Diversity Patterns and Ecological Footprint of RNA Viruses Along a Permafrost Thaw Gradient
Authors:
Akbar Adjie Pratama1*, Guillermo Dominguez-Huerta1*, Ahmed A. Zayed1, James M. Wainaina1, Benjamin Bolduc1, Funing Tian1, Jared Ellenbogen2, Jiarong Guo1, EMERGE Biology Integration Institute Team1, EMERGE Coordinators1, Kelly C. Wrighton2, and Matthew B. Sullivan1
Institutions:
1The Ohio State University and 2Colorado State University
Goals
The overarching goal of this project is to establish ecological paradigms for how viruses alter soil microbiomes and nutrient cycles by developing foundational (eco)systems biology approaches for soil viruses. Specifically, this study aims to establish a fundamental knowledge of RNA viruses in permafrost regions and provide a comprehensive framework for understanding their complex interactions with hosts and the environment. To achieve this, the team will investigate the diversity and distribution of RNA viruses. In addition, to investigate their ecological impact, team members will examine the virus-host dynamics and evolution and identify the occurrence of auxiliary metabolic genes in RNA viruses. Ultimately, this research can significantly contribute to the integration of RNA viruses into the ecosystem and climate-related models.
Abstract
As global atmospheric temperatures rise, sequestered permafrost soil carbon may be released via microorganismal activity, which can lead to a positive feedback loop effectively speeding up greenhouse gas emissions and climate change. While data are emerging about how prokaryotes and their DNA viruses may respond to permafrost thaw, the role of RNA viruses that infect soil eukaryotes remains less clear even though they may be important for nutrient cycling as demonstrated previously for the global oceans (Zayed et al. 2022; Dominguez-Huerta et al. 2022) and a diversity of forest, mountain, semi- desert, agricultural and sedimentary soils (Chen et al. 2022). Here team members leverage 55 metatranscriptomes (630 gigabases) collected along a permafrost thaw gradient in the model ecosystem Stordalen Mire to identify, quantify, and ecologically contextualize RNA viruses in these soils. Application of analytical approaches optimized for maximal sensitivity and largely automated systematic classification to these data identified 2,651 species-like RNA virus taxa. Though most of these species derive from the five known established phyla (Wolf et al. 2018), including one vOTUs in the recently suggested phylum Taraviricota (Zayed et al. 2022), nearly all represent novel species within these higher taxa and five likely represent a novel class in the phylum Lenarviricota (proposed name, “Stomiviricetes”). Ecological analyses of the approximately species-level taxa revealed strong habitat specificity as well as depth trends where RNA virus diversity decreased with depth. To assess the ecological footprint of Stordalen Mire RNA viruses, team members predicted hosts and evaluated gene content. This revealed that most (68%) likely infect key nutrient cycling eukaryotes that span multiple levels in the food web (only a few percent RNA viruses were predicted to infect prokaryotes), as well as 96 that carried virus-encoded auxiliary metabolic genes hinting at metabolic reprogramming of miscellaneous metabolic pathways, cellular and molecular processes, such as transport, transcription, countering antiviral defense, and coping to environmental stress. Together these findings provide baseline RNA virus diversity and ecology data and tantalizing hints at ecosystem impacts that establish fundamental knowledge for integrating them into predictive ecological models in the rapidly changing Arctic environment.
References
Chen, Y., et al. 2022. “RNA Viromes from Terrestrial Sites Across China Expand Environmental Viral Diversity,” Nat. Microbiol. 7, 1312–23.
Dominguez-Huerta, G., et al. 2022. “Diversity and Ecological Footprint of Global Ocean RNA Viruses,” Science 80(1208), 1202–08.
Wolf, Y. I. et al. 2018. “ Origins and Evolution of the Global RNA Virome,” MBio 9, 1–31.
Zayed, A. A. et al. 2022. “Cryptic and Abundant Marine Viruses at the Evolutionary Origins of Earth’s RNA Virome,” Science 80(376), 156–62.