Potential virus-mediated nitrogen cycling in oxygen-depleted oceanic waters

Abstract

Viruses play an important role in the ecology and biogeochemistry of marine ecosystems. Beyond mortality and gene transfer, viruses can reprogram microbial metabolism during infection by expressing auxiliary metabolic genes (AMGs) involved in photosynthesis, central carbon metabolism, and nutrient cycling. While previous studies have focused on AMG diversity in the sunlit and dark ocean, less is known about the role of viruses in shaping metabolic networks along redox gradients associated with marine oxygen minimum zones (OMZs). Here, we analyzed relatively quantitative viral metagenomic datasets that profiled the oxygen gradient across Eastern Tropical South Pacific (ETSP) OMZ waters, assessing whether OMZ viruses might impact nitrogen (N) cycling via AMGs. Identified viral genomes encoded six N-cycle AMGs associated with denitrification, nitrification, assimilatory nitrate reduction, and nitrite transport. The majority of these AMGs (80%) were identified in T4-like Myoviridae phages, predicted to infect Cyanobacteria and Proteobacteria, or in unclassified archaeal viruses predicted to infect Thaumarchaeota. Four AMGs were exclusive to anoxic waters and had distributions that paralleled homologous microbial genes. Together, these findings suggest viruses modulate N-cycling processes within the ETSP OMZ and may contribute to nitrogen loss throughout the global oceans thus providing a baseline for their inclusion in the ecosystem and geochemical models.

Genome‐resolved viral ecology in a marine oxygen minimum zone

“…First, we were unable to confidently link more than 1% of viruses to their microbial hosts (Supporting Information Table S4), and as a result, we were not able to draw any conclusions regarding differences in host prevalence across samples and depths. In addition, while we detected many putative, viral-encoded AMGs through DRAM-v (Shaffer et al, 2020), we did not manually curate these in a method similar to the study by Gazitúa et al (2020). Future work in OMZs should be enabled by our current findings and the vast sequence database of reference virus genomes that will empower a new generation of researchers to evaluate viral roles in modulating microbial population dynamics and biogeochemical cycling climate-critical OMZs as they expand due to climate change.…”

Microbial Ecology of Oxygen Minimum Zones Amidst Ocean Deoxygenation

“…However, the relative abundance of psbA genes in T4-like cyanophages decreases with depth in the ETNP, which may be reflective of its low-light adapted Prochlorococcus host in anoxic chlorophyll maxima and suggests other AMGs are more important in OMZs (Fuchsman et al, 2021). For instance, several putative AMGs have been identified from the Cariaco Basin, the ETNP, the ETSP, and Saanich Inlet (Roux et al, 2014;Ahlgren et al, 2019;Mara et al, 2020;Vik et al, 2020;Gazitúa et al, 2021). Some of the putative AMGs found within OMZs and their overlying oxic waters potentially contribute to important processes in the carbon, nitrogen, and sulfur cycles (Figure 2).…”

“…AMGs putatively involved in sulfite oxidation, soxY, have also been observed in the ETSP (Kieft et al, 2021). 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).…”

Members of a highly widespread bacteriophage family are hallmarks of metabolic syndrome gut microbiomes

“…Heliusviridae into their hosts alters the behavior of the bacteria to an extend that they become detrimental to health. This could be achieved with phage-encoded auxiliary genes, an occurrence known from marine viruses 69,70 . Alternatively, the location of integration on the bacterial genome can alter its behaviour 8 .…”

“…The strong correlation of VC_659_0 to MetS phenotypes, coupled to the commonly found correlation to healthy microbiomes of VC_659_0 host bacteria, and the presence of potential auxiliary metabolic genes in VC_659_0 phage sequences combined introduce the possibility that prophage formation of these Ca. Heliusviridae phages alters the metabolic behavior of their host bacteria, as is known to happen in marine environments 75,76 . This could make these bacteria detrimental to health.…”