Conserved Transcriptional Responses to Nutrient Stress in Bloom-Forming Algae

Abstract

The concentration and composition of bioavailable nitrogen (N) and phosphorus (P) in the upper ocean shape eukaryotic phytoplankton communities and influence their physiological responses. Phytoplankton are known to exhibit similar physiological responses to limiting N and P conditions such as decreased growth rates, chlorosis, and increased assimilation of N and P. Are these responses similar at the molecular level across multiple species? To interrogate this question, five species from biogeochemically important, bloom-forming taxa (Bacillariophyta, Dinophyta, and Haptophyta) were grown under similar low N, low P, and replete nutrient conditions to identify transcriptional patterns and associated changes in biochemical pools related to N and P stress. Metabolic profiles, revealed through the transcriptomes of these taxa, clustered together based on species rather than nutrient stressor, suggesting that the global metabolic response to nutrient stresses was largely, but not exclusively, species-specific. Nutrient stress led to few transcriptional changes in the two dinoflagellates, consistent with other research. An orthologous group analysis examined functionally conserved (i.e., similarly changed) responses to nutrient stress and therefore focused on the diatom and haptophytes. Most conserved ortholog changes were specific to a single nutrient treatment, but a small number of orthologs were similarly changed under both N and P stress in 2 or more species. Many of these orthologs were related to photosynthesis and may represent generalized stress responses. A greater number of orthologs were conserved across more than one species under low P compared to low N. Screening the conserved orthologs for functions related to N and P metabolism revealed increased relative abundance of orthologs for nitrate, nitrite, ammonium, and amino acid transporters under N stress, and increased relative abundance of orthologs related to acquisition of inorganic and organic P substrates under P stress. Although the global transcriptional responses were dominated by species-specific changes, the analysis of conserved responses revealed functional similarities in resource acquisition pathways among different phytoplankton taxa. This overlap in nutrient stress responses observed among species may be useful for tracking the physiological ecology of phytoplankton field populations.

Diverse CO2-Induced Responses in Physiology and Gene Expression among Eukaryotic Phytoplankton

“…The exception to this being the reduced expression of TCA cycle genes by P. minimum , which may help to explain the decrease in growth rate (Figure 1 ). A limited transcriptional response of the dinoflagellates has been observed in experiments with nutrient limitation (Harke et al, 2017 ) and elevated temperatures (Barshis et al, 2014 ). The limited transcriptional response to environmental perturbations may be largely explained by the underlying regulatory mechanisms of cell physiology occurring at the translational or post-translational level for an estimated ~73–90% of dinoflagellate genes (Lin, 2011 ; Murray et al, 2016 ).…”

Shifting metabolic priorities among key protistan taxa within and below the euphotic zone

“…Further, transcript-based studies have revealed information on the metabolic adaptations of phytoplankton to specific environmental conditions, such as light or nutrient availability (e.g., Moustafa et al, 2010;Beszteri et al, 2012;Dyhrman et al, 2012;Frischkorn et al, 2014;Liu et al, 2015a;Harke et al, 2017).…”

Metabolomic Fingerprints of Individual Algal Cells Using the Single-Probe Mass Spectrometry Technique

“…N-deplete cultures were generated by first growing cells on L1 media with an N:P ratio of 2.4:1 (88 mM nitrate: 36 mM phosphate) analogous what has been previously described ( Harke et al, 2017 ). This lower ratio stoichiometrically limited cultures in nitrogen and at least three transfers were performed to ensure no carryover from higher nutrient full L1 medium.…”

“…However, while this approach is powerful, it typically requires a fairly good understanding of the underlying molecular mechanisms and genetic diversity of related genes to allow for the derivation of probes or primers. Other studies have applied less targeted, transcriptomic approaches to detect nutrient limitation in marine phytoplankton ( Hwang et al, 2008 ; Cooper et al, 2016 ; Harke et al, 2017 ), but analogous studies are more difficult in diverse natural assemblages for which genetic information is not necessarily available. Given this, our understanding of the degree and severity of nutrient limitation in the marine environment, especially at the induvial species and cellular level, remains poorly constrained.…”