Ecogenomics reveals distinctive viral-bacterial communities in the surface microlayer of a natural surface slick

Visible surface films, termed slicks, can extensively cover the sea surface, particularly in coastal regions. The sea-surface microlayer (SML), the upper 1-mm at the air-water interface in slicks (slick SML) harbors a distinctive bacterial community, but little is known about SML viruses. Using flow cytometry, metagenomics, and cultivation, we investigated viruses and the bacterial community from a brackish slick SML in comparison to non-slick SML as well as the seawater below (SSW). We conducted size-fractionated filtration of all samples to distinguish viral attachment to hosts and particles. The slick SML contained higher abundances of virus-like particles, prokaryotic cells, and dissolved organic carbon compared to non-slick SML and SSW. The community of 428 viral operational taxonomic units (vOTUs), 426 predicted as lytic, distinctly differed across all size fractions in the slick SML compared to non-slick SML and SSW. The distinctness was underlined by specific metabolic profiles of bacterial metagenome assembled genomes and isolates, which revealed prevalence of motility genes and diversity of CAZymes in the slick SML. Despite overall lower diversity, several vOTUs were enriched in slick SML over slick SSW. Nine vOTUs were only found in slick SML and six of them were targeted by slick SML-specific CRISPR spacers likely originating from Gammaproteobacteria. Moreover, isolation of three previously unknown lytic phages for Alishewanella sp. and Pseudoalteromonas tunicata, representing abundant and actively replicating slick SML bacteria, suggests that viral activity in slicks can contribute to biogeochemical cycling in coastal ecosystems.