Virus-mediated recycling of chemoautotrophic biomass

Abstract

Aquatic environments absorb [~]2.5 gigatonnes of atmospheric carbon each year1, more than the carbon stored in the atmosphere, soils, and all biomass combined. Primary producers transform this dissolved inorganic carbon into biomass that can subsequently flow into other trophic levels, or be released back into the environment through viral lysis. While there is substantial knowledge about the diversity and activity of viruses infecting photoautotrophic primary producers, little is known about viruses infecting chemoautotrophs, representing a gap in our understanding of key microbial processes driving global carbon cycles. Here, we combine metagenomics with 12/13C stable isotopic probing mesocosm experiments in a marine-derived meromictic pond to quantify lineage-specific carbon cycling activity to identify key microbial populations driving carbon cycling. We then tracked the flow of carbon from active chemoautotrophs to their viruses and found evidence supporting virus-mediated recycling of chemoautotrophic biomass through the production of viral particles. In particular, active populations of hydrogen/sulfur-oxidizing chemoautotrophs (Thiomicrorhabdus, Hydrogenovibrio, Sulfurimonas, Sulfurovum) were targeted by viruses. Considering the widespread distribution of chemoautotrophs on Earth, we postulate that this previously overlooked component of the microbial carbon cycle is a globally relevant process that has implications for our planets carbon cycle. This work provides the foundation for revealing the role of viral lysis in chemoautotrophic primary production and builds toward biogeochemical models that incorporate viral recycling of chemoautotrophic biomass. Summary statementThe diversity, mechanisms, and processes governing microbial primary production and the recycling of autotrophic biomass are fundamental to our planets carbon cycle. These processes have implications for carbon sequestration, ocean biogeochemistry, and the overall balance of carbon dioxide in the atmosphere. Beneath the Earths sunlit layer, primary production is driven by microbial chemoautotrophs that derive energy from the oxidation of reduced compounds, such as hydrogen and sulfur, to form the base of the food web. Growing evidence suggests that aquatic ecosystems fueled by chemoautotrophy are widely distributed on Earth, ranging from beneath ice shelves to coastal upwelling regions to oxygen minimum zones, deep-sea hydrothermal vents and cold seeps, groundwater, and meromictic ponds and lakes2-7. Studying microbial processes regulating chemoautotrophic primary production and the recycling of chemoautotrophic biomass is fundamental to our understanding of global carbon cycles. While the diversity, function, and activity of viruses targeting photoautotrophs have been well-described across aquatic ecosystems8, we have little understanding of viruses involved in the recycling of chemoautotrophic biomass. Viruses are a major source of cellular mortality and carbon cycling in aquatic environments9-11. Viral lysis is estimated to transform [~]150 gigatonnes of carbon annually from biomass back into the environment, equivalent to [~]25 times that of the oceans biological carbon pump12,13. Despite recognition of the important role of viruses in aquatic habitats, there is a large gap in our understanding of the impact of viruses on globally distributed chemoautotrophs2,4,5,14-18. In this study, we show that viruses are not merely passive players but active agents recycling carbon fixed by productive chemoautotrophs, fundamentally reshaping how we view carbon and nutrient cycling in redox-active ecosystems.