The deep-sea is the largest biome of the biosphere, and contains more than half of the whole ocean’s microbes. Uncovering their general patterns of diversity and community structure at a global scale remains a great challenge, as only fragmentary information of deep-sea microbial diversity exists based on regional-scale studies. Here we report the first globally comprehensive survey of the prokaryotic communities inhabiting the bathypelagic ocean using high-throughput sequencing of the 16S rRNA gene. This work identifies the dominant prokaryotes in the pelagic deep ocean and reveals that 50% of the operational taxonomic units (OTUs) belong to previously unknown prokaryotic taxa, most of which are rare and appear in just a few samples. We show that whereas the local richness of communities is comparable to that observed in previous regional studies, the global pool of prokaryotic taxa detected is modest (~3600 OTUs), as a high proportion of OTUs are shared among samples. The water masses appear to act as clear drivers of the geographical distribution of both particle-attached and free-living prokaryotes. In addition, we show that the deep-oceanic basins in which the bathypelagic realm is divided contain different particle-attached (but not free-living) microbial communities. The combination of the aging of the water masses and a lack of complete dispersal are identified as the main drivers for this biogeographical pattern. All together, we identify the potential of the deep ocean as a reservoir of still unknown biological diversity with a higher degree of spatial complexity than hitherto considered.

Recent studies suggest that previous estimates of mesopelagic biomasses are severely biased, with the new, higher estimates underlining the need to unveil behaviourally mediated coupling between shallow and deep ocean habitats. We analysed vertical distribution and diel vertical migration (DVM) of mesopelagic acoustic scattering layers (SLs) recorded at 38 kHz across oceanographic regimes encountered during the circumglobal Malaspina expedition. Mesopelagic SLs were observed in all areas covered, but vertical distributions and DVM patterns varied markedly. The distribution of mesopelagic backscatter was deepest in the southern Indian Ocean (weighted mean daytime depth: WMD 590 m) and shallowest at the oxygen minimum zone in the eastern Pacific (WMD 350 m). DVM was evident in all areas covered, on average ~50% of mesopelagic backscatter made daily excursions from mesopelagic depths to shallow waters. There were marked differences in migrating proportions between the regions, ranging from ~20% in the Indian Ocean to ~90% in the Eastern Pacific. Overall the data suggest strong spatial gradients in mesopelagic DVM patterns, with implied ecological and biogeochemical consequences. Our results suggest that parts of this spatial variability can be explained by horizontal patterns in physical-chemical properties of water masses, such as oxygen, temperature and turbidity.

The atmosphere plays a fundamental role in the transport of microbes across the planet but it is often neglected as a microbial habitat. Although the ocean represents two thirds of the Earth’s surface, there is little information on the atmospheric microbial load over the open ocean. Here we provide a global estimate of microbial loads and air-sea exchanges over the tropical and subtropical oceans based on the data collected along the Malaspina 2010 Circumnavigation Expedition. Total loads of airborne prokaryotes and eukaryotes were estimated at 2.2 × 10²¹ and 2.1 × 10²¹ cells, respectively. Overall 33–68% of these microorganisms could be traced to a marine origin, being transported thousands of kilometres before re-entering the ocean. Moreover, our results show a substantial load of terrestrial microbes transported over the oceans, with abundances declining exponentially with distance from land and indicate that islands may act as stepping stones facilitating the transoceanic transport of terrestrial microbes.

Global patterns of planktonic diversity are mainly determined by the dispersal of propagules with ocean currents. However, the role that abundance and body size play in determining spatial patterns of diversity remains unclear. Here we analyse spatial community structure - β-diversity - for several planktonic and nektonic organisms from prokaryotes to small mesopelagic fishes collected during the Malaspina 2010 Expedition. β-diversity was compared to surface ocean transit times derived from a global circulation model, revealing a significant negative relationship that is stronger than environmental differences. Estimated dispersal scales for different groups show a negative correlation with body size, where less abundant large-bodied communities have significantly shorter dispersal scales and larger species spatial turnover rates than more abundant small-bodied plankton. Our results confirm that the dispersal scale of planktonic and micro-nektonic organisms is determined by local abundance, which scales with body size, ultimately setting global spatial patterns of diversity.

The biological pump transports organic carbon produced by photosynthesis to the meso- and bathypelagic zones, the latter removing carbon from exchanging with the atmosphere over centennial time scales. Organisms living in both zones are supported by a passive flux of particles, and carbon transported to the deep-sea through vertical zooplankton migrations. Here we report globally-coherent positive relationships between zooplankton biomass in the epi-, meso-, and bathypelagic layers and average net primary production (NPP). We do so based on a global assessment of available deep-sea zooplankton biomass data and large-scale estimates of average NPP. The relationships obtained imply that increased NPP leads to enhanced transference of organic carbon to the deep ocean. Estimated remineralization from respiration rates by deep-sea zooplankton requires a minimum supply of 0.44 Pg C y⁻¹ transported into the bathypelagic ocean, comparable to the passive carbon sequestration. We suggest that the global coupling between NPP and bathypelagic zooplankton biomass must be also supported by an active transport mechanism associated to vertical zooplankton migration.

The shallow submarine eruption which took place in October 10^th 2011, 1.8 km south of the island of El Hierro (Canary Islands) allowed the study of the abrupt changes in the physical-chemical properties of seawater caused by volcanic discharges. In order to monitor the evolution of these changes, seven oceanographic surveys were carried out over six months (November 2011-April 2012) from the beginning of the eruptive stage to the post-eruptive phase. Here, we present dramatic changes in the water column chemistry including large decreases in pH, striking effects on the carbonate system, decreases in the oxygen concentrations and enrichment of Fe(II) and nutrients. Our findings highlight that the same volcano which was responsible for the creation of a highly corrosive environment, affecting marine biota, has also provided the nutrients required for the rapid recuperation of the marine ecosystem.