Award: OCE-1829831

Throughout the global oceans, microscopic organisms such as protists, bacteria, and viruses - collectively called plankton - carry out essential ecosystem functions. These plankton serve as the foundation of marine food webs and they control biogeochemical cycles that fuel the planet. Plankton also acts as a biological carbon pump that dictates what to do with human-released carbon dioxide that the ocean absorbs from the atmosphere. Over a decade ago, an international project - the Tara Oceans Expedition - was launched to systematically sample, catalog, and study the plankton throughout the world?s oceans. Through NSF funding, we previously discovered over 200,000 ?species? of bacteria-infecting DNA viruses and found that they impact the ocean biological carbon pump, and also contained ?exotic? metabolism genes in their genomes such as photosynthesis and nitrogen metabolism genes. If viruses ?stole? these genes and repurposed them for infection, is this another way viruses impact the plankton and overall biogeochemical cycles? How many such metabolism genes have viruses stolen and do they follow any ecological patterns? Our current NSF-funded project builds on this prior work in two ways. First, we wanted to dive deeper into the ecology and impact of these virus-encoded metabolism genes, to establish a baseline understanding of how viruses might directly impact their host metabolism, and how these are distributed throughout the global oceans. We found that about 1 in 10 marine viruses carries at least one such metabolic gene and developed a global catalog for the range of metabolisms viruses could directly impact. We also found that the abundance of these metabolic functions encoded varied by ocean region and depth. Such data provide foundational ecological information that will be used in future work to parameterize models of how the oceans work. Second, this current project opened up a window into a previously near-completely neglected fraction of the viruses in the oceans - RNA viruses. To do this, we developed a novel detection pipeline, implemented a classification framework, and unraveled the biogeographical patterns of RNA viruses on a global scale that resulted in two papers published in Science. Specifically, our novel detection methods identified 5,504 RNA virus ?species?, and >99% were new species that spanned all 5 known RNA virus phyla (high-level classifications), but also revealed 5 entirely new phyla and 11 new classes. With all these new RNA viruses now ?visible? to us, we next studied their ecological patterns, drivers, and community structure, and found that they were organized around four ecological zones, and had diversity correlates with latitude, depth, and environmental variables like temperature. For example, nutrients were a strong predictor of RNA virus diversity, while depth correlated with decreased diversity. When we used machine learning and ecosystem modeling approaches to assess RNA virus roles in the ocean biological carbon pump, we see that their abundances were strongly predictive, and identified 11 specific RNA viruses that were most significant for these predictions (great targets for follow-on work). Just like with DNA viruses, we also saw that RNA viruses have stolen metabolic genes hinting at specific ways they too could be critical members of carbon flux in the oceans. Overall, the data resources, discoveries, and analytical tools that enabled them that resulted from this award will have broad impacts across several fields including virus ecology, marine microbiology, biological oceanography, microbiome science, epidemiology, as well as human and veterinary medicine. For example, our improved virus-encoded metabolic gene catalogs and RNA virus catalogs, and associated new paradigms, will be critical for oceanographic modelers, while our new RNA virus identification and classification pipelines will have impacts well outside the oceans. Last Modified: 12/02/2022 Submitted by: Matthew Sullivan