Appearance of viral genomes with high GC base proportion in atmospheric samples from Europe and Antarctica

Outdoor viruses from atmospheric ecosystems have rarely been investigated, and thus only a few viral genomes from the air can be found in public databases. Viruses and their hosts have positively correlating guanine-cytosine (GC) contents in their DNA¹. High GC content was previously found in actinobacterial and betaproteobacterial isolates from the stratosphere² as well as in aerosol and rainwater viruses³. This is proposed as an adaptation to harsh environmental conditions, primarily as protection against ultraviolet radiation. Here, we combine metagenomically derived viral operational taxonomic units (vOTUs) collected from aerosols and precipitation samples from the Swedish coast³, along with time-series data collected in Antarctica using different sampling devices. Additionally, cloud water samples from the Puy de Dôme in France⁴ were included. A total of 80 assembled vOTUs, of which 37 were predicted phages, across all samples, had a GC content between 55.2% and 70.3%, considered 'high GC.' Antarctic air vOTUs were found after sampling with the Coriolis µ (wet) but not with the Coriolis Compact (dry) air sampler. The time series indicates overlapping vOTUs between days and sampling height (sea-level or altitude). In Antarctic air, high GC vOTUs (mean GC = 59.6% ± 4.0) were detected on one of the seven days, while low GC viruses were absent in this sample. On other days, the GC of vOTUs was <39%. Thirteen high GC vOTUs from Sweden and Antarctica clustered in a proteomic tree analysis with known high GC phage isolates infecting Microbacterium radiodurans and Arthrobacter sp. (both phylum Actinomycetota). Host predictions using iPHoP revealed that only 11 of the 80 vOTUs could be assigned to bacterial hosts with good confidence, namely to genera Mycobacterium, Ralstonia, Sphingomonas, and Bradyrhizobium. Our results suggest that high GC is a feature in air viruses from different atmospheric sources and latitudes. While these vOTUs occur irregularly at near-ground sampling heights, a high GC content could favor the survival of airborne viruses higher in the troposphere and thus enable infections of extremophilic hosts within air ecosystems.

References:

¹ Simón, D., Cristina, J., & Musto, H. (2021). Nucleotide composition and codon usage across viruses and their respective hosts. Frontiers in Microbiology, 12, 646300.

² Ellington, A. J., Bryan, N. C., Christner, B. C., & Reisch, C. R. (2021). Draft Genome Sequences of Actinobacterial and Betaproteobacterial Strains Isolated from the Stratosphere. Microbiology Resource Announcements, 10(50), e01009-21.

³ Rahlff, J., Esser, S.P., Plewka, J., Heinrichs, M.E., Soares, A., Scarchilli, C., Grigioni, P., Wex, H., Giebel, H.A. and Probst, A.J., 2023. Marine viruses disperse bidirectionally along the natural water cycle. Nature Communications, 14(1), p.6354.

⁴ Dillon, K. P., Correa, F., Judon, C., Sancelme, M., Fennell, D. E., Delort, A. M., & Amato, P. (2020). Cyanobacteria and Algae in Clouds and Rain in the Area of puy de Dôme, Central France. Applied and Environmental Microbiology, 87(1), e01850-20.