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We describe five novel Methylophilaceae ecotypes from a single ecological niche in Lake Washington, USA, and compare them to three previously described ecotypes, in terms of their phenotype and genome sequence divergence. Two of the ecotypes appear to represent novel genera within the Methylophilaceae. Genome-based metabolic reconstruction highlights metabolic versatility of Methylophilaceae with respect to methylotrophy and nitrogen metabolism, different ecotypes possessing different combinations of primary substrate oxidation systems (MxaFI-type methanol dehydrogenase versus XoxF-type methanol dehydrogenase; methylamine dehydrogenase versus N-methylglutamate pathway) and different potentials for denitrification (assimilatory versus respiratory nitrate reduction). By comparing pairs of closely related genomes, we uncover that site-specific recombination is the main means of genomic evolution and strain divergence, including lateral transfers of genes from both closely- and distantly related taxa. The new ecotypes and the new genomes contribute significantly to our understanding of the extent of genomic and metabolic diversity among organisms of the same family inhabiting the same ecological niche. These organisms also provide novel experimental models for studying the complexity and the function of the microbial communities active in methylotrophy.

Phylogenetic positions, and genotypic and phenotypic characteristics of three novel methylotrophic isolates, strains 301(T), 30S and SIP3-4, from sediment of Lake Washington, Seattle, USA, are described. The strains were restricted facultative methylotrophs capable of growth on single carbon compounds (methylamine and methanol) in addition to a limited range of multicarbon compounds. All strains used the N-methylglutamate pathway for methylamine oxidation. Strain SIP3-4 possessed the canonical (MxaFI) methanol dehydrogenase, but strains 301(T) and 30S did not. All three strains used the ribulose monophosphate pathway for C1 assimilation. The major fatty acids in the three strains were C(16:0) and C(16:1)ω7c. The DNA G+C contents of strains 301(T) and SIP3-4 were 42.6 and 54.6 mol%, respectively. Based on 16S rRNA gene sequence phylogeny and the relevant phenotypic characteristics, strain SIP3-4 was assigned to the previously defined species Methylovorus glucosotrophus. Strains 301(T) and 30S were closely related to each other (100% 16S rRNA gene sequence similarity) and shared 96.6% 16S rRNA gene sequence similarity with a previously described isolate, Methylotenera mobilis JLW8(T). Based on significant genomic and phenotypic divergence with the latter, strains 301(T) and 30S represent a novel species within the genus Methylotenera, for which the name Methylotenera versatilis sp. nov. is proposed; the type strain is 301(T) (=VKM B-2679(T)=JCM 17579(T)). An emended description of the genus Methylotenera is provided.