An aerobic link between lignin degradation and C1 metabolism: growth on methoxylated aromatic compounds by members of the genus Methylobacterium

Microorganisms faces many barriers in the degradation of the polycyclic aromatic polymer lignin, one of which is an abundance of methoxy substituents. Demethoxylation of lignin-derived aromatic monomers in aerobic environments releases formaldehyde, a potent cellular toxin that organisms must eliminate in order to further degrade the aromatic ring. Here we provide the first comprehensive description of the ecology and evolution of the catabolism of methoxylated aromatics in the genus Methylobacterium, a plant-associated genus of methylotrophs capable of using formaldehyde for growth. Using comparative genomics, we found that the capacity for aromatic catabolism is ancestral to two clades, but has also been acquired horizontally by other members of the genus. Through laboratory growth assays, we demonstrated that several Methylobacterium strains can grow on p-hydroxybenzoate, protocatechuate, vanillate, and ferulate; furthermore, whereas non-methylotrophs excrete formaldehyde as a byproduct during growth on vanillate, Methylobacterium do not. Finally, we surveyed published metagenome data to find that vanillate-degrading Methylobacterium can be found in many soil and rhizosphere ecosystems but is disproportionately prominent in the phyllosphere, and the most highly represented clade in the environment (the root-nodulating species M. nodulans) is one with few cultured representatives.