Harmful Algal Bloom-Forming Organism Responds to Nutrient Stress Distinctly From Model Phytoplankton

Abstract

Resources such as nitrogen (N) and phosphorus (P) play an important role in primary production and constraining phytoplankton bloom dynamics. Models to predict bloom dynamics require mechanistic knowledge of algal metabolic shifts in response to resource limitation. For well-studied model phytoplankton like diatoms, this information is plentiful. However, for less-studied groups such as the raphidophytes, there remain significant gaps in understanding metabolic changes associated with nutrient limitation. Using a novel combination of metabolomics and transcriptomics, we examined how the harmful algal bloom-forming raphidophyte Heterosigma akashiwo shifts its metabolism under N- and P-stress. We chose H. akashiwo because of its ubiquity within estuarine environments worldwide, where bloom dynamics are influenced by N and P availability. Our results show that each stress phenotype is distinct in both the allocation of carbon and the recycling of macromolecules. Further, we identified biomarkers of N- and P-stress that may be applied in situ to help modelers and stakeholders manage, predict, and prevent future blooms. These findings provide a mechanistic foundation to model the metabolic traits and trade-offs associated with N- and P-stress in H. akashiwo, and evaluate the extent to which these metabolic responses can be inferred in other phytoplankton groups.

Active reconfiguration of cytoplasmic lipid droplets governs migration of nutrient-limited phytoplankton

“…The yellow-orange regions, initially scattered across the cytosol, represent intracellular LDs in S-1 (false-colour epifluorescence micrographs, Figure 1A, Methods), undergo significant growth as the NO 3 − availability drops to C ~0 μM, 225 h after cells were freshly inoculated with C 0 = 600 μM of NO 3 − (~165 pmole/cell). LDs do not nucleate till t ~ 200 h (Figure 1B), suggesting it is the sustained limitation of NO 3 − , and not PO 4 3− , that drives the growth of the LDs ( 50 ). Over the course of population growth, the cell area increases, reaching a maximum at the onset of the stationary growth stage (~180 μm 2 at t = 396 h), coinciding with ~0 μM availability of NO 3 − .…”

A metabolic lens on phytoplankton physiology

“…For example, these techniques have been used to study how stress induces changes in metabolism of diatoms and coccolithophores [35][36][37], to determine the allocation of luxury nitrogen within diatoms [38], and how particulate and dissolved organic matter changes by depth [39,40] and under a diel cycle [41]. Additionally, these approaches can help reconstruct pathways lacking complete gene annotations [42]. Thus, metabolomics is a promising approach to understand metabolic dynamics within organisms lacking reference genetic material.…”

“…Acclimations describe behaviors these organisms employ over short time scales to respond to changes in the environment. Examples of acclimation strategies include increased production of inorganic nutrient transporters [24,25], upregulation of enzymatic recycling [42], and the release of infochemical signals between community members [158]. Understanding how adaptive and acclimatory strategies distinguish phytoplankton would improve our ability to forecast future phytoplankton community dynamics under changing environmental conditions.…”

“…The use of metabolomics to understand phytoplankton is burgeoning. Recent studies show they viably describe system-level changes in phytoplankton metabolism as a result of stress [42] and diel dynamics of in situ phytoplankton communities [41]. Additionally, due to the paucity of available genomes for most phytoplankton [23], these approaches can help reconstruct pathways that lack complete genomic resolution [42].…”

“…Understanding phytoplankton metabolism can reveal mechanisms responsible for driving the unique acclimations of phytoplankton [42]. For example, the raphidophyte Heterosigma akashiwo acclimates to nitrogen stress by producing greater quantities of triacylglyceride lipids [137].…”