Article
Open Access
Published: 16 November 2020
Potential virus-mediated nitrogen cycling in oxygen-depleted oceanic watersAbstract
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.
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Earth’s biogeochemical cycles are driven by microbial interaction networks, with significant contributions from the oceans [1, 2]. These networks and the distribution of metabolic pathways within them are modulated by environmental factors, grazing, and viral infections. Ocean viruses are abundant, kill ~20–40% of microbial cells per day,
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Earth’s biogeochemical cycles are driven by microbial interaction networks, with significant contributions from the oceans [1, 2]. These networks and the distribution of metabolic pathways within them are modulated by environmental factors, grazing, and viral infections. Ocean viruses are abundant, kill ~20–40% of microbial cells per day,
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In summary, understanding how viruses alter N-related biogeochemical cycling in OMZs is critical, considering the expansion of these suboxic and anoxic water masses and their effects in surface primary production, greenhouse gas emission, and fixed-nitrogen loss [32,33,34]. Our findings imply that OMZ viruses impact N cycling not only through lysis of key N-cycling microbes but also by modulating diverse N-metabolisms during infection. Such infected “virocells” [10] would be drastically altered in their metabolic capacity and biogeochemical outputs as has been shown now in several environmental model virus–host systems [10, 12, 129]. With these N-related virus AMGs now uncovered, future OMZ virus work can evaluate virocell-impacted nitrogen cycling, as well as develop primer sets for “viral” vs “cellular” versions to differentially quantify the biogeochemical impacts of viruses in OMZ N-cycling genes and transcripts. As standardized practices emerge for viral ecogenomics [130,131,132], they are enabling the development of global maps of ocean viruses [30, 49, 133] that can be integrated into multi-organism ecological studies [134]. Together these efforts to understand virus-mediated nutrient cycling in climate-critical environments, along with parallel efforts on land (e.g., thawing permafrosts [135, 136]), are now providing quantitative information needed to incorporate viruses into predictive models [137].
https://www.nature.com/articles/s41396-020-00825-6