Genomic Insights into Methanotrophy: The Complete Genome Sequence of Methylococcus capsulatus (Bath)

Abstract

Methanotrophs are ubiquitous bacteria that can use the greenhouse gas methane as a sole carbon and energy source for growth, thus playing major roles in global carbon cycles, and in particular, substantially reducing emissions of biologically generated methane to the atmosphere. Despite their importance, and in contrast to organisms that play roles in other major parts of the carbon cycle such as photosynthesis, no genome-level studies have been published on the biology of methanotrophs. We report the first complete genome sequence to our knowledge from an obligate methanotroph, Methylococcus capsulatus (Bath), obtained by the shotgun sequencing approach. Analysis revealed a 3.3-Mb genome highly specialized for a methanotrophic lifestyle, including redundant pathways predicted to be involved in methanotrophy and duplicated genes for essential enzymes such as the methane monooxygenases. We used phylogenomic analysis, gene order information, and comparative analysis with the partially sequenced methylotroph Methylobacterium extorquens to detect genes of unknown function likely to be involved in methanotrophy and methylotrophy. Genome analysis suggests the ability of M. capsulatus to scavenge copper (including a previously unreported nonribosomal peptide synthetase) and to use copper in regulation of methanotrophy, but the exact regulatory mechanisms remain unclear. One of the most surprising outcomes of the project is evidence suggesting the existence of previously unsuspected metabolic flexibility in M. capsulatus, including an ability to grow on sugars, oxidize chemolithotrophic hydrogen and sulfur, and live under reduced oxygen tension, all of which have implications for methanotroph ecology. The availability of the complete genome of M. capsulatus (Bath) deepens our understanding of methanotroph biology and its relationship to global carbon cycles. We have gained evidence for greater metabolic flexibility than was previously known, and for genetic components that may have biotechnological potential.

Microbial minorities modulate methane consumption through niche partitioning

“…(Supplementary Tables S2-S6). Although several genome sequences of MOB (Methylomonas methanica MC09 (Boden et al, 2011), Methylomicrobium album strain BG8, Methylococcus capsulatus strain Bath and Texas (Ward et al, 2004;Kleiveland et al, 2012), Methylocystis strain Rockwell (Stein et al, 2011), Methylocystis strain SC2 (Dam et al, 2012), Methylocystis parvus OBBP (del Cerro et al, 2012), Methylosinus trichosporium OB3b (Stein et al, 2010)) were deposited in the consulted NCBI nr database, almost no other labeled peptide sequences affiliated to MOB were identified besides peptides of Methylobacter tundripaludum SV96. In addition, most of the identified peptide sequences had to be excluded according to the stringent Mascot scoring parameters, which may be related to the soil matrix.…”

Functioning in situ: gene expression in Methylotenera mobilis in its native environment as assessed through transcriptomics

“…Indeed, such lesions have been confirmed through the genomic analysis of some obligate methylotrophs, such as Methylobacillus flagellatus (Chistoserdova et al, 2007). However, genomes of other obligate methylotrophs, such as Methylococcus capsulatus, were found to encode all the functions necessary for growth on multicarbon compounds (Ward et al, 2004;Kelly et al, 2005). This points to the fact that growth and behavior of such microbes as observed in the laboratory may not fully reflect their physiological potential encoded in the genome and that some of the genomic features must be only expressed under specific environmental conditions.…”

Mutagenesis of a Copper P-Type ATPase Encoding Genein Methylococcus capsulatus (Bath) Results inCopper-Resistance

“…Copper also increases the synthesis of an extensive network of intracytoplasmic membranes [10] and is the active center metal of pMMO [11] Little is known about copper homeostasis in M. capsulatus although copper has a significant physiological role in this methanotroph. The genome sequencing of M. capsulatus led to the identification of four copper transport homologues [12]. Among them, three copper translocating P-type ATPase homologues; MCA0705, MCA0805 and MCA2072 were identified.…”