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.

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


This content will become publicly available on May 21, 2026

Title: Rival phytoplankton contribute to the cross protection of Prochlorococcus from oxidative stress
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
Award ID(s):
2023680
PAR ID:
10621271
Author(s) / Creator(s):
; ;
Editor(s):
Bose, Arpita
Publisher / Repository:
ASM Journals
Date Published:
Journal Name:
Applied and Environmental Microbiology
Volume:
91
Issue:
5
ISSN:
0099-2240
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. ; ; (, 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
  2. ; (, Environmental Microbiology)
    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. ; ; ; ; (, Biological and Chemical Oceanography Data Management Office (BCO-DMO))
    The CO2 content of Earth's atmosphere is rapidly increasing due to human consumption of fossil fuels. Models based on short-term culture experiments predict that major changes will occur in marine phytoplankton communities in the future ocean, but these models rarely consider how the evolutionary potential of phytoplankton or interactions within marine microbial communities may influence these changes. Here we experimentally evolved representatives of four phytoplankton functional types (silicifiers, calcifiers, coastal cyanobacteria, and oligotrophic cyanobacteria) in co-culture with a heterotrophic bacterium, Alteromonas, under either present-day or predicted future pCO2 conditions. The data and analysis code in this dataset show that the growth rates of cyanobacteria generally increased under both conditions, and the growth defects observed in ancestral Prochlorococcus cultures at elevated pCO2 and in axenic culture were diminished after evolution. Evolved Alteromonas were also poorer "helpers" for Prochlorococcus, supporting the assertion that the interaction between Prochlorococcus and heterotrophic bacteria is not a true mutualism but rather a competitive interaction stabilized by Black Queen processes. This work provides new insights on how phytoplankton will respond to anthropogenic change and on the evolutionary mechanisms governing the structure and function of marine microbial communities. 
    more » « less
  4. ; ; ; ; (, mBio)
    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 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
  5. ; ; ; ; ; ; (, Applied and Environmental Microbiology)
    Nojiri, Hideaki (Ed.)
    ABSTRACT In the oligotrophic oceans, key autotrophs depend on “helper” bacteria to reduce oxidative stress from hydrogen peroxide (H 2 O 2 ) in the extracellular environment. H 2 O 2 is also a ubiquitous stressor in freshwaters, but the effects of H 2 O 2 on autotrophs and their interactions with bacteria are less well understood in freshwaters. Naturally occurring H 2 O 2 in freshwater systems is proposed to impact the proportion of microcystin-producing (toxic) and non-microcystin-producing (nontoxic) Microcystis in blooms, which influences toxin concentrations and human health impacts. However, how different strains of Microcystis respond to naturally occurring H 2 O 2 concentrations and the microbes responsible for H 2 O 2 decomposition in freshwater cyanobacterial blooms are unknown. To address these knowledge gaps, we used metagenomics and metatranscriptomics to track the presence and expression of genes for H 2 O 2 decomposition by microbes during a cyanobacterial bloom in western Lake Erie in the summer of 2014. katG encodes the key enzyme for decomposing extracellular H 2 O 2 but was absent in most Microcystis cells. katG transcript relative abundance was dominated by heterotrophic bacteria. In axenic Microcystis cultures, an H 2 O 2 scavenger (pyruvate) significantly improved growth rates of one toxic strain while other toxic and nontoxic strains were unaffected. These results indicate that heterotrophic bacteria play a key role in H 2 O 2 decomposition in Microcystis blooms and suggest that their activity may affect the fitness of some Microcystis strains and thus the strain composition of Microcystis blooms but not along a toxic versus nontoxic dichotomy. IMPORTANCE Cyanobacterial harmful algal blooms (CHABs) threaten freshwater ecosystems globally through the production of toxins. Toxin production by cyanobacterial species and strains during CHABs varies widely over time and space, but the ecological drivers of the succession of toxin-producing species remain unclear. Hydrogen peroxide (H 2 O 2 ) is ubiquitous in natural waters, inhibits microbial growth, and may determine the relative proportions of Microcystis strains during blooms. However, the mechanisms and organismal interactions involved in H 2 O 2 decomposition are unexplored in CHABs. This study shows that some strains of bloom-forming freshwater cyanobacteria benefit from detoxification of H 2 O 2 by associated heterotrophic bacteria, which may impact bloom development. 
    more » « less
  • Citation Formats
  • MLA
  • APA
  • Chicago
  • BibTeX
  • Save / Share this Record
  • Send to Email