The etherase system of 𝘕𝘰𝘷𝘰𝘴𝘱𝘩𝘪𝘯𝘨𝘰𝘣𝘪𝘶𝘮 sp. MBES04 functions as a sensor of lignin fragments through phenylpropanone production to induce specific transcriptional responses

Abstract

The MBES04 strain of 𝘕𝘰𝘷𝘰𝘴𝘱𝘩𝘪𝘯𝘨𝘰𝘣𝘪𝘶𝘮 accumulates phenylpropanone monomers as end-products of the etherase system, which specifically and reductively cleaves the β-O-4 ether bond (a major bond in lignin molecules). However, it does not utilise phenylpropanone monomers as an energy source. Here, we studied the response to the lignin-related perturbation to clarify the physiological significance of its etherase system. Transcriptome analysis revealed two gene clusters, each consisting of four tandemly linked genes, specifically induced by a lignin preparation extracted from hardwood (𝘌𝘶𝘤𝘢𝘭𝘺𝘱𝘵𝘶𝘴 𝘨𝘭𝘰𝘣𝘶𝘭𝘶𝘴) and a β-O-4-type lignin model biaryl compound, but not by vanillin. The most strongly induced gene was a 2, 4′-dihydroxyacetophenone dioxygenase-like protein, which leads to energy production through oxidative degradation. The other cluster was related to multidrug resistance. The former cluster was transcriptionally regulated by a common promoter, where a phenylpropanone monomer acted as one of the effectors responsible for gene induction. These results indicate that the physiological significance of the etherase system of the strain lies in its function as a sensor for lignin fragments. This may be a survival strategy to detect nutrients and gain tolerance to recalcitrant toxic compounds, while the strain preferentially utilises easily degradable aromatic compounds with lower energy demands for catabolism.