Integrative omics identification, evolutionary and structural analysis of low affinity nitrate transporters in diatoms, diNPFs

Abstract

Diatoms are one of the major and most diverse groups of phytoplankton, with chimeric genomes harbouring a combination of genes of bacterial, animal and plant origin. They have developed sophisticated mechanisms to face environmental variations. In marine environments, nutrients concentration shows significant temporal and spatial variability, influencing phytoplankton growth. Among nutrients, nitrogen, present at micromolar levels, is often a limiting resource. Here, we report a comprehensive characterization of the Nitrate Transporter 1/Peptide Transporter Family (NPF) in diatoms, diNPFs. NPFs are well characterized in many organisms where they recognize a broad range of substrates, ranging from short-chained di- and tri-peptides in bacteria, fungi and mammals to a wide variety of molecules including nitrate in higher plants. Scarce information is available for diNPFs. We integrated-omics, phylogenetic, structural and expression analyses, to infer information on their role in diatoms. diNPF genes diverged to produce two distinct clades with strong sequence and structural homology with either bacterial or plant NPFs, with different predicted sub-cellular localization, suggesting that the divergence resulted in functional diversification. Moreover, transcription analysis of diNPF genes under different laboratory and environmental growth conditions suggests that diNPF diversification led to genetic adaptations that might contribute to diatoms ability to flourish in diverse environmental conditions.

Gene expression during the formation of resting spores in the marine diatom Chaetoceros socialis

“…We could not detect any low-a nity nitrate transporters (NPFs) in C. socialis, thus con rming the results recently obtained for various Chaetoceros species in which NPFs are missing ( [32]); this could support the suggestion that the species of this genus can preferentially use ammonia, possibly from bacteria, as a source of N in case of uctuating nitrate concentrations ( [33]). While the expression of ammonium transporters was somehow variable in our dataset, the high-a nity urea active transporters DUR3 were upregulated at least in one sampling point, with two of them already differentially expressed at T2 (Figure 4, Table S4).…”

A metabolic, phylogenomic and environmental atlas of diatom plastid transporters from the model species Phaeodactylum

“…Marchand et al presented overviews of the localization and activity of ion and metabolite plastid transporters from algae to land plants (Marchand et al, 2018;Marchand et al, 2020); and Brownlee et al recently summarized key mechanisms of diatom key nutrient transport and acquisition (Brownlee et al, 2022). Specific studies have further elaborated on the diversity of diatom plastid sugar transporters (which typically transport triose phosphates) (Moog et al, 2015;Moog et al, 2020); low CO 2 induced HCO − 3 transporters (SLC) (Nakajima et al, 2013;Matsuda et al, 2017;Tsuji et al, 2017); nitrate/peptide transporters (Santin et al, 2021); and nucleotide triphosphate transporters (Ast et al, 2009).…”

Sensing and Signalling in Diatom Responses to Abiotic Cues

“…NPF genes have been found in the genomes of several diatom species (Rogato et al 2015). Considering the low concentration of nitrate in the oceans, it has been hypothesized that the diatom NPFs, predicted to be located in the plasma membrane, could bind alternative substrates such as oligopeptides or hormones and be involved in the control of different processes such as interactions between diatoms and bacteria (Santin et al 2021). A similar function in nutrient sensing has been proposed for the silicic acid transporter (SIT) of T. pseudonana (Shrestha and Hildebrand 2015).…”