Biological composition and microbial dynamics of sinking particulate organic matter at abyssal depths in the oligotrophic open ocean

Abstract

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.

Major imprint of surface plankton on deep ocean prokaryotic structure and activity

“…The stations sampled covered a relatively wide gradient of surface conditions and average productivity levels across the subtropical and tropical waters, since they belonged to seven different Longhurst provinces (Longhurst, 1998). This was reflected in variations in the abundances of surface micro‐, nano‐ and pico‐photosynthetic and heterotrophic organisms, which probably translated into diverse food‐web structures and interactions that ultimately modulate the export fluxes and the nature of the sinking particles reaching the deep ocean (Bach et al., 2016; Boeuf et al., 2019; Guidi et al., 2009; Stukel et al., 2011).…”

“…For instance, a dominance of dinoflagellates, ciliates and nanoflagellates may represent mature communities for which some export had already occurred (Hansen, Ohde, & Wasmund, 2014; Schmoker, Ojeda, & Hernández‐Leon, 2014), or assemblages where intense particle production as zooplankton faecal pellets is occurring (Wiedmann, Reich, Reigstad, Sundfjord, & Basedow, 2014). In any case, nanoflagellates, ciliates or dinoflagellates have also been found in sediment traps deployed at depth (Amacher et al., 2009; Boeuf et al., 2019; Fontánez et al., 2015; Gutiérrez‐Rodríguez et al, 2019), and photosynthetic dinoflagellates represented more than 60% of the autotrophic microplankton sampled in the bathypelagic ocean in some areas of the North Atlantic and Indian Ocean during our expedition (Agustí et al., 2015). We thus cannot discard a direct contribution of these plankton groups in the downward transport of prokaryotic diversity across the global oligotrophic ocean.…”

“…The amount, quality, size and sinking rates of the particles leaving the photic ocean are ultimately determined by the community structure of phytoplankton and other food web processes such as grazing (Bach et al., 2019; Boyd & Newton, 1995; Guidi et al., 2009; Laurenceau‐Cornec, Trull, Davies, De la Rocha, & Blain, 2015; Stukel, Landry, Benitez‐Nelson, & Goericke, 2011). For example, diatoms and mesozooplankton are considered main drivers of carbon export due to fast sinking rates of large cells or dense faecal pellets, respectively (Agustí et al., 2015; Al‐Mutairi & Landry, 2001; Boyd & Newton, 1995; Fender et al., 2019; Stukel et al., 2011), but multiple studies have unveiled that groups such as picoeukaryotes, radiolarians, ciliates, dinoflagellates and even picocyanobacteria can also be delivered at depth, probably as fast‐sinking aggregates (Agustí et al., 2015; Amacher, Anderson, & Massana, 2009; Boeuf et al., 2019; Fontánez, Eppley, Samo, Karl, & DeLong, 2015; Guidi et al., 2016; Gutiérrez‐Rodríguez et al., 2019; Lundgreen et al., 2019). Epipelagic planktonic assemblages may thus shape bathypelagic microbial communities by determining the quality and amount of the exported materials; for example, nutrients deriving from sinking particles were suggested to explain the propagation of temporal patterns in free‐living microbial community composition between surface and mesopelagic waters (Cram, Xia, et al, 2015; Parada & Furhman, 2017).…”

“…In fact, a global bathypelagic survey conducted during the Malaspina expedition (Salazar, Cornejo‐Castillo, Benítez‐Barrios, et al, 2015) did not find evidence that deep‐sea prokaryotic assemblages differed among Longhurst biogeographic provinces, characterized by different phytoplankton communities (Longhurst, 1998), although they did not consider the environmental conditions associated to each province and targeted communities from two small size‐fractions potentially less prone to sink (0.2–0.8 µm and 0.8–20 µm; Salazar, Cornejo‐Castillo, Benítez‐Barrios, et al, 2015). In addition, microbial communities in the deep ocean may no longer reflect the original surface processes delivering the particles if the attached microbial communities change during sinking, or if the local bathypelagic physicochemistry plays a larger role in species sorting than the arriving material (Boeuf et al., 2019; Datta, Sliwerska, Gore, Polz, & Cordero, 2016; Pelve, Fontánez, & DeLong, 2017). Finally, the prevalence of autotrophic metabolisms among bathypelagic prokaryotes (Acinas et al, 2019; Pachiadaki et al., 2017; Swan et al., 2011), or the ability to use recalcitrant organic matter derived from old particles (Landry, Swan, Herndl, Stepanauskas, & Giovannoni, 2017), could also lead to an apparent decoupling of bathypelagic microbial community structure from surface processes.…”

Reviews and syntheses: Bacterial bioluminescence – ecology and impact in the biological carbon pump

“…In order to efficiently describe bioluminescent or non-bioluminescent bacteria, the description at the species level is a strong requirement. As an example, Vibrio are important contributors to particulate organic carbon fluxes that have been observed at abyssal depths in the Pacific Ocean (Preston et al, 2019, Boeuf et al, 2019. A better characterization at species or functional level should highlight the luminous potential related to the presence of such organisms, even at low abundance.…”