Sinking particles are a critical conduit for the export of organic material from surface waters to the deep ocean. Despite their importance in oceanic carbon cycling and export, little is known about the biotic composition, origins, and variability of sinking particles reaching abyssal depths. Here, we analyzed particle-associated nucleic acids captured and preserved in sediment traps at 4,000-m depth in the North Pacific Subtropical Gyre. Over the 9-month time-series, Bacteria dominated both the rRNA-gene and rRNA pools, followed by eukaryotes (protists and animals) and trace amounts of Archaea. Deep-sea piezophile-like Gammaproteobacteria, along with Epsilonproteobacteria, comprised >80% of the bacterial inventory. Protists (mostly Rhizaria, Syndinales, and ciliates) and metazoa (predominantly pelagic mollusks and cnidarians) were the most common sinking particle-associated eukaryotes. Some near-surface water-derived eukaryotes, especially Foraminifera, Radiolaria, and pteropods, varied greatly in their abundance patterns, presumably due to sporadic export events. The dominance of piezophile-like Gammaproteobacteria and Epsilonproteobacteria, along with the prevalence of their nitrogen cycling-associated gene transcripts, suggested a central role for these bacteria in the mineralization and biogeochemical transformation of sinking particulate organic matter in the deep ocean. Our data also reflected several different modes of particle export dynamics, including summer export, more stochastic inputs from the upper water column by protists and pteropods, and contributions from sinking mid- and deep-water organisms. In total, our observations revealed the variable and heterogeneous biological origins and microbial activities of sinking particles that connect their downward transport, transformation, and degradation to deep-sea biogeochemical processes.

SignificanceMarine microbial communities exert a large influence on ocean ecosystem processes, and viruses in these communities play key roles in controlling microbial abundances, nutrient cycling, and productivity. We show here that dominant viruses in the open ocean persist for long time periods and that many appear tightly locked in coordinated diel oscillations with their bacterial hosts. The persistent structure of viral assemblages, as well as synchronized daily oscillations of viruses and hosts, are in part the result of the regular diurnal coupling of viral and host replication cycles. Collectively, our results suggest that viruses, as key components of marine ecosystems, are intrinsically synchronized with the daily rhythms of microbial community processes in the ocean’s photic zone.

Proteorhodopsin is a light-activated retinal-containing proton pump found in many marine bacteria. These photoproteins are globally distributed in the ocean’s photic zone and are capable of generating a proton motive force across the cell membrane. We investigated the phylogenetic diversity, distribution, and abundance of proteorhodopsin encoding genes in free-living bacterioplankton in the North Pacific Subtropical Gyre, leveraging a gene catalog derived from metagenomic samples from the ocean’s surface to 1000 m depth. Proteorhodopsin genes were identified at all depths sampled, but were most abundant at depths shallower than 200 m. The majority of proteorhodopsin gene sequences (60.9%) belonged to members of the SAR11 lineage, with remaining sequences distributed among other diverse taxa. We observed variations in the conserved residues involved in ion pumping and spectral tuning, and biochemically confirmed four different proton pumping proteorhodopsin motifs, including one unique to deep-water SAR11. We also identified a new group of putative proteorhodopsins having unknown function. Our results reveal a broad organismal and unexpected depth distribution for different proteorhodopsin types, as well as substantial within-taxon variability. These data provide a framework for exploring the ecological relevance of proteorhodopsins and their spatiotemporal variation and function in heterotrophic bacteria in the open ocean.

Aerobic anoxygenic phototrophic (AAP) bacteria are found in a range of aquatic and terrestrial environments, potentially playing unique roles in biogeochemical cycles. Although known to occur in the Arctic Ocean, their ecology and the factors that govern their community structure and distribution in this extreme environment are poorly understood. Here, we examined summer AAP abundance and diversity in the North East Pacific and the Arctic Ocean with emphasis on the southern Beaufort Sea. AAP bacteria comprised up to 10 and 14% of the prokaryotic community in the bottom nepheloid layer and surface waters of the Mackenzie plume, respectively. However, relative AAP abundances were low in offshore waters. Environmental pufM clone libraries revealed that AAP bacteria in the Alphaproteobacteria and Betaproteobacteria classes dominated in offshore and in river-influenced surface waters, respectively. The most frequent AAP group was a new uncultivated betaproteobacterial clade whose abundance decreased along the salinity gradient of the Mackenzie plume even though its photosynthetic genes were actively expressed in offshore waters. Our data indicate that AAP bacterial assemblages represented a mixture of freshwater and marine taxa mostly restricted to the Arctic Ocean and highlight the substantial influence of riverine inputs on their distribution in coastal environments.