Of mothballs and old yellow enzymes.

Abstract

Polycyclic aromatic hydrocarbons (PAHs) are persistent and toxic environmental pollutants that accumulate in anoxic habitats. With the exception of naphthalene, nothing is known about the microbial degradation of PAH in these environments. The challenge that must be met in anaerobic PAH degradation is the destabilization of the resonance energy of the aromatic ring system, which requires electrons with very negative redox potentials. Estelmann et al. (2014) identify two enzymes from sulphate-reducing bacteria that perform successive 2-electron reductions of a coenzyme A thioester derivative of naphthalene. The first reduces 2-naphthoyl-CoA to 5,6-dihydro-2-naphthoyl-CoA and the second generates 5,6,7,8-tetrahydro-2-naphthoyl-CoA. Surprisingly, both enzymes are members of the 'old yellow enzyme' (OYE) family of flavoproteins. Neither uses adenosine triphosphate to achieve reduction of the aromatic ring. Typically, OYEs have flavin mononucleotide as cofactor and use nicotinamide adenine dinucleotide (phosphate) as reductant. Both ring reductases have flavin adenine dinucleotide and an iron-sulphur cluster as additional cofactors. Evidence also suggests that in the sulphate-reducing bacteria, these enzymes form a complex, allowing substrate channeling. The findings of this superb study represent unprecedented biochemistry. This work sheds light on how microbes meet the thermodynamic challenges of life at the redox limit.