Abstract
There is growing evidence that phages with unusually large genomes are common across various microbiomes, but little is known about their genetic inventories or potential ecosystem impacts. In the present study, we reconstructed large phage genomes from freshwater lakes known to contain bacteria that oxidize methane. Of manually curated genomes, 22 (18 are complete), ranging from 159 kilobase (kb) to 527 kb in length, were found to encode the pmoC gene, an enzymatically critical subunit of the particulate methane monooxygenase, the predominant methane oxidation catalyst in nature. The phage-associated PmoC sequences show high similarity to (>90%), and affiliate phylogenetically with, those of coexisting bacterial methanotrophs, including members of Methyloparacoccus, Methylocystis and Methylobacter spp. In addition, pmoC-phage abundance patterns correlate with those of the coexisting bacterial methanotrophs, supporting host–phage relationships. Future work is needed to determine whether phage-associated PmoC has similar functions to additional copies of PmoC encoded in bacterial genomes, thus contributing to growth on methane. Transcriptomics data from Lake Rotsee (Switzerland) showed that some phage-associated pmoC genes were highly expressed in situ and, of interest, that the most rapidly growing methanotroph was infected by three pmoC-phages. Thus, augmentation of bacterial methane oxidation by pmoC-phages during infection could modulate the efflux of this potent greenhouse gas into the environment.
Highlights
There is growing evidence that phages with unusually large genomes are common across various microbiomes, but little is known about their genetic inventories or potential ecosystem impacts
Biological oxidation of methane is largely driven by microorganisms, including aerobic methanotrophs belonging to Alphaproteobacteria, Gammaproteobacteria and Verrucomicrobia[9,10] which use soluble methane monooxygenases and/or particulate methane monooxygenases[11]
We investigated the metagenomic datasets from freshwater lakes Crystal Bog and Lake Mendota in Madison, WI, United States and Lake Rotsee in Switzerland[16], which are known sources of sediment-derived methane[17], and found examples of pmoC on a subset of phage genomic fragments from all three ecosystems
Summary
There is growing evidence that phages with unusually large genomes are common across various microbiomes, but little is known about their genetic inventories or potential ecosystem impacts. We reconstructed large phage genomes from freshwater lakes known to contain bacteria that oxidize methane. 22 (18 are complete), ranging from 159 kilobase (kb) to 527 kb in length, were found to encode the pmoC gene, an enzymatically critical subunit of the particulate methane monooxygenase, the predominant methane oxidation catalyst in nature. The pMMO, the predominant methane oxidation catalyst in nature, is a 300-kDa trimeric metalloenzyme[12] that converts methane to methanol in the periplasm[11,13] It is encoded by the pmoCAB operon[14] and some bacterial genomes encode multiple pmoCAB operons as well as additional copies of pmoC that appear to be essential for growth on methane[15]. We suggest that pmoC-phages may play important roles in the methane cycle when infecting their bacterial hosts
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