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The urea cycle in diatoms. Scheme showing the principal components of the diatom urea cycle. Genes encoding enzymes of bacterial origin are indicated in purple, metazoan origin in black, and red algal origin in red. Those with uncertain affiliation are shaded in blue. Abbreviations: Agm, agmatinase; Arg, arginase; ASL, argininosuccinate lyase; AsuS, argininosuccinate synthase; CK, carbamate kinase; OCD, ornithine cyclodeaminase; OdC, ornithine decarboxylase; OTC, ornithine transcarbamylase; unCPS, mitochondrial carbamoyl phosphate synthase III; Ure, urease.
Source publication
Diatoms are unicellular, mainly photosynthetic, eukaryotes living within elaborate silicified cell walls and believed to be
responsible for around 40% of global primary productivity in the oceans. Their abundance in aquatic ecosystems is such that
they have on different occasions been described as the insects, the weeds, or the cancer cells of the...
Contexts in source publication
Context 1
... of the first surprises to emerge from the sequencing of diatom genomes was the presence of an apparently fully functional urea cycle (Fig. 5) (Armbrust et al., 2004). Diatoms were, in fact, the first photosynthetic organisms to contain all the genes for such a cycle, and so it was of great interest to understand its role in the context of a photosyn- thetic cell. Prior to its discovery in diatoms, it was believed to have been a metazoan innovation, invented to cope with the ...
Context 2
... known as unCPS (Allen AE et al., 2011), which provides the substrate carbamoyl phosphate for the cycle (Fig. 5). Although absent in plants, in metazoans it plays an important role in vertebrate metabolic adaptations (Anderson, 1980;Guppy, 1986;Mommsen and Walsh, 1989;Hong et al., 1994;Lawson et al., 1996;Holden et al., 1999). Phylogenetic analysis of the unCPS sequences from T. pseudonana and P. tricornutum revealed their similarity with the ...
Context 3
... components of the diatom urea cycle closely resemble those found in the metazoan cycle from a func- tional point of view, although the genes do not all appear to be of exosymbiont origin (Fig. 5). Furthermore, diatom genomes appear to encode several enzymes acquired by horizontal gene transfer from bacteria that potentially can greatly expand the functionality of the cycle with respect to its animal counterpart. Of particular interest, both diatom nuclear genomes encode an ornithine cyclodeaminase (OCD), predicted to convert ...
Context 4
... are precursors for polyamines such as spermidine and putrescine (Kröger and Poulsen, 2008), which are, in turn, converted into highly modified long-chain polyamines that are used for building the diatom-specific siliceous cell walls (Kröger and Poulsen, 2008). Both these offshoots of the urea cycle are probably enabled by bacterial genes (Fig. 5). Hence, the diatom urea cycle appears to play an important role in building organic nitrogen compounds that are particularly critical for building the unique features of diatom cells. In addition, it was proposed that the urea cycle is connected to glutamine synthetase/glutamate synthase (GS/GOGAT) and to the tricarboxylic acid (TCA) ...
Context 5
... play an important role in building organic nitrogen compounds that are particularly critical for building the unique features of diatom cells. In addition, it was proposed that the urea cycle is connected to glutamine synthetase/glutamate synthase (GS/GOGAT) and to the tricarboxylic acid (TCA) cycle through the aspartate- argininosuccinate shunt (Fig. 5). Such interactions are not unique to diatoms, but it is of interest that the shunt provides an additional point of integration for the urea cycle into central metabolism. In summary, the urea cycle appears to function in the recycling and biosynthesis of organic nitrogen compounds, rather than for their breakdown as in animals. Due to ...
Citations
... We suggest that these characteristic features of energy partitioning and the metabolome in C. priscuii compared to those of the mesophiles can be accounted for, in part, by the significant genetic redundancy reported for C. priscuii (Zhang et al. 2021) as well as the other photopsychrophiles such as Chlamydomonas ICE-L ) and the diatom, Fragilariopsis cylindrus (Mock et al. 2017). The superior stress tolerance of diatoms typically involves close energetic coupling of chloroplasts and mitochondria with unusual plastid transporters (Liu at al. 2022), allowing facile transfer of reduction equivalents to mitochondria for dissipation in alternative electron flow routes (Bailleul et al. 2015;Prihoda et al. 2012). It has been also reported that the morphological plasticity and the constitutive protection of thylakoid membranes allows the Antarctic alga, Prasiola antarctica, to survive and thrive in contrasting harsh environments (Arzac et al. 2024). ...
Photostasis is the light-dependent maintenance of energy balance associated with cellular homeostasis in photoautotrophs. We review evidence that illustrates how photosynthetic adaptation in polar photoautrophs such as aquatic green algae, cyanobacteria, boreal conifers as well as terrestrial angiosperms exhibit an astonishing plasticity in structure and function of the photosynthetic apparatus. This plasticity contributes to the maintenance of photostasis, which is essential for the long-term survival in the seemingly inhospitable Antarctic and Arctic habitats. However, evidence indicates that polar photoautrophic species exhibit different functional solutions for the maintenance of photostasis. We suggest that this reflects, in part, the genetic diversity symbolized by inherent genetic redundancy characteristic of polar photoautotrophs which enhances their survival in a thermodynamically challenging environment.
... This generates less energy, but allows a more rapid supply of ADP and electron carriers to the chloroplast, avoiding photoinhibition due to the lack of these compounds in the chloroplast (Bailleul et al. 2015;Launay et al. 2020). The increase of AOX : Respiration we observed under elevated temperature, despite lower dark respiration and higher photosynthetic rates, suggests that the mitochondrion was acting as an electron sink as a stress response mechanism (Allen et al. 2008;Prihoda et al. 2012). Regarding the detoxification of oxidative stress, we observed an overall lower activity of most antioxidant enzymes under high temperatures (GPx, GST, SOD-Mn; CAT under low N : P). ...
Phytoplankton are responsible for about 90% of the oceanic primary production, largely supporting marine food webs, and actively contributing to the biogeochemical cycling of carbon. Yet, increasing temperature and pCO2, along with higher dissolved nitrogen: phosphorus ratios in coastal waters are likely to impact phytoplankton physiology, especially in terms of photosynthetic rate, respiration, and dissolved organic carbon (DOC) production. Here, we conducted a full-factorial experiment to identify the individual and combined effects of temperature, pCO2, and N : P ratio on the antioxidant capacity and carbon metabolism of the diatom Phaeodactylum tricornutum. Our results demonstrate that, among these three drivers, temperature is the most influential factor on the physiology of this species, with warming causing oxidative stress and lower activity of antioxidant enzymes. Furthermore, the photosynthetic rate was higher under warmer conditions and higher pCO2, and, together with a lower dark respiration rate and higher DOC exudation, generated cells with lower carbon content. An enhanced oceanic CO2 uptake and an overall stimulated microbial loop benefiting from higher DOC exudation are potential longer-term consequences of rising temperatures, elevated pCO2 as well as shifted dissolved N : P ratios.
... Since they are central to diatom metabolism, chloroplasts must be tightly controlled and quickly repaired and can be expected to feature prominently in response to environmental stressors. Diatoms arose from a secondary endosymbiotic event and have a highly reduced plastid genome and distinctive evolutionary history compared with green algae and higher plants (Prihoda et al., 2012). Genes may have been retained in the plastid because of their importance in maintaining redox balance, their high turnover rates, and consequent need for tight regulation relative to the redox state of the plastid (Nisbet et al., 2004). ...
Marine planktonic diatoms are among the most important contributors to phytoplankton blooms and marine net primary production. Their ecological success has been attributed to their ability to rapidly respond to changing environmental conditions.
Here, we report common molecular mechanisms used by the model marine diatom Thalassiosira pseudonana to respond to 10 diverse environmental stressors using RNA‐Seq analysis.
We identify a specific subset of 1076 genes that are differentially expressed in response to stressors that induce an imbalance between energy or resource supply and metabolic capacity, which we termed the diatom environmental stress response (d‐ESR). The d‐ESR is primarily composed of genes that maintain proteome homeostasis and primary metabolism. Photosynthesis is strongly regulated in response to environmental stressors but chloroplast‐encoded genes were predominantly upregulated while the nuclear‐encoded genes were mostly downregulated in response to low light and high temperature.
In aggregate, these results provide insight into the molecular mechanisms used by diatoms to respond to a range of environmental perturbations and the unique role of the chloroplast in managing environmental stress in diatoms. This study facilitates our understanding of the molecular mechanisms underpinning the ecological success of diatoms in the ocean.
... For example, polyamines such as spermidine and putrescine are derived from the diatom urea cycle. Polyamines are required by both partners: diatoms use polyamines to build their siliceous cell walls, and cyanobacteria require polyamines for heterocyst differentiation (19,20). Unexpectedly, the ReuHH01 genome lacks genes for a complete polyamine biosynthesis pathway (11). ...
A few genera of diatoms are widespread and thrive in low-nutrient waters of the open ocean due to their close association with N2-fixing, filamentous heterocyst-forming cyanobacteria. In one of these symbioses, the symbiont, Richelia euintracellularis, has penetrated the cell envelope of the host, Hemiaulus hauckii, and lives inside the host cytoplasm. How the partners interact, including how the symbiont sustains high rates of N2 fixation, is unstudied. Since R. euintracellularis has evaded isolation, heterologous expression of genes in model laboratory organisms was performed to identify the function of proteins from the endosymbiont. Gene complementation of a cyanobacterial invertase mutant and expression of the protein in Escherichia coli showed that R. euintracellularis HH01 possesses a neutral invertase that splits sucrose producing glucose and fructose. Several solute-binding proteins (SBPs) of ABC transporters encoded in the genome of R. euintracellularis HH01 were expressed in E. coli, and their substrates were characterized. The selected SBPs directly linked the host as the source of several substrates, e.g. sugars (sucrose and galactose), amino acids (glutamate and phenylalanine), and a polyamine (spermidine), to support the cyanobacterial symbiont. Finally, transcripts of genes encoding the invertase and SBPs were consistently detected in wild populations of H. hauckii collected from multiple stations and depths in the western tropical North Atlantic. Our results support the idea that the diatom host provides the endosymbiotic cyanobacterium with organic carbon to fuel N2 fixation. This knowledge is key to understanding the physiology of the globally significant H. hauckii–R. euintracellularis symbiosis.
... As a consequence of the H + -dependent conversion of HCO 3 À into CO 2 in the lumen, the PMF is partially consumed, thereby decreasing the plastidial ATP : NADPH ratio, or rather PMF : electron-transport ratio. In response to this apparent relative 'overreduction', reduction equivalents are exported and directed toward alternative sinks, in this case the mitochondrial oxidative phosphorylation, likely via malate shuttles (Kinoshita et al., 2011;Prihoda et al., 2012). Hence, R O 2 is partly fueled by the imported reduction equivalents from the chloroplast, thus the mitochondrial redox state shifts and R CO 2 is downregulated. ...
Growth rates and other biomass traits of phytoplankton are strongly affected by temperature. We hypothesized that resulting phenotypes originate from deviating temperature sensitivities of underlying physiological processes.
We used membrane‐inlet mass spectrometry to assess photosynthetic and respiratory O2 and CO2 fluxes in response to abrupt temperature changes as well as after acclimation periods in the diatom Phaeodactylum tricornutum.
Abrupt temperature changes caused immediate over‐ or undershoots in most physiological processes, that is, photosynthetic oxygen release (PSO2), photosynthetic carbon uptake (PSCO2), and respiratory oxygen release (RO2). Over acclimation timescales, cells were, however, able to re‐adjust their physiology and revert to phenotypic ‘sweet spots’.
Respiratory CO2 release (RCO2) was generally inhibited under high temperature and stimulated under low‐temperature settings, on abrupt as well as acclimation timescales. Such behavior may help mitochondria to stabilize plastidial ATP : NADPH ratios and thus maximize photosynthetic carbon assimilation.
... One of the most relevant changes during the formation of spores is the deposition of two thick heteromorphic siliceous thecae that confer mechanical protection to the spores. Metabolites such as spermidine and long-chain polyamines (LCA) are involved in the synthesis of the organic component of the siliceous cell wall and their synthesis is connected to the urea cycle and the TCA cycle ( [39]). Evidence of spermidine production, another polyamine, came from the upregulation of several spermidine synthases, especially when spores were present (Fig. 4, Figure S3e, Table S6). ...
Background
Dormancy is widespread in both multicellular and unicellular organisms. Among diatoms, unicellular microalgae at the base of all aquatic food webs, several species produce dormant cells (spores or resting cells) that can withstand long periods of adverse environmental conditions.
Results
We present the first gene expression study during the process of spore formation induced by nitrogen depletion in the marine planktonic diatom Chaetoceros socialis. In this condition, genes related to photosynthesis and nitrate assimilation, including high-affinity nitrate transporters (NTRs), were downregulated. While the former result is a common reaction among diatoms under nitrogen stress, the latter seems to be exclusive of the spore-former C. socialis. The upregulation of catabolic pathways, such as tricarboxylic acid cycle, glyoxylate cycle and fatty acid beta-oxidation, suggests that this diatom could use lipids as a source of energy during the process of spore formation. Furthermore, the upregulation of a lipoxygenase and several aldehyde dehydrogenases (ALDHs) advocates the presence of oxylipin-mediated signaling, while the upregulation of genes involved in dormancy-related pathways conserved in other organisms (e.g. serine/threonine-protein kinases TOR and its inhibitor GATOR) provides interesting avenues for future explorations.
Conclusions
Our results demonstrate that the transition from an active growth phase to a resting one is characterized by marked metabolic changes and provides evidence for the presence of signaling pathways related to intercellular communication.
... In diatoms, a cross talk between mitochondria and chloroplasts under stress was proposed to be mediated by the AOX, which has a calmodulin-like calcium-binding motif, suggesting thus regulation by calcium. 94 In C. reinhardtii, less is known about calcium signaling pathways, but some evidences are linking calcium to stress responses-in fact, a chloroplast calcium sensor is required for photoacclimation in high light conditions 81 and phototaxis, contributing to photoprotection to avoid excess exposure to light. ...
... The second step led to the rise of Dinoflagellates, Cryptophytes, Euglenida, and Heterokont groups that consist of brown algae (Phaeophyceae), yellow-green algae (Xanthophyceae), golden algae (Chrysophyceae), and diatom (Bacillariophyceae) [13]. In the first stage of endosymbiosis (1.8 billion years ago), cyanobacteria invaded non-photosynthetic eukaryotes; which causes the recent plastids of eukaryotic cells to have a monophyletic origin [15]. The second is the subsequent spread of this organelle through secondary endosymbiosis to a diverse array of photosynthetic lineages collectively referred to as 'chromalveolates' (for example diatoms, haptophytes, and dinoflagellates) that are dominant marine primary producers [15]. ...
... In the first stage of endosymbiosis (1.8 billion years ago), cyanobacteria invaded non-photosynthetic eukaryotes; which causes the recent plastids of eukaryotic cells to have a monophyletic origin [15]. The second is the subsequent spread of this organelle through secondary endosymbiosis to a diverse array of photosynthetic lineages collectively referred to as 'chromalveolates' (for example diatoms, haptophytes, and dinoflagellates) that are dominant marine primary producers [15]. ...
... These include a complete plastid-targeted ornithine cycle, which interacts with a complete mitochondria-targeted urea cycle in diatom amino acid metabolism and recycling (Allen et al., 2011;Nonoyama et al., 2019); a complex suite of plastid-targeted proteins involved in iron storage, acquisition, and stress tolerance (Gao et al., 2021); and elaborate CO 2 concentration and carbon metabolism systems (e.g., a complete glycolysis-gluconeogenesis pathway) not known in plant plastids (Marchand et al., 2018;Nonoyama et al., 2019). Moreover, many of these diatom-associated plastid metabolic innovations, including but not limited to central nitrogen and carbon metabolism, depend on intricate crosstalk between diatom plastids and mitochondria, which typically show close proximity to one another in diatom cells (Prihoda et al., 2012;Bailleul et al., 2015;Uwizeye et al., 2020). These plastid-related novel metabolic activities may depend on transporter innovations across the four membranes, or metabolite exchanges between organelles (Shai et al., 2016;Dorrell et al., 2017;Mix et al., 2018). ...
... The intricate metabolic connections between diatom plastids and mitochondria (Prihoda et al., 2012;Bailleul et al., 2015;Uwizeye et al., 2020) likely depend on transporters that transfer metabolites either between the two organelles, or with adjacent compartments such as the peroxisome (Shai et al., 2016;Dorrell et al., 2017;Mix et al., 2018). In order to find potential plastid transporters that may be related to this cross-talk, the average Pearson correlation coefficient values were calculated between 66 plastid transporters and 34 genes from the mitochondria genome, for which equivalent relative fold-expression change data were present in published microarray data (Oudot-Le Secq et al.; Ashworth et al., 2016). ...
... The transporter architecture of the diatom plastid may underpin its unique metabolic potential (Prihoda et al., 2012;Marchand et al., 2018;Nonoyama et al., 2019). Previously, for example, Bailleul et al. have proposed that import of mitochondrial ATP and export of plastid NADPH facilitates diatom photoacclimation to high light and post-illumination conditions (Bailleul et al., 2015). ...
Diatoms are an important group of algae, contributing nearly 40% of total marine photosynthetic activity. However, the specific molecular agents and transporters underpinning the metabolic efficiency of the diatom plastid remain to be revealed. We performed in silico analyses of 70 predicted plastid transporters identified by genome-wide searches of Phaeodactylum tricornutum. We considered similarity with Arabidopsis thaliana plastid transporters, transcriptional co-regulation with genes encoding core plastid metabolic pathways and with genes encoded in the mitochondrial genomes, inferred evolutionary histories using single-gene phylogeny, and environmental expression trends using Tara Oceans meta-transcriptomics and meta-genomes data. Our data reveal diatoms conserve some of the ion, nucleotide and sugar plastid transporters associated with plants, such as non-specific triose phosphate transporters implicated in the transport of phosphorylated sugars, NTP/NDP and cation exchange transporters. However, our data also highlight the presence of diatom-specific transporter functions, such as carbon and amino acid transporters implicated in intricate plastid-mitochondria crosstalk events. These confirm previous observations that substrate non-specific triose phosphate transporters (TPT) may exist as principal transporters of phosphorylated sugars into and out of the diatom plastid, alongside suggesting probable agents of NTP exchange. Carbon and amino acid transport may be related to intricate metabolic plastid-mitochondria crosstalk. We additionally provide evidence from environmental meta-transcriptomic/meta- genomic data that plastid transporters may underpin diatom sensitivity to ocean warming, and identify a diatom plastid transporter (J43171) whose expression may be positively correlated with temperature.
... One of the most relevant changes during the formation of spores is the deposition of two thick heteromorphic siliceous thecae that confer mechanical protection to the spores. Metabolites such as proline and long-chain polyamines (LCA) are involved in the synthesis of the organic component of the siliceous cell wall and their synthesis is connected to the urea cycle and the TCA cycle ( [37]). Transcripts related to the proline biosynthesis were not particularly overexpressed at any sampling point, but evidence of spermidine production, another polyamine, came from the upregulation of several spermidine synthases, especially when spores were present (Table S4). ...
Background
Dormancy is widespread in both multicellular and unicellular organisms. Among diatoms, unicellular microalgae at the base of all aquatic food webs, several species produce dormant cells (spores or resting cells) that can withstand long periods of adverse environmental conditions.
Results
We present the first gene expression study during the process of spore formation in the marine planktonic diatom Chaetoceros socialis. Spore formation was induced by nitrogen depletion. Genes related to photosynthesis and nitrate assimilation, including high-affinity nitrate transporters (NTRs), were downregulated. While the former result is a common reaction among diatoms under nitrogen stress, the latter seems to be exclusive of the spore-former C. socialis. The upregulation of catabolic pathways, such as tricarboxylic acid cycle, glyoxylate cycle and beta-oxidation, suggests that this diatom could use lipids as a source of energy during the process of spore formation. Furthermore, the upregulation of a lipoxygenase and several aldehyde dehydrogenases (ALDHs) advocates the presence of oxylipin-mediated signalling, while the upregulation of genes involved in dormancy-related pathways conserved in other organisms (e.g. serine/threonine-protein kinases TOR and its inhibitor GATOR) provides interesting avenues for future explorations.
Conclusions
Our results demonstrate that the transition from an active growth phase to a resting one is characterized by marked metabolic changes and provide evidence for the presence of signalling pathways related to intercellular communication.
