skip to main content


Title: Transcriptional response of Emiliania huxleyi under changing nutrient environments in the North Pacific Subtropical Gyre
Summary

The widespread coccolithophoreEmiliania huxleyiis an abundant oceanic phytoplankton, impacting the global cycling of carbon through both photosynthesis and calcification. Here, we examined the transcriptional responses of populations ofE. huxleyiin the North Pacific Subtropical Gyre to shifts in the nutrient environment. Using a metatranscriptomic approach, nutrient‐amended microcosm studies were used to track the global metabolism ofE. huxleyi. The addition of nitrate led to significant changes in transcript abundance for gene pathways involved in nitrogen and phosphorus metabolism, with a decrease in the abundance of genes involved in the acquisition of nitrogen (e.g. N‐transporters) and an increase in the abundance of genes associated with phosphate acquisition (e.g. phosphatases). Simultaneously, after the addition of nitrate, genes associated with calcification and genes unique to the diploid life stages ofE. huxleyisignificantly increased. These results suggest that nitrogen is a major driver of the physiological ecology ofE. huxleyiin this system and further suggest that the addition of nitrate drives shifts in the dominant life‐stage of the population. Together, these results underscore the importance of phenotypic plasticity to the success ofE. huxleyi, a characteristic that likely underpins its ability to thrive across a variety of marine environments.

 
more » « less
NSF-PAR ID:
10458728
Author(s) / Creator(s):
 ;  ;  ;  
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Environmental Microbiology
Volume:
22
Issue:
5
ISSN:
1462-2912
Page Range / eLocation ID:
p. 1847-1860
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Summary

    Emiliania huxleyiis a calcifying haptophyte, contributing to both the organic and inorganic marine carbon cycles. In marine ecosystems, light is a major driver of phytoplankton physiology and ultimately carbon flow through the ecosystem. Here, we analysed a Lagrangian time‐series of metatranscriptomes collected in the North Pacific Subtropical Gyre (NPSG) to examine howin situpopulations ofE.huxleyimodulate gene expression over day–night transitions. ManyE.huxleyicontigs had a diel expression pattern, with 61% of contigs clustering into modules with statistically significant diel periodicity. Contigs involved in processes that build up energy stores, like carbon fixation and lipid synthesis, peaked around dawn. In contrast, contigs involved in processes that released energy stores, like respiration and lipid degradation, peaked mid‐day and towards dusk. These patterns suggest an orchestrated cycle of building, then consuming energy stores inE.huxleyipopulations in the NPSG. Selected contigs related to the cell cycle also exhibited significant diel periodicity consistent with phased modulations of division observed in culture. Overall, these patterns of gene expression suggest a daily metabolic cascade that could contribute to both organic and inorganic carbon flow in this nutrient depleted ecosystem.

     
    more » « less
  2. Temperature and nutrient supply are key factors that control phytoplankton ecophysiology, but their role is commonly investigated in isolation. Their combined effect on resource allocation, photosynthetic strategy, and metabolism remains poorly understood. To characterize the photosynthetic strategy and resource allocation under different conditions, we analyzed the responses of a marine cyanobacterium (SynechococcusPCC7002) to multiple combinations of temperature and nutrient supply. We measured the abundance of proteins involved in the dark (RuBisCO,rbcL) and light (PhotosystemII, psbA) photosynthetic reactions, the content of chlorophylla, carbon and nitrogen, and the rates of photosynthesis, respiration, and growth. We found thatrbcL and psbA abundance increased with nutrient supply, whereas a temperature‐induced increase in psbA occurred only in nutrient‐replete treatments. Low temperature and abundant nutrients caused increased RuBisCOabundance, a pattern we observed also in natural phytoplankton assemblages across a wide latitudinal range. Photosynthesis and respiration increased with temperature only under nutrient‐sufficient conditions. These results suggest that nutrient supply exerts a stronger effect than temperature upon both photosynthetic protein abundance and metabolic rates inSynechococcussp. and that the temperature effect on photosynthetic physiology and metabolism is nutrient dependent. The preferential resource allocation into the light instead of the dark reactions of photosynthesis as temperature rises is likely related to the different temperature dependence of dark‐reaction enzymatic rates versus photochemistry. These findings contribute to our understanding of the strategies for photosynthetic energy allocation in phytoplankton inhabiting contrasting environments.

     
    more » « less
  3. High‐affinity nitrate transporters are considered to be the major transporter system for nitrate uptake in diatoms. In the diatom genusSkeletonema, three forms of genes encoding high‐affinity nitrate transporters (NRT2) were newly identified from transcriptomes generated as part of the marine microbial eukaryote transcriptome sequencing project. To examine the expression of each form ofNRT2under different nitrogen environments, laboratory experiments were conducted under nitrate‐sufficient, ammonium‐sufficient, and nitrate‐limited conditions using three ecologically importantSkeletonemaspecies:S. dohrnii,S. menzelii,andS. marinoi. Primers were developed for eachNRT2form and species and Q‐RTPCRwas performed. For eachNRT2form, the threeSkeletonemaspecies had similar transcriptional patterns. The transcript levels ofNRT2:1were significantly elevated under nitrogen‐limited conditions, but strongly repressed in the presence of ammonium. The transcript levels ofNRT2:2were also repressed by ammonium, but increased 5‐ to 10‐fold under nitrate‐sufficient and nitrogen‐limited conditions. Finally, the transcript levels ofNRT2:3did not vary significantly under various nitrogen conditions, and behaved more like a constitutively expressed gene. Based on the observed transcript variation amongNRT2forms, we propose a revised model describing nitrate uptake kinetics regulated by multiple forms of nitrate transporter genes in response to various nitrogen conditions inSkeletonema. The differentialNRT2transcriptional responses among species suggest that species‐specific adaptive strategies exist within this genus to cope with environmental changes.

     
    more » « less
  4. Summary

    Bryophytes harbour microbiomes, including diverse communities of fungi. The molecular mechanisms by which perennial mosses interact with these fungal partners along their senescence gradients are unknown, yet this is an ideal system to study variation in gene expression associated with trophic state transitions. We investigated differentially expressed genes of fungal communities and their hostDicranum scopariumacross its naturally occurring senescence gradient using a metatranscriptomic approach. Higher activity of fungal nutrient‐related (carbon, nitrogen, phosphorus and sulfur) transporters and Carbohydrate‐Active enZyme (CAZy) genes was detected toward the bottom, partially decomposed, layer of the moss. The most prominent variation in the expression levels of fungal nutrient transporters was from inorganic nitrogen‐related transporters, whereas the breakdown of organonitrogens was detected as the most enriched gene ontology term for the hostD. scoparium, for those transcripts having higher expression in the partially decomposed layer. The abundance of bacterial rRNA transcripts suggested that more living members ofCyanobacteriaare associated with the photosynthetic layer ofD. scoparium, while members ofRhizobialesare detected throughout the gametophytes. Plant genes for specific fungal–plant communication, including defense responses, were differentially expressed, suggesting that different genetic pathways are involved in plant‐microbe crosstalk in photosynthetic tissues compared to partially decomposed tissues.

     
    more » « less
  5. Summary

    Alternative polyadenylation (APA) is a widespread post‐transcriptional mechanism that regulates gene expression throughmRNAmetabolism, playing a pivotal role in modulating phenotypic traits in rice (Oryza sativaL.). However, little is known about theAPA‐mediated regulation underlying the distinct characteristics between two major rice subspecies,indicaandjaponica. Using a poly(A)‐tag sequencing approach, polyadenylation (poly(A)) site profiles were investigated and compared pairwise from germination to the mature stage betweenindicaandjaponica, and extensive differentiation inAPAprofiles was detected genome‐wide. Genes with subspecies‐specific poly(A) sites were found to contribute to subspecies characteristics, particularly in disease resistance ofindicaand cold‐stress tolerance ofjaponica. In most tissues, differential usage ofAPAsites exhibited an apparent impact on the gene expression profiles between subspecies, and genes with those APA sites were significantly enriched in quantitative trait loci (QTL) related to yield traits, such as spikelet number and 1000‐seed weight. In leaves of the booting stage,APAsite‐switching genes displayed global shortening of 3′ untranslated regions with increased expression inindicacompared withjaponica, and they were overrepresented in the porphyrin and chlorophyll metabolism pathways. This phenomenon may lead to a higher chlorophyll content and photosynthesis inindicathan injaponica, being associated with their differential growth rates and yield potentials. We further constructed an online resource for querying and visualizing the poly(A) atlas in these two rice subspecies. Our results suggest thatAPAmay be largely involved in developmental differentiations between two rice subspecies, especially in leaf characteristics and the stress response, broadening our knowledge of the post‐transcriptional genetic basis underlying the divergence of rice traits.

     
    more » « less