Viruses at the air-water boundary and in the atmosphere: insights from metagenomics
Centre for Ecology and Evolution in Microbial Model Systems (EEMiS), Department of Biology and Environmental Science, Linnaeus University
Group for Aquatic Microbial Ecology, University of Duisburg-Essen, Department of Chemistry, Environmental Microbiology and Biotechnology (EMB)
Prokaryotic viruses have key impacts in regulating microbial communities in marine ecosystems, from the deep sea to the surface ocean. However, little is known about neustonic viruses residing in the ocean’s skin, the 1 mm thin sea-surface microlayer, especially within visible surface films (“slicks”) that occur in high frequency in coastal regions and viral exchange with the atmosphere. In this study, we collected seawater, microlayer (inside and outside a slick), sea foams, aerosols, and rain to metagenomically investigate viral communities and their dispersal. We found that microlayer from a brackish surface slick, which was highly enriched in surface-active molecules and virus-like particles, harbors distinctive bacteriophage communities. Despite viral communities of the microlayer from a slick having an overall lower Shannon-Wiener diversity, certain viral clusters for instance of flavobacterial phages are particularly abundant in slicks, and slick viruses are equipped with auxiliary metabolic genes, e.g., related to nucleotide synthesis or carbohydrate metabolism. Slick phage isolates are morphologically diverse, show a narrow host range, and infect abundant and actively replicating Gammaproteobacteria, such as particle-associated Alishewanella sp. and Rheinheimera baltica as well as free-living Pseudoaltermonas tunicata. Across 55 metagenomes from marine and air ecosystems sampled in a coastal region of the Skagerrak in Sweden, 1813 viral scaffolds were recovered, and read mapping revealed a virome overlap of 6.2% between rain and marine samples. Variant analysis of a potential Porticoccaceae virus provides evidence for viral dispersal from sea foams to aerosols and rain. Foams as the “hyperneuston” were particularly enriched in virus-like particles. Analysis of air mass trajectories support long-range transport of marine microbes and viruses from the Atlantic Ocean to the Swedish coast, where they are deposited with precipitation. Rain additionally contained 109 viruses that were unique to this ecosystem and mostly unrelated to RefSeq database viruses. Viral scaffolds unique to rain and aerosols had a significantly higher G/C base content compared to marine counterparts suggesting a genetic adaptation for atmospheric residence. Yet, targeting by the adaptive immune system of sea surface prokaryotes indicates previous encounters of marine hosts with the peculiar rain viruses. Our findings demonstrate that lytic viral lifestyle at the air-sea interface is common and that particularly slicks can be hotspots for the viral shunt and thus influence carbon cycling. Moreover, our data support bidirectional dispersal of viruses across the air-sea interface allowing to infer viral distribution on a large spatial scale.