Nitrogen and Iron Availability Drive Metabolic Remodeling and Natural Selection of Diverse Phytoplankton during Experimental Upwelling

ABSTRACT Nearly half of carbon fixation and primary production originates from marine phytoplankton, and much of it occurs in episodic blooms in upwelling regimes. Here, we simulated blooms limited by nitrogen and iron by incubating Monterey Bay surface waters with subnutricline waters and inorganic nutrients and measured the whole-community transcriptomic response during mid- and late-bloom conditions. Cell counts revealed that centric and pennate diatoms (largely Pseudo-nitzschia and Chaetoceros spp.) were the major blooming taxa, but dinoflagellates, prasinophytes, and prymnesiophytes also increased. Viral mRNA significantly increased in late bloom and likely played a role in the bloom’s demise. We observed conserved shifts in the genetic similarity of phytoplankton populations to cultivated strains, indicating adaptive population-level changes in community composition. Additionally, the density of single nucleotide variants (SNVs) declined in late-bloom samples for most taxa, indicating a loss of intraspecific diversity as a result of competition and a selective sweep of adaptive alleles. We noted differences between mid- and late-bloom metabolism and differential regulation of light-harvesting complexes (LHCs) under nutrient stress. While most LHCs are diminished under nutrient stress, we showed that diverse taxa upregulated specialized, energy-dissipating LHCs in low iron. We also suggest the relative expression of NRT2 compared to the expression of GSII as a marker of cellular nitrogen status and the relative expression of iron starvation-induced protein genes (ISIP1, ISIP2, and ISIP3) compared to the expression of the thiamine biosynthesis gene (thiC) as a marker of iron status in natural diatom communities. IMPORTANCE Iron and nitrogen are the nutrients that most commonly limit phytoplankton growth in the world’s oceans. The utilization of these resources by phytoplankton sets the biomass available to marine systems and is of particular interest in high-nutrient, low-chlorophyll (HNLC) coastal fisheries. Previous research has described the biogeography of phytoplankton in HNLC regions and the transcriptional responses of representative taxa to nutrient limitation. However, the differential transcriptional responses of whole phytoplankton communities to iron and nitrogen limitation has not been previously described, nor has the selective pressure that these competitive bloom environments exert on major players. In addition to describing changes in the physiology of diverse phytoplankton, we suggest practical indicators of cellular nitrogen and iron status for future monitoring.