Sea foams are ephemeral hotspots for distinctive bacterial communities contrasting sea-surface microlayer and underlying surface water

Abstract

The occurrence of foams at oceans' surfaces is patchy and generally short-lived, but a detailed understanding of bacterial communities inhabiting sea foams is lacking. Here, we investigated how marine foams differ from the sea-surface microlayer (SML), a <1-mm-thick layer at the air-sea interface, and underlying water from 1 m depth. Samples of sea foams, SML and underlying water collected from the North Sea and Timor Sea indicated that foams were often characterized by a high abundance of small eukaryotic phototrophic and prokaryotic cells as well as a high concentration of surface-active substances (SAS). Amplicon sequencing of 16S rRNA (gene) revealed distinctive foam bacterial communities compared with SML and underlying water, with high abundance of Gammaproteobacteria. Typical SML dwellers such as Pseudoalteromonas and Vibrio were highly abundant, active foam inhabitants and thus might enhance foam formation and stability by producing SAS. Despite a clear difference in the overall bacterial community composition between foam and SML, the presence of SML bacteria in foams supports the previous assumption that foam is strongly influenced by the SML. We conclude that active and abundant bacteria from interfacial habitats potentially contribute to foam formation and stability, carbon cycling and air-sea exchange processes in the ocean.

Keywords: 16S rRNA amplicon sequencing; air–sea interface; neuston; particles; surfactants.

Figure 1.

Marine foam originating from (A) presumptive phytoplankton exudates (Jade Bay), (B)Trichodesmium bloom (Timor Sea) and (C) whitecaps produced by convergence of surface water (Jade Bay, North Sea).

Figure 2.

Absolute cell counts mL⁻¹ for (A) prokaryotes and (B) small eukaryotic phototrophic cells and (C) concentration of SAS in µg Teq L⁻¹ for foam, SML and ULW. Foam samples from the North Sea, NS_FO1_210416 and NS_FO2_210416, were produced by waves, whereas NS_FO1_190516, NS_FO2_190516 and NS_FO1_190716 are foams likely derived from phytoplankton exudates. Foams from the Timor Sea (TS) originated from a Trichodesmium sp. bloom.

Figure 3.

(A) 16S rRNA and 16S rRNA gene-derived numbers of OTUs for foam, SML and ULW habitat of pooled North Sea stations. The total number of OTUs of the three habitats is further distinguished between free-living (FL) and particle-associated (PA) bacterial communities. Grey and black lines indicate inter- and intrahabitat comparisons, respectively. The box plot shows the 25–75% quartiles; the median is indicated by the horizontal line inside the box. Error bars show minimal and maximal values. Asterisks indicate the level of significant differences: *P ≤ 0.05, **P ≤ 0.01; for reasons of the different number of observations (n), see Table S1 (Supporting Information) and for all statistical results, see Table S2 (Supporting Information). (B) Venn diagram showing overlapping and unique OTUs for foam, SML and ULW separated by free-living and particle-associated OTUs.

Figure 4.

NMDS plot shows distinct clustering of foam (red), SML (blue) and underlying water (green) based on total (squares) and active (circles) bacterial communities. Further separation of communities into (A) 16S rRNA-based with free-living (open symbols) and particle-associated (filled symbols) stress = 0.14; (B) 16S rRNA gene-based with free-living (open symbols) and particle-associated (filled symbols) stress = 0.11.

Figure 5.

Composition of phylum level of foam, SML and ULW samples of 16S rRNA and 16S rRNA gene-based relative abundance of OTUs of pooled North Sea stations. Each habitat is further separated into free-living (FL) and particle-associated (PA) bacterial communities. Dashed lines separate foam from SML and ULW.

Figure 6.

Heat map showing OTUs with significant different relative abundance in foam, SML and ULW based on LEfSe analysis from pooled North Sea samples; OTUs are derived from sequencing amplicons derived from 16S rRNA and its gene. The vertical axis indicates the key species for these three biomes, respectively, while the horizontal axis shows how abundant these key OTUs were in the other two habitats. Dashed lines separate foam from SML and ULW.