A recent study has advanced our understanding of how viruses interact with the global ocean’s nutrient cycling system, involving vital elements like nitrogen, phosphorus, and particularly carbon. Researchers have developed a comprehensive catalog of genes that viruses have appropriated from marine microbes they have infected across the oceans, successfully identifying and compiling nearly 23,000 auxiliary metabolic genes (AMGs), including over 7,000 that had never been documented before.
Microbes play a crucial role in nutrient cycling within the ocean, but they do not accomplish this alone. The viruses that infect these microbes also significantly influence this process. This interaction is essential for the planet, enabling oceans to absorb around half of the carbon produced by human activities and generating about half of the oxygen we rely on.
This new research builds on a discovery made two decades ago regarding the exchange of genes between viruses and the photosynthetic cells they invade, consolidating findings from over 100 research papers focused on viruses and their metabolic roles.
Led by The Ohio State University, the research team reports their findings in the journal Microbiome. They created a catalog showcasing genes that viruses have “taken” from marine microbes across the world’s oceans. This investigation revealed nearly 23,000 auxiliary metabolic genes (AMGs), with over 7,000 of these being newly identified. The analysis indicates that roughly 20% of ocean virus populations harbor at least one AMG.
To further elaborate on the role of these viruses, the researchers mapped out 340 metabolic pathways associated with oceanic microbes. These pathways represent changes in nutrient dynamics driven by organisms’ consumption and metabolic activities. Out of these, they discovered that viral AMGs were linked to 128 pathways, suggesting that viruses impact over 37% of the metabolic processes involved.
“While we still have much to learn about the overall influence of viruses, now that we understand which pathways they target through AMGs, we can apply metabolic modeling techniques to estimate how these viruses affect host communities and ocean health,” said Funing Tian, the first author of the study and a PhD student in microbiology at Ohio State.
“Future modeling could involve adjusting the metabolic activity across these pathways to observe how the influence of viruses varies,” she added.
Tian and co-author James Wainaina concentrated particularly on DNA viruses that invade prokaryotic organisms like bacteria and other single-celled life forms found in the oceans.
Both Wainaina and Tian were part of the research group led by senior author Matthew Sullivan, a microbiology professor and founding director of the Center of Microbiome Science at Ohio State.
Sullivan also acted as the viral coordinator for the Tara Oceans Consortium, a comprehensive three-year study assessing the effects of climate change on oceanic systems. He has previously led efforts to catalog close to 200,000 DNA and 5,500 RNA virus species found in the oceans and evaluate their potential for climate change mitigation.
For this study, Tian and Wainaina examined 7.6 terabytes of metagenomic sequence data from Tara Oceans, expanding the documented populations of oceanic DNA viruses to 579,904. The team undertook extensive computational analysis steps to pinpoint the auxiliary metabolic genes embedded in viral genomes.
They conservatively identified a total of 86,913 AMGs grouped into 22,779 sequence-based gene clusters, of which 7,248 were identified for the first time. These viruses recruit genes from the microbial cells they infect, integrating these genes into their own genomes to exploit microbial functions for their own survival.
The challenge posed by auxiliary metabolic genes lies in distinguishing between the viral versions and their microbial counterparts. “People are aware of their existence, but since the genes are often similar to the versions found in the host cells, it becomes crucial to differentiate between them,” Wainaina remarked.
“To reduce false positives, we implemented curation processes to ensure we focused solely on AMGs that were present in viral genome segments,” Tian explained.
Following this, they analyzed the genomic data further to identify metabolic pathways—action sequences that modify a cell’s functions—that were traceable to specific microbial types, resulting in the identification of 340 pathways. With the newly established catalog of “stolen” genes, the researchers found that 128 of these pathways were engaged by viral AMGs.
“That’s our significant discovery,” Tian noted. “Prior to this research, the number of metabolic pathways encoded by microbes in earth’s oceans was unknown, and even less was understood about how many were targeted by viruses through AMGs.”
“It’s not just about the quantity; it’s also crucial to identify which specific pathways viruses manipulate,” added Wainaina. “This insight informs us about the biogeochemical cycles that viruses are reshaping and influencing in the ocean.”
The catalog of AMGs and the mapping of metabolic pathways lay the groundwork for microbiome engineering experiments and models that will enable scientists to make better predictions about the role of viruses in ocean biogeochemical activities, Sullivan said.
“Currently, most models either do not account for viruses or include only a minimal representation of microbes,” he noted. “We are thrilled to have generated this data, which is vital for integrating viruses and their effects into new predictive models.”
This research received support from various entities, including the National Science Foundation, the Gordon and Betty Moore Foundation, and several other foundations and organizations.
Tian is now working as a bioinformatician at the University of Chicago, while Wainaina serves as an assistant scientist in the Biology Department at Woods Hole Oceanographic Institution. Additional contributors to this research include Cristina Howard-Varona, Guillermo DomÃnguez-Huerta, Benjamin Bolduc, Garrett Smith, Marissa Gittrich, Olivier Zablocki, and Dylan Cronin from Ohio State; Maria Consuelo Gazitúa of Viromica Consulting; Damien Eveillard from Nantes Université; and Steven Hallam from the University of British Columbia.
