Methylospira mobilis is a recently described spiral-shaped, micro-aerobic methanotroph, which inhabits northern freshwater wetlands and sediments. Due to difficulties of cultivation, it could not be obtained in a pure culture for a long time. Here, we report on the successful isolation of strain Shm1, the first axenic culture of this unique methanotroph. The complete genome sequence obtained for strain Shm1 was 4.7 Mb in size and contained over 4800 potential protein-coding genes. The array of genes encoding C metabolic capabilities in strain Shm1 was highly similar to that in the closely related non-motile, moderately thermophilic methanotroph Methylococcus capsulatus Bath. The genomes of both methanotrophs encoded both low- and high-affinity oxidases, which allow their survival in a wide range of oxygen concentrations. The repertoire of signal transduction systems encoded in the genome of strain Shm1, however, by far exceeded that in Methylococcus capsulatus Bath but was comparable to those in other motile gammaproteobacterial methanotrophs. The complete set of motility genes, the presence of both the molybdenum-iron and vanadium-iron nitrogenases, as well as a large number of insertion sequences were also among the features, which define environmental adaptation of to water-saturated, micro-oxic, heterogeneous habitats depleted in available nitrogen.