A novel soluble di‐iron monooxygenase from the soil bacterium Solimonas soli

• Published in: Environmental microbiology 2024-02, Vol.26 (2), p.e16567-n/a
• Main Authors: Yang, Sui Nin Nicholas, Haritos, Victoria, Kertesz, Michael A., Coleman, Nicholas V.
• Format: Article
• Language: English
• Subjects: Acrylic acid; Alkenes; Alkenes - metabolism; Amino acids; biocatalysis; Biodegradation, Environmental; Biogeochemistry; Bioremediation; carboxylation; Catalysis; chlorinated hydrocarbons; Chlorine compounds; E coli; Epoxidation; epoxidation reactions; Epoxides; Escherichia coli; Gammaproteobacteria - metabolism; Genes; Genomes; Iron; Mixed Function Oxygenases - genetics; Mixed Function Oxygenases - metabolism; octane; Organic compounds; Organochlorine compounds; oxygen; phenol; Phenols; propylene; Pseudomonas putida; Pseudomonas putida - genetics; Pseudomonas putida - metabolism; Recombinants; Soil bacteria; soil biota; Soil microorganisms; Soils; Substrates; Vinyl Chloride
• ISSN: 1462-2912; 1462-2920
• DOI: 10.1111/1462-2920.16567

Soluble di‐iron monooxygenase (SDIMO) enzymes enable insertion of oxygen into diverse substrates and play significant roles in biogeochemistry, bioremediation and biocatalysis. An unusual SDIMO was detected in an earlier study in the genome of the soil organism Solimonas soli, but was not characterized. Here, we show that the S. soli SDIMO is part of a new clade, which we define as ‘Group 7’; these share a conserved gene organization with alkene monooxygenases but have only low amino acid identity. The S. soli genes (named zmoABCD) could be functionally expressed in Pseudomonas putida KT2440 but not in Escherichia coli TOP10. The recombinants made epoxides from C2C8 alkenes, preferring small linear alkenes (e.g. propene), but also epoxidating branched, carboxylated and chlorinated substrates. Enzymatic epoxidation of acrylic acid was observed for the first time. ZmoABCD oxidised the organochlorine pollutants vinyl chloride (VC) and cis‐1,2‐dichloroethene (cDCE), with the release of inorganic chloride from VC but not cDCE. The original host bacterium S. soli could not grow on any alkenes tested but grew well on phenol and n‐octane. Further work is needed to link ZmoABCD and the other Group 7 SDIMOs to specific physiological and ecological roles. Heterologous expression of an unusual soluble di‐iron monooxygenase (SDIMO) gene cluster from Solimonas soli reveals that this enzyme oxidizes C2C8 alkenes, although S. soli does not use these as carbon and energy sources. A new SDIMO clade (“Group 7”) is defined, which includes ZmoABCD as the first characterized representative.