Complex Response of the Chlorarachniophyte Bigelowiella natans to Iron Availability

Abstract

The productivity of the ocean is largely dependent on iron availability, and marine phytoplankton have evolved sophisticated mechanisms to cope with chronically low iron levels in vast regions of the open ocean. By analyzing the metabarcoding data generated from the Tara Oceans expedition, we determined how the global distribution of the model marine chlorarachniophyte Bigelowiella natans varies across regions with different iron concentrations. We performed a comprehensive proteomics analysis of the molecular mechanisms underpinning the adaptation of B. natans to iron scarcity and report on the temporal response of cells to iron enrichment. Our results highlight the role of phytotransferrin in iron homeostasis and indicate the involvement of CREG1 protein in the response to iron availability. Analysis of the Tara Oceans metagenomes and metatranscriptomes also points to a similar role for CREG1, which is found to be widely distributed among marine plankton but to show a strong bias in gene and transcript abundance toward iron-deficient regions. Our analyses allowed us to define a new subfamily of the CobW domain-containing COG0523 putative metal chaperones which are involved in iron metabolism and are restricted to only a few phytoplankton lineages in addition to B. natans. At the physiological level, we elucidated the mechanisms allowing a fast recovery of PSII photochemistry after resupply of iron. Collectively, our study demonstrates that B. natans is well adapted to dynamically respond to a changing iron environment and suggests that CREG1 and COG0523 are important components of iron homeostasis in B. natans and other phytoplankton. IMPORTANCE Despite low iron availability in the ocean, marine phytoplankton require considerable amounts of iron for their growth and proliferation. While there is a constantly growing knowledge of iron uptake and its role in the cellular processes of the most abundant marine photosynthetic groups, there are still largely overlooked branches of the eukaryotic tree of life, such as the chlorarachniophytes. In the present work, we focused on the model chlorarachniophyte Bigelowiella natans, integrating physiological and proteomic analyses in culture conditions with the mining of omics data generated by the Tara Oceans expedition. We provide unique insight into the complex responses of B. natans to iron availability, including novel links to iron metabolism conserved in other phytoplankton lineages.

Whole-genome scanning reveals environmental selection mechanisms that shape diversity in populations of the epipelagic diatom Chaetoceros

“…The former are found in light-harvesting complexes of the photosynthetic apparatus while the latter form a large family of metal chaperones associated with metal homeostasis processes either with zinc, iron, or cobalt molecules [ 55 , 56 ]. Interestingly, both these functions may have a link with iron availability status, as phytoplankton can cope with iron limitation through remodelling of light-harvesting complexes, while some CobW proteins may exert iron-responsive patterns [ 57 , 58 ]. Comparing the frequency of these variants among the 2 genomes, both ARC_217 and SOC_37 populations were found at stations TARA_201 (Arctic Archipelago) and TARA_173 (Kara-Laptev) and showed elevated frequency of this variant at the former, whereas those at station TARA_173 exhibited lower frequency (Tables E and F in S7 Table ).…”

Flow cytometry-based study of model marine microalgal consortia revealed an ecological advantage of siderophore utilization by the dinoflagellate Amphidinium carterae

“…Iron starvation-induced proteins and the P. tricornutum cellular repressor of E1A stimulated genes 1 (CREG1) were downregulated more than 2-fold 6 h after iron enrichment. These proteins are known to be major markers of iron limitation [12] , [21] . Proteins that changed more than 2-fold only 24 h after iron enrichment included other ISIPs, flavodoxins (downregulated) and ascorbate peroxidase, PsbC, SOD1 (upregulated).…”

“…Amphidinium carterae (CCMP1314), Bigelowiella natans (CCMP2755), Eutreptiella gymnastica (K-0333), Emiliania huxleyi (CCMP371), Heterocapsa triquetra (CCMP449), Phaeodactylum tricornutum (CCMP2561), Tetraselmis sp. (CCMP961), Thalassiosira oceanica (CCMP1005) and Thalassiosira pseudonana (CCMP1335) were grown at 18 °C under a 12 h/12 h light (50 μmol m −2 s −1 )/dark regime in filtered modified f (Mf) medium, as described previously [12] . The composition of the Mf medium was as follows: 40 g/l sea salts; 75 mg/l NaNO 3 ; 2.66 mg/l NH 4 NO 3 ; 22.8 mg/l Na 2 SiO 3 ·5H 2 O; 15 mg/l NaH 2 PO 4 ; 1 ml of trace metal stock (200 mg/l MnCl 2 ·4H 2 O; 40 mg/l ZnSO 4 ·7H 2 O; 20 mg/l Na 2 MoO 4 ·2H 2 O; 14 mg/l CoCl 2 ·6H 2 O; 10 mg/l Na 3 VO 4 ·nH 2 O; 10 mg/l NiCl 2 ; 10 mg/ml H 2 SeO 3 ) and 1 ml of vitamin stock (20 mg/l thiamine-HCl, 1 mg/ml biotin, 1 mg/ml B12).…”

Whole-genome scanning reveals selection mechanisms in epipelagic Chaetoceros diatom populations

“…The former are found in light-harvesting complexes of the photosynthetic apparatus while the latter form a large family of metal chaperones associated with metal homeostasis processes either with zinc, iron or cobalt molecules (Haas et al 2009; Hsieh et al 2013). Interestingly, both these functions may have a link with iron availability status, as phytoplankton can cope with iron limitation through remodelling of light-harvesting complexes, while some CobW proteins may exert iron-responsive patterns (Behrenfeld and Milligan 2013; Kotabova et al 2021). Comparing the frequency of these variants among the two genomes, both ARC_217 and SOC_37 populations were found at stations TARA_201 (Arctic archipelago) and TARA_173 (Kara-Laptev) and showed elevated frequency of this variant at the former, whereas those at station TARA_173 exhibited lower frequency (Supplementary Table S6E-F).…”