Large Freshwater Phages with the Potential to Augment Aerobic Methane Oxidation

Abstract

There is growing evidence that phages with unusually large genomes are common across various natural and human microbiomes, but little is known about their genetic inventories or potential ecosystem impacts. Here, we reconstructed large phage genomes from freshwater lakes known to contain bacteria that oxidize methane. Twenty-two manually curated genomes (18 are complete) ranging from 159 to 527 kbp 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 show high similarity (> 90%) and affiliate phylogenetically with those of coexisting bacterial methanotrophs, and their abundance patterns correlate with the abundances of these bacteria, supporting host-phage relationships. We suggest that phage PmoC has similar functions to additional copies of PmoC encoded in bacterial genomes, thus contribute to growth on methane. Transcriptomics data from one system showed that the phage-associated pmoC genes are actively expressed in situ . Augmentation of bacterial methane oxidation by pmoC-phages during infection could modulate the efflux of this powerful greenhouse gas into the environment.

Viral elements and their potential influence on microbial processes along the permanently stratified Cariaco Basin redoxcline

“…For example, cyanoviruses have auxiliary metabolic genes (AMGs) that encode for core photosynthetic reaction centers [5] and these genes are expressed during infection to boost photosynthesis and increase viral abundance [6]. Virus-encoded AMGs are known to include genes involved with nearly all of central carbon metabolism [7], nitrogen [8], phosphorus [9] and sulfur cycling [10,11], nucleotide metabolism [12][13][14], oxidative stress responses [15] and methane oxidation [16]. Even degraded prophages can reprogram metabolisms through altered gene regulation at the phage integration site [17] or by horizontal gene transfer enabling niche expansion among susceptible hosts [1].…”

Ecology of inorganic sulfur auxiliary metabolism in widespread bacteriophages

“…PsbA and PsbD play important roles in maintenance of photosynthetic energy production over time within the host; this energy is subsequently utilized for the production of resources (e.g., nucleotides) for phage propagation 12,14 . Other descriptions of AMGs include those for sulfur oxidation in the pelagic oceans 16,22 , methane oxidation in freshwater lakes 23 , ammonia oxidation in surface oceans 24 , carbon utilization (e.g., carbohydrate hydrolysis) in soils 25,26 , and marine ammonification 27 . Beyond these examples, the combined effect of phage auxiliary metabolism on ecosystems scales has yet to be fully explored or implemented into conceptualizations of microbial community functions and interactions.…”

Ecology of inorganic sulfur auxiliary metabolism in widespread bacteriophages

“…PsbA and PsbD play important roles in maintenance of photosynthetic energy production over time within the host; this energy is subsequently utilized for the production of resources (e.g., nucleotides) for phage propagation 12,14 . Other descriptions of AMGs include those for sulfur oxidation in the pelagic oceans 16,22 , methane oxidation in freshwater lakes 23 , ammonia oxidation in surface oceans 24 , carbon utilization (e.g., carbohydrate hydrolysis) in soils 25,26 , and marine ammonification 27 . Beyond these examples, the combined effect of phage auxiliary metabolism on ecosystems scales has yet to be fully explored or implemented into conceptualizations of microbial community functions and interactions.…”