skip to main content


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 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
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. 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 NO3uptake 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 NO3uptake rates were higher thanProchlorococcusones. Pico‐sized pigmented groups accounted for a significant fraction of the community C‐fixation (63% ± 27%), NH4+uptake (47% ± 27%), NO3uptake (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. Summary

    Anthropogenic CO2emissions are projected to lower the pH of the ocean 0.3 units by 2100. Previous studies suggested thatProchlorococcusandSynechococcus, the numerically dominant phytoplankton in the oceans, have different responses to elevated CO2that may result in a dramatic shift in their relative abundances in future oceans. Here we showed that the exponential growth rates of these two genera respond to future CO2conditions in a manner similar to other cyanobacteria, butProchlorococcusstrains had significantly lower realized growth rates under elevated CO2regimes due to poor survival after exposure to fresh culture media. Despite this, aSynechococcusstrain was unable to outcompete aProchlorococcusstrain in co‐culture at elevated CO2. Under these conditions,Prochlorococcus' poor response to elevated CO2disappeared, andProchlorococcus'relative fitness showed negative frequency dependence, with both competitors having significant fitness advantages when initially rare. These experiments suggested that the two strains should be able to coexist indefinitely in co‐culture despite sharing nearly identical nutritional requirements. We speculate that negative frequency dependence exists due to reductive Black Queen evolution that has resulted in a passively mutualistic relationship analogous to that connectingProchlorococcuswith the ‘helper’ heterotrophic microbes in its environment.

     
    more » « less
  3. 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
  4. Abstract

    A few members of the bacterial genusThermushave been shown to be incomplete denitrifiers, terminating with nitrite (NO2) or nitrous oxide (N2O). However, the denitrification abilities of the genus as a whole remain poorly characterized. Here, we describe diverse denitrification phenotypes and genotypes of a collection of 24 strains representing ten species, all isolated from a variety of geothermal systems in China. Confirmed terminal products of nitrate reduction were nitrite or N2O, while nitric oxide (NO) was inferred as the terminal product in some strains. Most strains produced N2O; complete denitrification was not observed. Denitrification phenotypes were largely consistent with the presence of denitrification genes, and strains of the same species often had the same denitrification phenotypes and largely syntenous denitrification gene clusters. Genes fornirSandnirKcoexisted in threeThermus brockianusand threeThermus oshimaigenomes, which is a unique hallmark of some denitrifyingThermusstrains and may be ecologically important. These results show that incomplete denitrification phenotypes are prominent, but variable, within and betweenThermusspecies. The incomplete denitrification phenotypes described here suggestThermusspecies may play important roles in consortial denitrification in high-temperature terrestrial biotopes where sufficient supply of oxidized inorganic nitrogen exists.

     
    more » « less
  5. 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