Interactive effects of iron and light limitation on the molecular physiology of the Southern Ocean diatom Fragilariopsis kerguelensis

Abstract

The polar diatom Fragilariopsis kerguelensis is ubiquitous in Southern Ocean waters and is a major responder to iron fertilization, encountering large gradients in iron concentrations and light availability. We performed a comparative transcriptomic analysis of F. kerguelensis grown under varying iron and light conditions in order to investigate the molecular underpinnings that may explain its physiological response to iron and light limitation. Low iron reduced growth rates more than low light, but there was not an additive effect of low iron and low light on growth rate. Low iron treatments (saturating and low light) had the largest transcriptomic response; however, expression patterns were more similar in low light treatments (high and low iron). Under iron and light limitation, carbon fixation and amino acid, ribosome, and sulfur metabolisms were overrepresented relative to the control (iron replete, saturating light). Transcripts of genes encoding for the proteins aquaporin, proteorhodopsin, plastocyanin, and flavodoxin were overrepresented to the greatest extent in the low iron/low light treatment, indicating there may be an additive effect of iron/light colimitation at the molecular level. Iron and light replete cells demonstrated increased expression of genes encoding for the proteins ferritin, carbonic anhydrase, and numerous irondependent proteins relative to the growth-limiting treatments. This transcriptome analysis reveals mechanisms that may underpin the ecological success of this diatom in low iron and light environments, highlighting the important role of diversified photosynthetic isoforms, iron acquisition, unique detoxification mechanisms of reactive oxygen species, and metabolic shifts in amino acid recycling and carbon metabolism.

Transitioning global change experiments on Southern Ocean phytoplankton from lab to field settings: Insights and challenges

“…We cross‐compared our findings to explore whether we can obtain insights into the individual environmental factors we manipulated (Table 2). The proteomic trends we observed in the photosystem I pathway in the control mesocosm are corroborated by previous work (Moreno et al 2020). We also detected flavodoxin and chloroplast ferredoxin dependent NADH oxidoreductase proteins in some taxa.…”

“…Others detected that phytoplankton photosynthetic competency and photosynthetic apparatus proteins decrease under low Fe alone (Wu et al 2019;Moreno et al 2020); we observed the opposite trend. In our manipulation, five environmental drivers were altered, whereas in experiments against which we compare our results, one or two drivers were amended.…”

“…Many photosystem proteins were at relatively lower abundances in the 2100 mesocosm compared to the control. This trend could be due to an up-regulation of photosystem protein production in the control to compensate for photosynthetically unfavorable conditions, as also seen in Moreno et al (2020) or resulting from down-regulation of photosystem proteins due to higher irradiance (Table 2). Additionally, the elevated pCO 2 (decreased pH) in the 2100 mesocosm may have stimulated an increase in enzyme-driven, as opposed to more passive, H + efflux to maintain intracellular pH (Raven and Smith 1974;Taylor et al, 2011), a function attributed to Vtype proton ATPase (Toei et al, 2010).…”

Iron metabolism strategies in diatoms

“…However, T. oceanica maintained high growth rates (~80% of the rate in iron-replete conditions) in low-iron media that restricted the growth of T. weissflogii to ~20% of its iron-replete growth rate. Two studies confirmed similar streamlining in F. kerguelensis and P. granii, polar diatoms that are abundant in the Southern Ocean and the Arctic Ocean, respectively ( Cohen et al , 2018a ; Moreno et al , 2020 ). In P. granii , the gene encoding PSI subunit IV ( PSAE ) was almost 4-fold more highly expressed under iron-replete conditions, and protein levels were more abundant by 35-fold compared with their levels under conditions of iron limitation ( Cohen et al , 2018a ).…”

“…3 ). In a recent study, Moreno et al (2020) investigated the response of three isoforms of PETE to iron in this species, and found that only two were significantly over-represented under low-iron conditions. In T. oceanica, which encodes PETE together with two functional copies of PETJ , the relative expression of plastocyanin was sensitive to iron status, while two genes encoding cytochrome c 6 were weakly but constitutively expressed ( Lommer et al , 2012 ).…”