anddehI, encoding anl-2-haloacid dehalogenase (l-DEX) and a halocarboxylic acid dehydrogenase (DehI), respectively. Hence, we studied the concurrent degradation of haloalkanoates and chlorate as a yet-unexplored trait of strain AW-1T. The deduced amino acid sequences ofl-DEX and DehI revealed 33 to 37% and 26 to 86% identities with biochemically/structurally characterizedl-DEX and thed- anddl-2-haloacid dehalogenase enzymes, respectively. Physiological experiments confirmed that strain AW-1Tcan grow on chloroacetate, bromoacetate, and bothl- andd-α-halogenated propionates with chlorate as an electron acceptor. Interestingly, growth and haloalkanoate degradation were generally faster with chlorate as an electron acceptor than with oxygen as an electron acceptor. In line with this, analyses ofl-DEX and DehI dehalogenase activities using cell-free extract (CFE) of strain AW-1Tgrown ondl-2-chloropropionate under chlorate-reducing conditions showed up to 3.5-fold higher dehalogenase activity than the CFE obtained from AW-1Tcells grown ondl-2-chloropropionate under aerobic conditions. Reverse transcription-quantitative PCR showed that thel-DEX gene was expressed constitutively independently of the electron donor (haloalkanoates or acetate) or acceptor (chlorate or oxygen), whereas the expression of dehI was induced by haloalkanoates. Concurrent degradation of organic and inorganic halogenated compounds by strain AW-1Trepresents a unique metabolic capacity in a single bacterium, providing a new piece of the puzzle of the microbial halogen cycle.

IMPORTANCEHalogenated organic and inorganic compounds are important environmental pollutants that have carcinogenic and genotoxic effects on both animals and humans. Previous research studied the degradation of organic and inorganic halogenated compounds separately but not concurrently. This study shows concurrent degradation of halogenated alkanoates and chlorate as an electron donor and acceptor, respectively, coupled to growth in a single bacterium,Pseudomonas chloritidismutansAW-1T. Hence, besides biogenesis of molecular oxygen from chlorate reduction enabling a distinctive placement of strain AW-1Tbetween aerobic and anaerobic microorganisms, we can now add another unique metabolic potential of this bacterium to the roster. The degradation of different halogenated compounds under anoxic conditions by a single bacterium is also of interest for the natural halogen cycle in different aquatic and terrestrial ecosystems where ample natural production of halogenated compounds has been documented.