Genomic adaptation of the picoeukaryote Pelagomonas calceolata to iron-poor oceans revealed by a chromosome-scale genome sequence

Abstract

The smallest phytoplankton species are key actors in oceans biogeochemical cycling and their abundance and distribution are affected with global environmental changes. Among them, algae of the Pelagophyceae class encompass coastal species causative of harmful algal blooms while others are cosmopolitan and abundant. The lack of genomic reference in this lineage is a main limitation to study its ecological importance. Here, we analysed Pelagomonas calceolata relative abundance, ecological niche and potential for the adaptation in all oceans using a complete chromosome-scale assembled genome sequence. Our results show that P. calceolata is one of the most abundant eukaryotic species in the oceans with a relative abundance favoured by high temperature, low-light and iron-poor conditions. Climate change projections based on its relative abundance suggest an extension of the P. calceolata habitat toward the poles at the end of this century. Finally, we observed a specific gene repertoire and expression level variations potentially explaining its ecological success in low-iron and low-nitrate environments. Collectively, these findings reveal the ecological importance of P. calceolata and lay the foundation for a global scale analysis of the adaptation and acclimation strategies of this small phytoplankton in a changing environment.

The Bay of Bengal exposes abundant photosynthetic picoplankton and newfound diversity along salinity‐driven gradients

“…We observed sharp transitions among pelagophytes at the surface, with PcC contributing the most at stations S1‐S6 whereas PEC‐VIII dominated S7‐S18 (Figure S9). P. calceolata has been increasingly recognized as a widely distributed oceanic photosynthetic picoeukaryote (Duerschlag et al, 2022; Guérin et al, 2022; Worden et al, 2012) that is particularly important at the SCM/DCM in mesotrophic and oligotrophic stations in the Eastern North Pacific, the Sargasso Sea (Choi et al, 2020; Dupont et al, 2015), and the South Pacific Subtropical Ocean (Duerschlag et al, 2022). Surprisingly, unlike these prior studies, here, P. calceolata was not among the dominant eukaryotic phytoplankton at the SCM.…”

Nitrogen metabolism in the picoalga Pelagomonas calceolata: disentangling cyanate lyase function under different nutrient conditions.

“…The NIT-sensing gene carrying a transmembrane domain is overexpressed in low-nitrate samples but not differentially expressed when the nitrate is replaced by another nitrogen source. This gene has been shown to be overexpressed by P. calceolata in low-nitrate environments (Dupont et al, 2015; Guérin et al, 2022) but is not significant in our environmental DESeq2 analysis. The two other nitrate-sensing genes carry a serine–threonine/tyrosine kinase domain, and might play a role in phosphorylation-based signal transduction.…”

“…Among them, genes coding for arginase, urease and cyanate lyase may suggest the capacity of organic nitrogen compounds metabolism. In the environment, several nitrogen ions transporters, nitrate and nitrite reductases, glutamine synthetase, nitrate/nitrite sensing proteins and the cyanate lyase are significantly expressed at higher levels in low-N environments (Dupont et al, 2015; Guérin et al, 2022). Here we cultivated two P. calceolata strains under high or limited nitrate conditions and tested the effect of several inorganic (nitrate, ammonia) and organic (urea, cyanate) sources of nitrogen on P. calceolata growth.…”

Phago-mixotrophy of small eukaryotic phytoplankton might alleviate iron limitation in HNLC Southern Ocean

“…Other adaptations to low iron conditions besides phago-mixotrophy were likely present in the community of SA cycles, especially within phototrophic picoeukaryotes. Based on genome analysis, Pelagophyceae and Phaeocystis antarctica suggests a physiological advantage in iron uptake and storage (Guérin et al 2022; Strzepek et al 2011). Mamiellophyceae species Bathycoccus prasinos is suggested to overcome iron limitation by nickel acquisition (Simmons et al 2016).…”