skip to main content

Attention:

The NSF Public Access Repository (PAR) system and access will be unavailable from 11:00 PM ET on Friday, December 13 until 2:00 AM ET on Saturday, December 14 due to maintenance. We apologize for the inconvenience.


Title: Co‐culture with Synechococcus facilitates growth of Prochlorococcus under ocean acidification conditions
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
Award ID(s):
1851085
PAR ID:
10455583
Author(s) / Creator(s):
 ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Environmental Microbiology
Volume:
22
Issue:
11
ISSN:
1462-2912
Page Range / eLocation ID:
p. 4876-4889
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. 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
  2. Abstract

    Many microbial photoautotrophs depend on heterotrophic bacteria for accomplishing essential functions. Environmental changes, however, could alter or eliminate such interactions. We investigated the effects of changing pCO2 on gene transcription in co-cultures of 3 strains of picocyanobacteria (Synechococcus strains CC9311 and WH8102 and Prochlorococcus strain MIT9312) paired with the ‘helper’ bacterium Alteromonas macleodii EZ55. Co-culture with cyanobacteria resulted in a much higher number of up- and down-regulated genes in EZ55 than pCO2 by itself. Pathway analysis revealed significantly different transcription of genes involved in carbohydrate metabolism, stress response, and chemotaxis, with different patterns of up- or down-regulation in co-culture with different cyanobacterial strains. Gene transcription patterns of organic and inorganic nutrient transporter and catabolism genes in EZ55 suggested resources available in the culture media were altered under elevated (800 ppm) pCO2 conditions. Altogether, changing transcription patterns were consistent with the possibility that the composition of cyanobacterial excretions changed under the two pCO2 regimes, causing extensive ecophysiological changes in both members of the co-cultures. Additionally, significant downregulation of oxidative stress genes in MIT9312/EZ55 cocultures at 800 ppm pCO2 were consistent with a link between the predicted reduced availability of photorespiratory byproducts (i.e., glycolate/2PG) under this condition and observed reductions in internal oxidative stress loads for EZ55, providing a possible explanation for the previously observed lack of “help” provided by EZ55 to MIT9312 under elevated pCO2. If similar broad alterations in microbial ecophysiology occur in the ocean as atmospheric pCO2 increases, they could lead to substantially altered ecosystem functioning and community composition.

     
    more » « less
  3. 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
  4. Summary

    In contrast to the current paradigm of using microbial mono‐cultures in most biotechnological applications, increasing efforts are being directed towards engineering mixed‐species consortia to perform functions that are difficult to programme into individual strains. In this work, we developed a synthetic microbial consortium composed of two genetically engineered microbes, a cyanobacterium (Synechococcus elongatusPCC 7942) and a heterotrophic bacterium (Pseudomonas putidaEM173). These microbial species specialize in the co‐culture: cyanobacteria fix CO2through photosynthetic metabolism and secrete sufficient carbohydrates to support the growth and active metabolism ofP. putida, which has been engineered to consume sucrose and to degrade the environmental pollutant 2,4‐dinitrotoluene (2,4‐DNT). By encapsulatingS. elongatuswithin a barium–alginate hydrogel, cyanobacterial cells were protected from the toxic effects of 2,4‐DNT, enhancing the performance of the co‐culture. The synthetic consortium was able to convert 2,4‐DNT with light and CO2as key inputs, and its catalytic performance was stable over time. Furthermore, cycling this synthetic consortium through low nitrogen medium promoted the sucrose‐dependent accumulation of polyhydroxyalkanoate, an added‐value biopolymer, in the engineeredP. putidastrain. Altogether, the synthetic consortium displayed the capacity to remediate the industrial pollutant 2,4‐DNT while simultaneously synthesizing biopolymers using light and CO2as the primary inputs.

     
    more » « less
  5. Synechococcus (WH8102 and CC9311) growth and genetic sequence accessions from experiments with variable pCO2 treatments. These data were produced as part of a study of the "Community context and pCO2 impact the transcriptome of the "helper" bacterium Alteromonas in co-culture with picocyanobacteria" (Barreto Filho et al., 2022). Sequences files are accessible from the National Center for Biotechnology Information (BioProject PRJNA377729). The following results abstract describes these data along with related datasets which can be accessed from the "Related Datasets" section of this page. Many microbial photoautotrophs depend on heterotrophic bacteria for accomplishing essential functions. Environmental changes, however, could alter or eliminate such interactions. We investigated the effects of changing pCO2 on gene expression in co-cultures of 3 strains of picocyanobacteria (Synechococcus strains CC9311 and WH8102 and Prochlorococcus strain MIT9312) paired with the ‘helper’ bacterium Alteromonas macleodii EZ55. Co-culture with cyanobacteria resulted in a much higher number of up- and down-regulated genes in EZ55 than pCO2 by itself. Pathway analysis revealed significantly different expression of genes involved in carbohydrate metabolism, stress response, and chemotaxis, with different patterns of up- or down-regulation in co-culture with different cyanobacterial strains. Gene expression patterns of organic and inorganic nutrient transporter and catabolism genes in EZ55 suggested resources available in the culture media were altered under elevated (800 ppm) pCO2 conditions. Altogether, changing expression patterns were consistent with the possibility that the composition of cyanobacterial excretions changed under the two pCO2 regimes, causing extensive ecophysiological changes in both members of the co-cultures. Additionally, significant downregulation of oxidative stress genes inMIT9312/EZ55 cocultures at 800 ppm pCO2 were consistent with a link between the predicted reduced availability of photorespiratory byproducts (i.e., glycolate/2PG) under this condition and observed reductions in internal oxidative stress loads for EZ55, providing a possible explanation for the previously observed lack of “help” provided by EZ55 to MIT9312 under elevated pCO2. The data and code stored in this archive will allow the reconstruction of our analysis pipelines. Additionally, we provide annotation mapping files and other resources for conducting transcriptomic analyses with Alteromonas sp. EZ55. 
    more » « less