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.

Attention:

The NSF Public Access Repository (PAR) system and access will be unavailable from 11:00 PM ET on Friday, November 14 until 2:00 AM ET on Saturday, November 15 due to maintenance. We apologize for the inconvenience.

Explore Research Products in the PAR
It may take a few hours for recently added research products to appear in PAR search results.


Title: Production and cross-feeding of nitrite within Prochlorococcus populations
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 NO2−maximum layer, an oceanographic feature that may, in part, be due to incomplete assimilatory NO3−reduction and subsequent NO2−release by phytoplankton. We hypothesized that someProchlorococcusexhibit incomplete assimilatory NO3−reduction and examined NO2−accumulation in cultures of threeProchlorococcusstrains (MIT0915, MIT0917, and SB) and twoSynechococcusstrains (WH8102 and WH7803). Only MIT0917 and SB accumulated external NO2−during growth on NO3−. Approximately 20–30% of the NO3−transported into the cell by MIT0917 was released as NO2−, with the rest assimilated into biomass. We further observed that co-cultures using NO3−as the sole N source could be established for MIT0917 andProchlorococcusstrain MIT1214 that can assimilate NO2−but not NO3−. In these co-cultures, the NO2−released 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 NO2−during growth on NO3−. In the wild,Prochlorococcuspopulations are composed of multiple functional types, including those that cannot use NO3−but can still assimilate NO2−. We show that metabolic dependencies arise whenProchlorococcusstrains with complementary NO2−production 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
Award ID(s):
2048470 2241005
PAR ID:
10492689
Author(s) / Creator(s):
; ; ; ;
Editor(s):
Dubilier, Nicole
Publisher / Repository:
American Society for Microbiology
Date Published:
Journal Name:
mBio
ISSN:
2150-7511
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; ; ; (, Limnology and Oceanography)
    Abstract Picoplankton populations dominate the planktonic community in the surface oligotrophic ocean. Yet, their strategies in the acquisition and the partitioning of organic and inorganic sources of nitrogen (N) and carbon (C) are poorly described. Here, we measured at the single‐cell level the uptake of dissolved inorganic C (C‐fixation), C‐leucine, N‐leucine, nitrate (NO3−), ammonium (NH4+), and N‐urea in pigmented and nonpigmented picoplankton groups at six low‐N stations in the northwestern Atlantic Ocean. Our study highlights important differences in trophic strategies betweenProchlorococcus,Synechococcus, photosynthetic pico‐eukaryotes, and nonpigmented prokaryotes. Nonpigmented prokaryotes were characterized by high leucine uptake rates, nonsignificant C‐fixation and relatively low NH4+, N‐urea, and NO3−uptake rates. Nonpigmented prokaryotes contributed to 7% ± 3%, 2% ± 2%, and 9% ± 5% of the NH4+, NO3−, and N‐urea community uptake, respectively. In contrast, pigmented groups displayed relatively high C‐fixation rates, NH4+and N‐urea uptake rates, but lower leucine uptake rates than nonpigmented prokaryotes.Synechococcusand photosynthetic pico‐eukaryotes NO3−uptake rates were higher thanProchlorococcusones. Pico‐sized pigmented groups accounted for a significant fraction of the community C‐fixation (63% ± 27%), NH4+uptake (47% ± 27%), NO3−uptake (62% ± 49%), and N‐urea uptake (81% ± 35%). Interestingly,Prochlorococcusand photosynthetic pico‐eukaryotes showed a greater reliance on C‐ and N‐leucine thanSynechococcuson average, suggesting a greater reliance on organic C and N sources. Taken together, our single‐cell results decipher the wide diversity of C and N trophic strategies between and within marine picoplankton groups, but a clear partitioning between pigmented and nonpigmented groups still remains. 
    more » « less
  2. ; ; (, Applied and Environmental Microbiology)
    Bose, Arpita (Ed.)
    ABSTRACT The marine cyanobacteriumProchlorococcusnumerically dominates the phytoplankton communities in all lower latitude, open ocean environments. Having lost the catalase gene,Prochlorococcusis highly susceptible to exogenous hydrogen peroxide (H2O2) produced at the ocean’s surface. Protection by H2O2-scavenging heterotrophic “helper” bacteria has been demonstrated in laboratory cultures and implicated as an important mechanism ofProchlorococcussurvival in the ocean. Importantly, some other phytoplankton can also scavenge H2O2, suggesting these competing microbes may inadvertently protectProchlorococcus. In this study, we assessed the ability of co-occurring phytoplankton, the cyanobacteriumSynechococcusand picoeukaryotesMicromonasandOstreococcus, to protectProchlorococcusfrom H2O2exposure when cocultured at ecologically relevant abundances. All three genera could significantly degrade H2O2and diminishProchlorococcusmortality during H2O2exposures simulating photochemical production and rainfall events. We suggest that these phytoplankton groups contribute significantly to the H2O2microbial sink of the open ocean, thus complicating their relationships with and perhaps contributing to the evolutionary history ofProchlorococcus.IMPORTANCEThe marine cyanobacteriumProchlorococcusis the most abundant photosynthetic organism on the planet and is crucially involved in microbial community dynamics and biogeochemical cycling in most tropical and subtropical ocean waters. This success is due, in part, to the detoxification of the reactive oxygen species hydrogen peroxide (H2O2) performed by “helper” organisms. Earlier work identified heterotrophic bacteria as helpers, and here, we demonstrate that rival cyanobacteria and picoeukaryotic phytoplankton can also contribute to the survival ofProchlorococcusduring exposure to H2O2. Whereas heterotrophic bacteria helper organisms can benefit directly from promoting the survival of carbon-fixingProchlorococcuscells, phytoplankton helpers may suffer a twofold injury: production of H2O2degrading enzymes constrains already limited resources in oligotrophic environments, and the activity of these enzymes bolsters the abundance of their numerically dominant competitor. These findings build toward a better understanding of the intricate dynamics and interactions that shape microbial community structure in the open ocean. 
    more » « less
  3. ; ; ; ; (, Journal of Geophysical Research: Oceans)
    Abstract The Southern Ocean is a high‐nutrient, low‐chlorophyll (HNLC) region characterized by incomplete nitrate (NO3−) consumption by phytoplankton in surface waters. During this incomplete consumption, phytoplankton preferentially assimilate the14N‐ versus the15N‐bearing form of NO3−, quantified as the NO3−assimilation isotope effect (15ε). Previous summertime estimates of the15ε from HNLC regions range from 4 to 11‰. While culture work has shown that the15ε varies among phytoplankton species, as well as with light and iron stress, we lack a systematic understanding of how and why the15ε varies in the field. Here we estimate the15ε from water‐column profile and surface‐water samples collected in the Indian sector of the Southern Ocean—the first leg of the Antarctic Circumnavigation Expedition (December 2016–January 2017) and the Crossroads transect (April 2016). Consistent with prior work in the mid‐to‐late summer Southern Ocean, we estimate a higher15ε (8.9 ± 0.6‰) for the northern Subantarctic Zone and a lower15ε (5.4 ± 0.9‰) at and south of the Subantarctic Front. We interpret our data in the context of coincident measurements of phytoplankton community composition and estimates of iron and light stress. Similar to prior work, we find a significant, negative relationship between the15ε and the average mixed‐layer photosynthetically active radiation flux of 30–100 μmol m−2 s−1, while above 100 μmol m−2 s−1,15ε increases again. In addition, while we observe no robust relationship of the15ε to iron availability or phytoplankton community, mixed‐layer nitrification over the Kerguelen Plateau appears to strongly influence its magnitude. 
    more » « less
  4. ; ; (, mBio)
    Martiny, Jennifer B. (Ed.)
    ABSTRACT The marine cyanobacterium Prochlorococcus numerically dominates the phytoplankton community of the nutrient-limited open ocean, establishing itself as the most abundant photosynthetic organism on Earth. This ecological success has been attributed to lower cell quotas for limiting nutrients, superior resource acquisition, and other advantages associated with cell size reduction and genome streamlining. In this study, we tested the prediction that Prochlorococcus outcompetes its rivals for scarce nutrients and that this advantage leads to its numerical success in nutrient-limited waters. Strains of Prochlorococcus and its sister genus Synechococcus grew well in both mono- and cocultures when nutrients were replete. However, in nitrogen-limited medium, Prochlorococcus outgrew Synechococcus but only when heterotrophic bacteria were also present. In the nitrogen-limited medium, the heterotroph Alteromonas macleodii outcompeted Synechococcus for nitrogen but only if stimulated by the exudate released by Prochlorococcus or if a proxy organic carbon source was provided. Genetic analysis of Alteromonas suggested that it outcompetes Synechococcus for nitrate and/or nitrite, during which cocultured Prochlorococcus grows on ammonia or other available nitrogen species. We propose that Prochlorococcus can stimulate antagonism between heterotrophic bacteria and potential phytoplankton competitors through a metabolic cross-feeding interaction, and this stimulation could contribute to the numerical success of Prochlorococcus in nutrient-limited regions of the ocean. IMPORTANCE In nutrient-poor habitats, competition for limited resources is thought to select for organisms with an enhanced ability to scavenge nutrients and utilize them efficiently. Such adaptations characterize the cyanobacterium Prochlorococcus , the most abundant photosynthetic organism in the nutrient-limited open ocean. In this study, the competitive superiority of Prochlorococcus over a rival cyanobacterium, Synechococcus , was captured in laboratory culture. Critically, this outcome was achieved only when key aspects of the open ocean were simulated: a limited supply of nitrogen and the presence of heterotrophic bacteria. The results indicate that Prochlorococcus promotes its numerical dominance over Synechococcus by energizing the heterotroph’s ability to outcompete Synechococcus for available nitrogen. This study demonstrates how interactions between trophic groups can influence interactions within trophic groups and how these interactions likely contribute to the success of the most abundant photosynthetic microorganism. 
    more » « less
  5. ; ; ; ; ; ; (, Environmental Microbiology)
    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
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email