Abstract
Understanding the interplay between genotype and phenotype is a fundamental goal of functional genomics. Methane oxidation is a microbial phenotype with global-scale significance as part of the carbon biogeochemical cycle and a sink for greenhouse gas. Microorganisms that oxidize methane (methanotrophs) are taxonomically diverse and widespread around the globe. In methanotrophic bacteria, enzymes in the methane oxidation metabolic module (KEGG module M00174, conversion of methane to formaldehyde) are encoded in four operons (pmoCAB, mmoXYZBCD, mxaFI, and xoxF). Recent reports have suggested that methanotrophs in Proteobacteria acquired methane monooxygenases through horizontal gene transfer. Here, we used a genomic meta-analysis to infer the transcriptional and translational advantages of coding sequences from the methane oxidation metabolic modules of different types of methanotrophs. By analyzing isolate and metagenome-assembled genomes from phylogenetically and geographically diverse sources, we detected an anomalous nucleotide composition bias in the coding sequences of particulate methane monooxygenase genes (pmoCAB) from type Ia methanotrophs. We found that this nucleotide bias increases the level of codon bias by decreasing the GC content in the third base of codons, a strategy that contrasts with that of other coding sequences in the module. Further codon usage analyses uncovered that codon variants of the type Ia pmoCAB coding sequences deviate from the genomic signature to match ribosomal protein-coding sequences. Subsequently, computation of transcription and translation metrics revealed that the pmoCAB coding sequences of type Ia methanotrophs optimize the usage of codon variants to maximize translation efficiency and accuracy, while minimizing the synthesis cost of transcripts and proteins.IMPORTANCE Microbial methane oxidation plays a fundamental role in the biogeochemical cycle of Earth's system. Recent reports have provided evidence for the acquisition of methane monooxygenases by horizontal gene transfer in methane-oxidizing bacteria from different environments, but how evolution has shaped the coding sequences to execute methanotrophy efficiently remains unexplored. In this work, we provide genomic evidence that among the different types of methanotrophs, type Ia methanotrophs possess a unique coding sequence of the pmoCAB operon that is under positive selection for optimal resource allocation and efficient synthesis of transcripts and proteins. This adaptive trait possibly enables type Ia methanotrophs to respond robustly to fluctuating methane availability and explains their global prevalence.
Highlights
Microbial methane oxidation plays a number of fundamental roles in the global ecosystem [1]
One unexplored question of fundamental importance to our understanding of methanotrophy is how the genes that encode the methane oxidation metabolic module have been shaped by evolution to efficiently execute methanotrophy, especially after recent reports have suggested that MMOs were potentially acquired by horizontal gene transfer in some types of methanotrophs [11,12,13,14]
The pxmABC and hao coding sequences, encoding a copper᎑containing membrane monooxygenase [13] and a hydroxylamine oxidoreductase [27], respectively, were selected as outgroups as they are present in a large number of methanotroph genomes but are not part of the set of genes that formed the focus of this study
Summary
Microbial methane oxidation plays a number of fundamental roles in the global ecosystem [1]. One unexplored question of fundamental importance to our understanding of methanotrophy is how the genes that encode the methane oxidation metabolic module have been shaped by evolution to efficiently execute methanotrophy, especially after recent reports have suggested that MMOs were potentially acquired by horizontal gene transfer in some types of methanotrophs [11,12,13,14]. Gene sequences can affect the cellular economy of protein synthesis [23], reduce the metabolic burden of nucleotide synthesis by incorporating less expensive nucleotides [24], and allocate resources required for transcription [25] and translation [26]. We found that evolution has shaped the pmoCAB operon of type Ia methanotrophs with a unique coding sequence that optimizes resource allocation by reducing the biosynthetic costs of transcription and translation while ensuring translation efficiency and accuracy.
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