skip to main content


Title: Vertical community patterns of Labyrinthulomycetes protists reveal their potential importance in the oceanic biological pump
The biological pump plays a vital role in exporting organic particles into the deep ocean for long-term carbon sequestration. However, much remains unknown about some of its key microbial players. In this study, Labyrinthulomycetes protists (LP) were used to understand the significance of heterotrophic microeukaryotes in the transport of particulate organic matter from the surface to the dark ocean. Unlike the sharp vertical decrease of prokaryotic biomass, the LP biomass only slightly decreased with depth and eventually exceeded prokaryotic biomass in the bathypelagic layer. Sequencing identified high diversity of the LP communities with a dominance of Aplanochytrium at all depths. Notably, ASVs that were observed in the surface layer comprised ~20% of ASVs and ~60% of sequences in each of the deeper (including bathypelagic) layers, suggesting potential vertical export of the LP populations to the deep ocean. Further analyses of the vertical patterns of the 50 most abundant ASVs revealed niche partitioning of LP phylotypes in the pelagic ocean, including those that could decompose organic detritus and/or facilitate the formation of fast-sinking particles. Overall, this study presents several lines of evidence that the LP can be an important component of the biological pump through their multiple ecotypes in the pelagic ocean.  more » « less
Award ID(s):
2033934 1416665
NSF-PAR ID:
10294417
Author(s) / Creator(s):
; ; ; ; ; ; ; ;
Date Published:
Journal Name:
Environmental Microbiology
ISSN:
1462-2912
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. dos Santos, Adriana Lopes (Ed.)
    ABSTRACT Labyrinthulomycetes protists are an important heterotrophic component of microeukaryotes in the world’s oceans, but their distribution patterns and ecological roles are poorly understood in pelagic waters. This study employed flow cytometry and high-throughput sequencing to characterize the abundance, diversity, and community structure of Labyrinthulomycetes in the pelagic Eastern Indian Ocean. The total Labyrinthulomycetes abundance varied much more among stations than did the abundance of prokaryotic plankton, reaching over 1,000 cells mL −1 at a few “bloom” stations. The total Labyrinthulomycetes abundance did not decline with depth throughout the whole water column (5 to 2,000 m) like the abundance of prokaryotic plankton did, and the Labyrinthulomycetes average projected biomass over all samples was higher than that of the prokaryotic plankton. However, Labyrinthulomycetes diversity showed obvious vertical variations, with richness, Shannon diversity, and evenness greatest in the upper epipelagic, lower epipelagic, and deep waters, respectively. Many abundant phylotypes were detected across multiple water layers, which aligned with the constant vertical Labyrinthulomycetes biomass, suggesting potential sinking and contribution to the biological pump. Hierarchical clustering revealed distinct ecotypes partitioning by vertical distribution patterns, suggesting their differential roles in the carbon cycle and storage processes. Particularly, most phylotypes showed patchy distributions (occurring in only few samples) as previously found in the coastal waters, but they were less associated with the Labyrinthulomycetes blooms than the prevalent phylotypes. Overall, this study revealed distinct patterns of Labyrinthulomycetes ecotypes and shed light on their importance in the pelagic ocean carbon cycling and sequestration relative to that of the prokaryotic plankton. IMPORTANCE While prokaryotic heterotrophic plankton are well accepted as major players in oceanic carbon cycling, the ecological distributions and functions of their microeukaryotic counterparts in the pelagic ocean remain largely unknown. This study focused on an important group of heterotrophic (mainly osmotrophic) protistan microbes, the Labyrinthulomycetes, whose biomass can surpass that of the prokaryotic plankton in many marine ecosystems, including the bathypelagic ocean. We found patchy horizontal but persistent vertical abundance profiles of the Labyrinthulomycetes protists in the pelagic waters of the Eastern Indian Ocean, which were distinct from the spatial patterns of the prokaryotic plankton. Moreover, multiple Labyrinthulomycetes ecotypes with distinct vertical patterns were detected and, based on the physiologic, metabolic, and genomic understanding of their cultivated relatives, were inferred to play multifaceted key roles in the carbon cycle and sequestration, particularly as contributors to the vertical carbon export from the surface to the dark ocean, i.e., the biological pump. 
    more » « less
  2. null (Ed.)
    In the open ocean, elevated carbon flux (ECF) events increase the delivery of particulate carbon from surface waters to the seafloor by severalfold compared to other times of year. Since microbes play central roles in primary production and sinking particle formation, they contribute greatly to carbon export to the deep sea. Few studies, however, have quantitatively linked ECF events with the specific microbial assemblages that drive them. Here, we identify key microbial taxa and functional traits on deep-sea sinking particles that correlate positively with ECF events. Microbes enriched on sinking particles in summer ECF events included symbiotic and free-living diazotrophic cyanobacteria, rhizosolenid diatoms, phototrophic and heterotrophic protists, and photoheterotrophic and copiotrophic bacteria. Particle-attached bacteria reaching the abyss during summer ECF events encoded metabolic pathways reflecting their surface water origins, including oxygenic and aerobic anoxygenic photosynthesis, nitrogen fixation, and proteorhodopsin-based photoheterotrophy. The abundances of some deep-sea bacteria also correlated positively with summer ECF events, suggesting rapid bathypelagic responses to elevated organic matter inputs. Biota enriched on sinking particles during a spring ECF event were distinct from those found in summer, and included rhizaria, copepods, fungi, and different bacterial taxa. At other times over our 3-y study, mid- and deep-water particle colonization, predation, degradation, and repackaging (by deep-sea bacteria, protists, and animals) appeared to shape the biotic composition of particles reaching the abyss. Our analyses reveal key microbial players and biological processes involved in particle formation, rapid export, and consumption, that may influence the ocean’s biological pump and help sustain deep-sea ecosystems. 
    more » « less
  3. Abstract. The ability to constrain the mechanisms that transport organiccarbon into the deep ocean is complicated by the multiple physical,chemical, and ecological processes that intersect to create, transform, andtransport particles in the ocean. In this paper we develop andparameterize a data-assimilative model of the multiple pathways of thebiological carbon pump (NEMUROBCP). The mechanistic model is designedto represent sinking particle flux, active transport by vertically migratingzooplankton, and passive transport by subduction and vertical mixing, whilealso explicitly representing multiple biological and chemical propertiesmeasured directly in the field (including nutrients, phytoplankton andzooplankton taxa, carbon dioxide and oxygen, nitrogen isotopes, and234Thorium). Using 30 different data types (including standing stockand rate measurements related to nutrients, phytoplankton, zooplankton, andnon-living organic matter) from Lagrangian experiments conducted on 11cruises from four ocean regions, we conduct an objective statisticalparameterization of the model and generate 1 million different potentialparameter sets that are used for ensemble model simulations. The modelsimulates in situ parameters that were assimilated (net primary productionand gravitational particle flux) and parameters that were withheld(234Thorium and nitrogen isotopes) with reasonable accuracy. Modelresults show that gravitational flux of sinking particles and verticalmixing of organic matter from the euphotic zone are more importantbiological pump pathways than active transport by vertically migratingzooplankton. However, these processes are regionally variable, with sinkingparticles most important in oligotrophic areas of the Gulf of Mexico andCalifornia Current, sinking particles and vertical mixing roughly equivalentin productive coastal upwelling regions and the subtropical front in theSouthern Ocean, and active transport an important contributor in the easterntropical Pacific. We further find that mortality at depth is an importantcomponent of active transport when mesozooplankton biomass is high, but itis negligible in regions with low mesozooplankton biomass. Our results alsohighlight the high degree of uncertainty, particularly amongstmesozooplankton functional groups, that is derived from uncertainty in modelparameters. Indeed, variability in BCP pathways between simulations for aspecific location using different parameter sets (all with approximatelyequal misfit relative to observations) is comparable to variability in BCPpathways between regions. We discuss the implications of these results forother data-assimilation approaches and for studies that rely on non-ensemblemodel outputs. 
    more » « less
  4. Abstract

    Tropical cyclones (hurricanes) generate intense surface ocean cooling and vertical mixing resulting in nutrient upwelling into the photic zone and episodic phytoplankton blooms. However, their influence on the deep ocean remains unknown. Here we present evidence that hurricanes also impact the ocean's biological pump by enhancing export of labile organic material to the deep ocean. In October 2016, Category 3 Hurricane Nicole passed over the Bermuda Time Series site in the oligotrophic NW Atlantic Ocean. Following Nicole's passage, particulate fluxes of lipids diagnostic of fresh phytodetritus, zooplankton, and microbial biomass increased by 30–300% at 1,500 m depth and 30–800% at 3,200 m depth. Mesopelagic suspended particles following Nicole were also enriched in phytodetrital material and in zooplankton and bacteria lipids, indicating particle disaggregation and a deepwater ecosystem response. Predicted climate‐induced increases in hurricane frequency and/or intensity may significantly alter ocean biogeochemical cycles by increasing the strength of the biological pump.

     
    more » « less
  5. Midwater zooplankton are major agents of biogeochemical transformation in the open ocean; however their characteristics and activity remain poorly known. Here we evaluate midwater zooplankton biomass, amino acid (AA)-specific stable isotope composition (δ15N values) using compound-specific isotope analysis of amino acids (CSIA-AA), trophic position, and elemental composition in the North Pacific Subtropical Gyre (NPSG). We focus on zooplankton collected in the winter, spring, and summer to evaluate midwater trophic dynamics over a seasonal cycle. For the first time we find that midwater zooplankton respond strongly to seasonal changes in production and export in the NPSG. In summer, when export from the euphotic zone is elevated and this ‘summer pulse’ material is transported rapidly to depth, CSIA-AA indicates that large particles (> 53 μm) dominate the food web base for zooplankton throughout the midwaters, and to a large extent even into the upper bathypelagic zone. In winter, when export is low, zooplankton in the mid-mesopelagic zone continue to rely on large particle basal resources, but resident zooplankton in the lower mesopelagic and upper bathypelagic zones switch to include smaller particles (0.7–53 μm) in their food web base, or even a subset of the small particle pool. Midwater zooplankton migration patterns also vary with season, with migrants distributed more evenly at night through the euphotic zone in summer as compared to being more compressed in the upper mixed layer in winter. Deeper zooplankton migration within the mesopelagic zone is also reduced in late summer, likely due to the increased magnitude of large particle material available at depth during this season. Our observed seasonal change in activity and trophic dynamics drives modestly greater biomass in summer than winter through the mesopelagic zone. In contrast midwater zooplankton carbon (C), nitrogen (N), and phosphorus (P) composition does not change with season. Instead we find increasing C:N, C:P, and N:P ratios with greater depths, likely due to decreases in proteinaceous structures and organic P compounds and increases in storage lipids with depth. Our study highlights the importance and diversity of feeding strategies for small zooplankton in NPSG midwaters. Many small zooplankton, such as oncaeid and oithonid copepods, are able to access small particle resources at depth and may be an important trophic link between the microbial loop and deep dwelling micronekton species that also rely on small particle-based food webs. Our observed midwater zooplankton trophic response to export-driven variation in the particle field at depth has important implications for midwater metabolism and the export of C to the deep sea. 
    more » « less