Methane-derived carbon flows into host–virus networks at different trophic levels in soil

Abstract

The concentration of atmospheric methane (CH4) continues to increase with microbial communities controlling soil–atmosphere fluxes. While there is substantial knowledge of the diversity and function of prokaryotes regulating CH4 production and consumption, their active interactions with viruses in soil have not been identified. Metagenomic sequencing of soil microbial communities enables identification of linkages between viruses and hosts. However, this does not determine if these represent current or historical interactions nor whether a virus or host are active. In this study, we identified active interactions between individual host and virus populations in situ by following the transfer of assimilated carbon. Using DNA stable-isotope probing combined with metagenomic analyses, we characterized CH4-fueled microbial networks in acidic and neutral pH soils, specifically primary and secondary utilizers, together with the recent transfer of CH4-derived carbon to viruses. A total of 63% of viral contigs from replicated soil incubations contained homologs of genes present in known methylotrophic bacteria. Genomic sequences of 13C-enriched viruses were represented in over one-third of spacers in CRISPR arrays of multiple closely related Methylocystis populations and revealed differences in their history of viral interaction. Viruses infecting nonmethanotrophic methylotrophs and heterotrophic predatory bacteria were also identified through the analysis of shared homologous genes, demonstrating that carbon is transferred to a diverse range of viruses associated with CH4-fueled microbial food networks.

Diversity in the soil virosphere: to infinity and beyond?

“…Consistent with established patterns for other soil microbes [9], viral community composition tends to vary with soil depth, pH, moisture, and across soil compartments, such as between rhizospheres and bulk soils [30,33,43,57,58,[61][62][63][64][65]. Early evidence also supports reproducible links between viruses and many components of the terrestrial carbon (C) cycle [33,57,64,[66][67][68][69].…”

Microbial Ecology of Oxygen Minimum Zones Amidst Ocean Deoxygenation

“…Additionally, viruses carrying putative AMGs from nitrogen cycle pathways have been observed in OMZs such as amoC, which encodes for ammonia monooxygenase subunit C involved in nitrification, nirK, which encodes for a Cu-containing nitrite reductase involved in denitrification, and norB, which encodes for a nitric oxide reductase involved in denitrification (Ahlgren et al, 2019;Gazitúa et al, 2021). Finally, viruses carrying the pmoC gene, a subunit of the particulate methane monooxygenase enzyme that catalyzes methane oxidation, have been observed in freshwater lakes (Chen et al, 2020) and soils (Lee et al, 2021). This indicates that viruses have the potential to augment methane oxidation by their methanotrophic hosts, even though they have yet to be observed in OMZs.…”

Substantial differences in soil viral community composition within and among four Northern California habitats

“…For example, viruses have been suggested to affect carbon cycling in thawing permafrost peatlands by preying on methanogens and methanotrophs and by encoding glycoside hydrolases to break down complex carbon into simple sugars [2]. Soil viral activity has been demonstrated [2,5,13], and soil viral communities can be spatially structured [14][15][16]. Despite these emerging ecological patterns, comparisons of soil viral diversity within and across habitats are limited.…”