skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Ubiquitous filter feeders shape open ocean microbial community structure and function
Abstract The mechanism of mortality plays a large role in how microorganisms in the open ocean contribute to global energy and nutrient cycling. Salps are ubiquitous pelagic tunicates that are a well-known mortality source for large phototrophic microorganisms in coastal and high-latitude systems, but their impact on the immense populations of smaller prokaryotes in the tropical and subtropical open ocean gyres is not well quantified. We used robustly quantitative techniques to measure salp clearance and enrichment of specific microbial functional groups in the North Pacific Subtropical Gyre, one of the largest ecosystems on Earth. We discovered that salps are a previously unknown predator of the globally abundant nitrogen fixer Crocosphaera; thus, salps restrain new nitrogen delivery to the marine ecosystem. We show that the ocean's two numerically dominant cells, Prochlorococcus and SAR11, are not consumed by salps, which offers a new explanation for the dominance of small cells in open ocean systems. We also identified a double bonus for Prochlorococcus, wherein it not only escapes salp predation but the salps also remove one of its major mixotrophic predators, the prymnesiophyte Chrysochromulina. When we modeled the interaction between salp mesh and particles, we found that cell size alone could not account for these prey selection patterns. Instead, the results suggest that alternative mechanisms, such as surface property, shape, nutritional quality, or even prey behavior, determine which microbial cells are consumed by salps. Together, these results identify salps as a major factor in shaping the structure, function, and ecology of open ocean microbial communities.  more » « less
Award ID(s):
1851537
PAR ID:
10558636
Author(s) / Creator(s):
; ; ;
Editor(s):
Bahar, Ivet
Publisher / Repository:
Oxford University Press
Date Published:
Journal Name:
PNAS Nexus
Volume:
3
Issue:
3
ISSN:
2752-6542
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract We investigated competition betweenSalpa thompsoniand protistan grazers during Lagrangian experiments near the Subtropical Front in the southwest Pacific sector of the Southern Ocean. Over a month, the salp community shifted from dominance by large (> 100 mm) oozooids and small (< 20 mm) blastozooids to large (~ 60 mm) blastozooids. Phytoplankton biomass was consistently dominated by nano‐ and microphytoplankton (> 2 μm cells). Using bead‐calibrated flow‐cytometry light scatter to estimate phytoplankton size, we quantified size‐specific salp and protistan zooplankton grazing pressure. Salps were able to feed at a > 10,000 : 1 predator : prey size (linear‐dimension) ratio. Small blastozooids efficiently retained cells > 1.4μm (high end of picoplankton size, 0.6–2 μm cells) and also obtained substantial nutrition from smaller bacteria‐sized cells. Larger salps could only feed efficiently on > 5.9μm cells and were largely incapable of feeding on picoplankton. Due to the high biomass of nano‐ and microphytoplankton, however, all salps derived most of their (phytoplankton‐based) nutrition from these larger autotrophs. Phagotrophic protists were the dominant competitors for these prey items and consumed approximately 50% of the biomass of all phytoplankton size classes each day. Using a Bayesian statistical framework, we developed an allometric‐scaling equation for salp clearance rates as a function of salp and prey size:urn:x-wiley:00243590:media:lno11770:lno11770-math-0001where ESD is prey equivalent spherical diameter (µm), TL isS. thompsonitotal length,φ = 5.6 × 10−3 ± 3.6 × 10−4,ψ = 2.1 ± 0.13,θ = 0.58 ± 0.08, andγ = 0.46 ± 0.03 and clearance rate is L d‐1salp‐1. We discuss the biogeochemical and food‐web implications of competitive interactions among salps, krill, and protozoans. 
    more » « less
  2. Abstract Mixotrophic nanoflagellates can account for more than half of the bacterivory in the sunlit ocean, yet very little is known about their ecophysiology. Here, we characterize the grazing ecology of an open‐ocean mixotroph in the genusFlorenciella(class Dictyochophyceae). Members of this class were indirectly implicated as major consumers ofProchlorococcusandSynechococcusin the oligotrophic North Pacific Subtropical Gyre, but their phagotrophic capabilities have never been investigated. Our studies showed thatFlorenciellareadily consumedProchlorococcus,Synechococcus, and heterotrophic bacteria, and that the ingested prey relieved nutrient limitations on growth.Florenciellagrew faster (3 d−1) in nitrogen‐deplete medium given sufficient liveSynechococcus, than in nitrogen‐replete K medium (2 d−1), but it did not grow in continuous darkness. Grazing rates were substantially higher under nutrient limitation and showed a hint of diel variability, with rates tending to be highest near the end of the light period. An apparent trade‐off between the maximum clearance rate (5 nLFlorenciella−1h−1) and the maximum ingestion rate (up to ∼ 10 prey cellsFlorenciella−1h−1) across experiments suggests that grazing behavior may also vary in response to prey concentration. If the observed grazing rates are representative of other open‐ocean mixotrophs, their collective activity could account for a significant fraction of the daily cyanobacterial mortality. This study provides essential parameters for understanding the grazing ecology of a common marine mixotroph and the first characterization of mixotrophic nanoflagellate functional responses when feeding on unicellular cyanobacteria, the dominant marine primary producers in the oligotrophic ocean. 
    more » « less
  3. Abstract Microbial mortality impacts the structure of food webs, carbon flow, and the interactions that create dynamic patterns of abundance across gradients in space and time in diverse ecosystems. In the oceans, estimates of microbial mortality by viruses, protists, and small zooplankton do not account fully for observations of loss, suggesting the existence of underappreciated mortality sources. We examined how ubiquitous mucous mesh feeders (i.e. gelatinous zooplankton) could contribute to microbial mortality in the open ocean. We coupled capture of live animals by blue‐water diving to sequence‐based approaches to measure the enrichment and selectivity of feeding by two coexisting mucous grazer taxa (pteropods and salps) on numerically dominant marine prokaryotes. We show that mucous mesh grazers consume a variety of marine prokaryotes and select between coexisting lineages and similar cell sizes. We show thatProchlorococcusmay evade filtration more than other cells and that planktonic archaea are consumed by macrozooplanktonic grazers. Discovery of these feeding relationships identifies a new source of mortality for Earth's dominant marine microbes and alters our understanding of how top‐down processes shape microbial community and function. 
    more » « less
  4. Abstract The Southern Ocean contributes substantially to the global biological carbon pump (BCP). Salps in the Southern Ocean, in particular Salpa thompsoni , are important grazers that produce large, fast-sinking fecal pellets. Here, we quantify the salp bloom impacts on microbial dynamics and the BCP, by contrasting locations differing in salp bloom presence/absence. Salp blooms coincide with phytoplankton dominated by diatoms or prymnesiophytes, depending on water mass characteristics. Their grazing is comparable to microzooplankton during their early bloom, resulting in a decrease of ~1/3 of primary production, and negative phytoplankton rates of change are associated with all salp locations. Particle export in salp waters is always higher, ranging 2- to 8- fold (average 5-fold), compared to non-salp locations, exporting up to 46% of primary production out of the euphotic zone. BCP efficiency increases from 5 to 28% in salp areas, which is among the highest recorded in the global ocean. 
    more » « less
  5. Dubilier, Nicole (Ed.)
    ABSTRACT Prochlorococcusis an abundant photosynthetic bacterium in the open ocean, where nitrogen (N) often limits phytoplankton growth. In the low-light-adapted LLI clade ofProchlorococcus, nearly all cells can assimilate nitrite (NO2), with a subset capable of assimilating nitrate (NO3). LLI cells are maximally abundant near the primary NO2maximum layer, an oceanographic feature that may, in part, be due to incomplete assimilatory NO3reduction and subsequent NO2release by phytoplankton. We hypothesized that someProchlorococcusexhibit incomplete assimilatory NO3reduction and examined NO2accumulation in cultures of threeProchlorococcusstrains (MIT0915, MIT0917, and SB) and twoSynechococcusstrains (WH8102 and WH7803). Only MIT0917 and SB accumulated external NO2during growth on NO3. Approximately 20–30% of the NO3transported into the cell by MIT0917 was released as NO2, with the rest assimilated into biomass. We further observed that co-cultures using NO3as the sole N source could be established for MIT0917 andProchlorococcusstrain MIT1214 that can assimilate NO2but not NO3. In these co-cultures, the NO2released by MIT0917 is efficiently consumed by its partner strain, MIT1214. Our findings highlight the potential for emergent metabolic partnerships that are mediated by the production and consumption of N cycle intermediates withinProchlorococcuspopulations. IMPORTANCEEarth’s biogeochemical cycles are substantially driven by microorganisms and their interactions. Given that N often limits marine photosynthesis, we investigated the potential for N cross-feeding within populations ofProchlorococcus, the numerically dominant photosynthetic cell in the subtropical open ocean. In laboratory cultures, someProchlorococcuscells release extracellular NO2during growth on NO3. In the wild,Prochlorococcuspopulations are composed of multiple functional types, including those that cannot use NO3but can still assimilate NO2. We show that metabolic dependencies arise whenProchlorococcusstrains with complementary NO2production and consumption phenotypes are grown together on NO3. These findings demonstrate the potential for emergent metabolic partnerships, possibly modulating ocean nutrient gradients, that are mediated by cross-feeding of N cycle intermediates. 
    more » « less