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Ecological and metabolic roles of viruses in the ocean ecosystem

Tian, Funing
http://orcid.org/0000-0002-7217-3125
http://rave.ohiolink.edu/etdc/view?acc_num=osu1714654106604689

Abstract Details

2024, Doctor of Philosophy, Ohio State University, Microbiology.
Microbes are engines of ocean biogeochemical processes. Viruses influence and shape microbial communities via lysis, horizontal gene transfer, and metabolic reprogramming. Viral lysis facilitates the export of carbon from the surface into the deep ocean via aggregates of sinking particles. In fact, they outperform prokaryotes and eukaryotes as the strong predictor for carbon fluxes in the oligotrophic ocean. Viruses also impact the gene flow of their hosts, and the genes transferred from virus-host interactions can be fixed in viral genomes. Viruses are known to carry and express host-derived auxiliary metabolic genes (AMGs) that directly reprogram metabolisms within virus-infected cells, termed virocells. However, viral communities are poorly characterized in the oligotrophic ocean, and their AMG-driven metabolic reprogramming lacks systematic descriptions from the global oceans. The Sargasso Sea is highly stratified and nutrient-depleted each year in the summer months. This seasonal pattern makes the Sargasso Sea one of the ideal model ecosystems to study oligotrophic oceans. In the Sargasso Sea, abundance of viral-like particles has seasonal and depth-associated structuring patterns. Here, to better survey the Sargasso Sea viruses, we apply sequencing approaches to characterize viral communities via metagenomics and uncover their biogeographical and ecological structures locally and globally in the ocean. As described in Chapter 2, comparison with global viral metagenomics revealed that Sargasso Sea viruses were similar across warm oligotrophic oceanic regions but not represented globally. They form discrete populations in the viral and cellular fractions at the viral maximum (80m) and mesopelagic (200m) depths. Inclusion of long-read data captured 1,257 viral genomes in addition to the 1,044 viral genomes derived from short-read assemblies, resulting in the identification of ecologically important and microdiverse viral genomes. Having established local viral community patterns at local geographical areas, we next leveraged on 7.6 terabases of sequencing to study viral AMG-driven metabolic reprogramming throughout global oceans. Although AMGs are now known to directly reprogram photosynthesis, carbon metabolism, and nutrient cycling in the oceans, approaches to identify bona fide AMGs (not just metabolic genes on cellular contigs) and best annotate AMGs lack standards and scalability. Here, leveraging global ocean sampling efforts enabled by Tara Oceans expedition and recent analytic improvements, we seek to systematically survey AMGs in viral genomes to establish a global ocean AMG catalog. Results from this analysis are described in Chapter 3 where we expanded known ocean viral populations to 579,904 (up 16%) and from these viral populations, we identified 22,779 AMGs with 32% of AMGs reported for the first time. Estimation from observed AMG frequencies and simulated mock community predicted that 19% of ocean viral populations could encode at least one AMG. Metabolically, these AMGs mapped to 128 out of 340 metabolic pathways present in ocean microbes. We focused on nine pathways where most steps (≥0.75) were AMG-targeted, identified as metabolic ‘hot spots’ and at a high level associated with carbohydrate, amino acid, fatty acid and nucleotide metabolisms. With a global ocean AMG catalog now in-hand, we next sought to apply a statistical modeling framework to quantitatively estimate community-level metabolic properties and biogeochemical impacts of marine viruses in Chapter 4. With a supra-organism assumption that treated each collection of marine microbes within a single metagenome as a single entity, we established genome-scale metabolic models from the metagenomic and metatranscriptomic profiling of prokaryote- and virus-enriched samples. This revealed ~5K reactions across the global oceans with an average of ~4.7K reactions from any given water sample and 99% of the reactions being expressed. These reactions captured global ocean ecological patterns, with their importance within each network quantified via a synergetic score. The synergism versus autonomy of each marine ecosystem was subsequently identified. This revealed that synergetic metabolic activities were in concordance with taxonomic diversity and the Redfield ratios associated with carbon and nitrogen, but not phosphate, due to the lack of autotrophy in the models. Given that metabolic synergy ranks showed strong correlations with lyase activity, we evaluated the role of viruses within the metabolic networks and found significant associations of AMGs with important reactions involved in purine, pyrimidine, and one-carbon metabolisms. Together, these findings present an extensive expansion of our current understanding of marine viral communities in the oligotrophic ocean, their metabolic reprogramming potential through AMGs globally, and the contribution of viruses within a statistical modeling framework via AMGs, thus providing valuable insights into the role of viruses in biogeochemistry.
Matthew Sullivan (Advisor)
Joseph Tien (Committee Member)
Virginia Rich (Committee Member)
Igor Jouline (Committee Member)
207 p.
Biogeochemistry; Bioinformatics; Biological Oceanography; Biology; Climate Change; Ecology; Environmental Science; Microbiology; Statistics; Virology
viruses; metagenomics; metatranscriptomics; genome-scale metabolic modeling; community ecology; marine biology

Recommended Citations

Citations

  • Tian, F. (2024). Ecological and metabolic roles of viruses in the ocean ecosystem [Doctoral dissertation, Ohio State University]. OhioLINK Electronic Theses and Dissertations Center. http://rave.ohiolink.edu/etdc/view?acc_num=osu1714654106604689

    APA Style (7th edition)

  • Tian, Funing. Ecological and metabolic roles of viruses in the ocean ecosystem. 2024. Ohio State University, Doctoral dissertation. OhioLINK Electronic Theses and Dissertations Center, http://rave.ohiolink.edu/etdc/view?acc_num=osu1714654106604689.

    MLA Style (8th edition)

  • Tian, Funing. "Ecological and metabolic roles of viruses in the ocean ecosystem." Doctoral dissertation, Ohio State University, 2024. http://rave.ohiolink.edu/etdc/view?acc_num=osu1714654106604689

    Chicago Manual of Style (17th edition)

osu1714654106604689
© 2024, all rights reserved.
This open access ETD is published by The Ohio State University and OhioLINK.