Ocean-wide comparisons of mesopelagic planktonic community structures

Abstract

For decades, marine plankton have been investigated for their capacity to modulate biogeochemical cycles and provide fishery resources. Between the sunlit (epipelagic) layer and the deep dark waters, lies a vast and heterogeneous part of the ocean: the mesopelagic zone. How plankton composition is shaped by environment has been well-explored in the epipelagic but much less in the mesopelagic ocean. Here, we conducted comparative analyses of trans-kingdom community assemblages thriving in the mesopelagic oxygen minimum zone (OMZ), mesopelagic oxic, and their epipelagic counterparts. We identified nine distinct types of intermediate water masses that correlate with variation in mesopelagic community composition. Furthermore, oxygen, NO₃^- and particle flux together appeared as the main drivers governing these communities. Novel taxonomic signatures emerged from OMZ while a global co-occurrence network analysis showed that about 70% of the abundance of mesopelagic plankton groups is organized into three community modules. One module gathers prokaryotes, pico-eukaryotes and Nucleo-Cytoplasmic Large DNA Viruses (NCLDV) from oxic regions, and the two other modules are enriched in OMZ prokaryotes and OMZ pico-eukaryotes, respectively. We hypothesize that OMZ conditions led to a diversification of ecological niches, and thus communities, due to selective pressure from limited resources. Our study further clarifies the interplay between environmental factors in the mesopelagic oxic and OMZ, and the compositional features of communities.

Fig. 1. Geographical locations of Tara Oceans epipelagic and mesopelagic sampling sites included in this study.

Symbol colors represent organism groups evaluated in the present study. Shape formats represent eco-regions, Epipelagic, Oxic MES = oxicmesopelagic, OMZ = oxygen minimum zone mesopelagic.

Fig. 2. Ordination plot of canonical correspondence analysis (CCA) from epipelagic (left) and mesopelagic (right) communities based on OTU composition.

Percentages in parentheses are the amount of variation constrained - in titles represent the total in each analysis, and in the axis represent the correspondent value for each dimension. Arrows represent environmental quantitative explanatory variables with arrowheads indicating their direction of increase. Shapes represent sampling sites. Shape formats represent eco-regions, epi epipelagic, Oxic MES oxic mesopelagic, OMZ oxygen minimum zone mesopelagic. IO Indian Ocean, NAO North Atlantic Ocean, NPO North Pacific Ocean, SAO South Atlantic Ocean, SPO South Pacific Ocean.

Fig. 3. Temperature and salinity plot indicating water mass designation for all mesopelagic samples.

Formats represent the different oceanic basins (■ - North Atlantic Ocean, ● - South Atlantic Ocean, ▲- Pacific Ocean, ★- Indian Ocean). Colors indicate the oxygen concentration at the sampling depth. LSW Labrador Sea Water, AAIW Antarctic Intermediate Water, tNPIW transitional North Pacific Intermediate Water, SAMW Subantarctic Mode Water, SPSTMW South Pacific Subtropical Mode Water, modAAIW modified Antarctic Intermediate Water, PGW Persian Gulf Water mass, RSW Red Sea Water mass, NASTMW North Atlantic Subtropical Mode Water.

Fig. 4. Heatmaps occurrence of OTUs assigned to mesopelagic eco-regions.

A Phages, B NCLDV, C Prokaryotes and D pico-Eukaryotes.

Fig. 5. Co-occurrence network in epipelagic and mesopelagic communities.

A Global network, with connected modules for OMZ (purple and orange) and Oxic MES (green) highlighted. B Relative taxa abundance in each module in each station and depth. C Relative number of OTUs classified in taxonomic groups. D Network representation of modules.