Ecogenomics and cultivation reveal distinctive viral-bacterial communities in the surface microlayer of a Baltic Sea slick

Abstract

Visible surface films, termed slicks, can extensively cover freshwater and marine ecosystems, with coastal regions being particularly susceptible to their presence. The sea-surface microlayer (SML), the upper 1-mm at the air-water interface in slicks (herein slick SML) harbors a distinctive bacterial community, but generally little is known about SML viruses. Using flow cytometry, metagenomics, and cultivation, we characterized viruses and bacteria in a brackish slick SML in comparison to non-slick SML as well as seawater below slick and non-slick areas (subsurface water = SSW). Size-fractionated filtration of all samples distinguished 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. Specific metabolic profiles of bacterial metagenome-assembled genomes and isolates in the slick SML included a prevalence of genes encoding motility and carbohydrate-active enzymes (CAZymes). Several vOTUs were enriched in slick SML, and many virus variants were associated with particles. Nine vOTUs were only found in slick SML, six of them being targeted by slick SML-specific clustered-regularly interspaced short palindromic repeats (CRISPR) spacers likely originating from Gammaproteobacteria. Moreover, isolation of three previously unknown lytic phages for Alishewanella sp. and Pseudoalteromonas tunicata, abundant and actively replicating slick SML bacteria, suggests that viral activity in slicks contributes to biogeochemical cycling in coastal ecosystems.

Viral challenges and adaptations between Central Arctic Ocean and atmosphere

“…In contrast, results from Baltic Sea SML showed, that an inducible phage occurred in one of the most abundant bacterial strains, Alishewanella sp. being additionally hunted by lytic phages [108]. Flavobacteria were previously found in the SML from different oceans [109, 110], represent frequent hosts for lytic and temperate phages in the SML [108], and were important predicted viral hosts in the Arctic in this study.…”

“…being additionally hunted by lytic phages [108]. Flavobacteria were previously found in the SML from different oceans [109, 110], represent frequent hosts for lytic and temperate phages in the SML [108], and were important predicted viral hosts in the Arctic in this study. Lysogeny is often prevalent or dominant in polar environments [82, 111, 112].…”

Marine viruses disperse bidirectionally along the natural water cycle

“…Such established adaptive immunity indicates previous virus-host encounters along with viruses from rain leaving their signatures in the form of host-acquired CRISPR spacers in the sea surface and suggests that viruses are probably still infectious, i.e., can inject their genome into the host after deposition. Recent work has shown that highly populated ecosystems such as hydrothermal mats allow viruses to infect hosts across microbial domains 67 , and that virus-host interactions can be specific to the SML within visible surface films 68 . At the same time protospacers can also be incorporated from defective phages 69 , thus do not necessarily always indicate a successful replication of the virus.…”