skip to main content


Title: A single Prochlorococcus ecotype dominates the tropical Bay of Bengal with ultradian growth
Abstract

The Bay of Bengal (BoB) spans >2.2 million km2in the northeastern Indian Ocean and is bordered by dense populations that depend upon its resources. Over recent decades, a shift from larger phytoplankton to picoplankton has been reported, yet the abundance, activity, and composition of primary producer communities are not well‐characterized. We analysed the BoB regions during the summer monsoon.Prochlorococcusranged up to 3.14 × 105cells mL−1in the surface mixed layer, averaging 1.74 ± 0.46 × 105in the upper 10 m and consistently higher thanSynechococcusand eukaryotic phytoplankton. V1‐V2 rRNA gene amplicon analyses showed the High Light II (HLII) ecotype formed 98 ± 1% ofProchlorococcusamplicons in surface waters, comprising six oligotypes, with the dominant oligotype accounting for 65 ± 4% of HLII. Diel sampling of a coherent water mass demonstrated evening onset of cell division and rapidProchlorococcusgrowth between 1.5 and 3.1 div day−1, based on cell cycle analysis, as confirmed by abundance‐based estimates of 2.1 div day−1. Accumulation ofProchlorococcusproduced by ultradian growth was restricted by high loss rates. Alongside prior Arabian Sea and tropical Atlantic rates, our results indicateProchlorococcusgrowth rates should be reevaluated with greater attention to latitudinal zones and influences on contributions to global primary production.

 
more » « less
Award ID(s):
2230811
PAR ID:
10504710
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Environmental Microbiology
Volume:
26
Issue:
3
ISSN:
1462-2912
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    The Bay of Bengal (BoB) is a 2,600,000 km2expanse in the Indian Ocean upon which many humans rely. However, the primary producers underpinning food chains here remain poorly characterized. We examined phytoplankton abundance and diversity along strong BoB latitudinal and vertical salinity gradients—which have low temperature variation (27–29°C) between the surface and subsurface chlorophyll maximum (SCM). In surface waters,Prochlorococcusaveraged 11.7 ± 4.4 × 104 cells ml−1, predominantly HLII, whereas LLII and ‘rare’ ecotypes, HLVI and LLVII, dominated in the SCM.Synechococcusaveraged 8.4 ± 2.3 × 104 cells ml−1in the surface, declined rapidly with depth, and population structure of dominant Clade II differed between surface and SCM; Clade X was notable at both depths. Across all sites,OstreococcusClade OII dominated SCM eukaryotes whereas communities differentiated strongly moving from Arabian Sea‐influenced high salinity (southerly; prasinophytes) to freshwater‐influenced low salinity (northerly; stramenopiles, specifically, diatoms, pelagophytes, and dictyochophytes, plus the prasinophyteMicromonas) surface waters. Eukaryotic phytoplankton peaked in the south (1.9 × 104 cells ml−1, surface) where a novelOstreococcuswas revealed, named hereOstreococcus bengalensis. We expose dominance of a single picoeukaryote and hitherto ‘rare’ picocyanobacteria at depth in this complex ecosystem where studies suggest picoplankton are replacing larger phytoplankton due to climate change.

     
    more » « less
  2. Johnson, Karyn N. (Ed.)
    ABSTRACT Coral reefs are possible sinks for microbes; however, the removal mechanisms at play are not well understood. Here, we characterize pelagic microbial groups at the CARMABI reef (Curaçao) and examine microbial consumption by three coral species: Madracis mirabilis , Porites astreoides , and Stephanocoenia intersepta . Flow cytometry analyses of water samples collected from a depth of 10 m identified 6 microbial groups: Prochlorococcus , three groups of Synechococcus , photosynthetic eukaryotes, and heterotrophic bacteria. Minimum growth rates (μ) for Prochlorococcus , all Synechococcus groups, and photosynthetic eukaryotes were 0.55, 0.29, and 0.45 μ day −1 , respectively, and suggest relatively high rates of productivity despite low nutrient conditions on the reef. During a series of 5-h incubations with reef corals performed just after sunset or prior to sunrise, reductions in the abundance of photosynthetic picoeukaryotes, Prochlorococcus and Synechococcus cells, were observed. Of the three Synechococcus groups, one decreased significantly during incubations with each coral and the other two only with M. mirabilis. Removal of carbon from the water column is based on coral consumption rates of phytoplankton and averaged between 138 ng h −1 and 387 ng h −1 , depending on the coral species. A lack of coral-dependent reduction in heterotrophic bacteria, differences in Synechococcus reductions, and diurnal variation in reductions of Synechococcus and Prochlorococcus , coinciding with peak cell division, point to selective feeding by corals. Our study indicates that bentho-pelagic coupling via selective grazing of microbial groups influences carbon flow and supports heterogeneity of microbial communities overlying coral reefs. IMPORTANCE We identify interactions between coral grazing behavior and the growth rates and cell abundances of pelagic microbial groups found surrounding a Caribbean reef. During incubation experiments with three reef corals, reductions in microbial cell abundance differed according to coral species and suggest specific coral or microbial mechanisms are at play. Peaks in removal rates of Prochlorococcus and Synechococcus cyanobacteria appear highest during postsunset incubations and coincide with microbial cell division. Grazing rates and effort vary across coral species and picoplankton groups, possibly influencing overall microbial composition and abundance over coral reefs. For reef corals, use of such a numerically abundant source of nutrition may be advantageous, especially under environmentally stressful conditions when symbioses with dinoflagellate algae break down. 
    more » « less
  3. 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.

    IMPORTANCE

    Earth’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
  4. Abstract

    Prochlorococcus is the most numerically abundant photosynthetic organism in the surface ocean. The Prochlorococcus high-light and warm-water adapted ecotype (HLII) is comprised of extensive microdiversity, but specific functional differences between microdiverse sub-clades remain elusive. Here we characterized both functional and phylogenetic diversity within the HLII ecotype using Bio-GO-SHIP metagenomes. We found widespread variation in gene frequency connected to local environmental conditions. Metagenome-assembled marker genes and genomes revealed a globally distributed novel HLII haplotype defined by adaptation to chronically low P conditions (HLII-P). Environmental correlation analysis revealed different factors were driving gene abundances verses phylogenetic differences. An analysis of cultured HLII genomes and metagenome-assembled genomes revealed a subclade within HLII, which corresponded to the novel HLII-P haplotype. This work represents the first global assessment of the HLII ecotype’s phylogeography and corresponding functional differences. These findings together expand our understanding of how microdiversity structures functional differences and reveals the importance of nutrients as drivers of microdiversity in Prochlorococcus.

     
    more » « less
  5. 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