Strain CSC1^T, a Gram-negative, aerobic, methane-oxidizing bacterium, was isolated from an uncontaminated aquifer nearly 20 years ago. Based on 16S rRNA gene sequence similarity, this strain was identified as a member of the Alphaproteobacteria, most closely related to an uncultured member of the Methylocystaceae as well as two cultured organisms, Methylocystis sp. L32 and Methylocystis sp. SC2. This strain differed from extant species in cell shape, size, expression of soluble methane monooxygenase and its unique spiny surface layers, composed of polysaccharide. DNA–DNA hybridization results showed only 3.8 % relatedness with Methylocystis echinoides NCIMB 13100 and 41.1 % relatedness with Methylocystis rosea SV97^T. Based on these genotypic and physiological differences, this isolate is proposed as a member of a novel species of the genus Methylocystis, Methylocystis hirsuta sp. nov. (type strain CSC1^T =ATCC BAA-1344^T =DSM 18500^T).