A Model for Carbohydrate Metabolism in the Diatom Phaeodactylum tricornutum Deduced from Comparative Whole Genome Analysis

Abstract

BackgroundDiatoms are unicellular algae responsible for approximately 20% of global carbon fixation. Their evolution by secondary endocytobiosis resulted in a complex cellular structure and metabolism compared to algae with primary plastids.Methodology/Principal FindingsThe whole genome sequence of the diatom Phaeodactylum tricornutum has recently been completed. We identified and annotated genes for enzymes involved in carbohydrate pathways based on extensive EST support and comparison to the whole genome sequence of a second diatom, Thalassiosira pseudonana. Protein localization to mitochondria was predicted based on identified similarities to mitochondrial localization motifs in other eukaryotes, whereas protein localization to plastids was based on the presence of signal peptide motifs in combination with plastid localization motifs previously shown to be required in diatoms. We identified genes potentially involved in a C4-like photosynthesis in P. tricornutum and, on the basis of sequence-based putative localization of relevant proteins, discuss possible differences in carbon concentrating mechanisms and CO2 fixation between the two diatoms. We also identified genes encoding enzymes involved in photorespiration with one interesting exception: glycerate kinase was not found in either P. tricornutum or T. pseudonana. Various Calvin cycle enzymes were found in up to five different isoforms, distributed between plastids, mitochondria and the cytosol. Diatoms store energy either as lipids or as chrysolaminaran (a β-1,3-glucan) outside of the plastids. We identified various β-glucanases and large membrane-bound glucan synthases. Interestingly most of the glucanases appear to contain C-terminal anchor domains that may attach the enzymes to membranes.Conclusions/SignificanceHere we present a detailed synthesis of carbohydrate metabolism in diatoms based on the genome sequences of Thalassiosira pseudonana and Phaeodactylum tricornutum. This model provides novel insights into acquisition of dissolved inorganic carbon and primary metabolic pathways of carbon in two different diatoms, which is of significance for an improved understanding of global carbon cycles.

The Response of Diatom Central Carbon Metabolism to Nitrogen Starvation Is Different from That of Green Algae and Higher Plants

“…In the fresh water green alga Chlamydomonas reinhardtii, on the other hand, excess carbon is reportedly directed to fatty acid biosynthesis (Wang et al, 2009;Moellering and Benning, 2010), and Miller et al (2010) found increased expression of genes involved in lipid biosynthesis in C. reinhardtii when nitrogen was not available. Diatoms are known to store carbon as chrysolaminaran (a b-1,3-glucan) or as lipids (Armbrust et al, 2004;Kroth et al, 2008); however, proteins directly related to the synthesis or degradation of these compounds were not identified in this study. The increase in glycolytic proteins and their transcripts in T. pseudonana seems opposed to the patterns described in higher plants and green algae: while they are increasing carbon stores, T. pseudonana appears to be remobilizing them.…”

Algal evolution in relation to atmospheric CO 2 : carboxylases, carbon-concentrating mechanisms and carbon oxidation cycles

“…Not only is there at least a minimal flux through Rubisco oxygenase and thence to intermediates of a glycolate metabolism pathway despite high levels of expression of CCMs [85,89,90,92,95], but elimination of the pathways of glycolate metabolism is fatal to the organism [85,90]. Previous misgivings [91,92] about the occurrence of the complete PCOC in diatoms have now been largely overcome, although there are still doubts as to the glycerate kinase step [61,88].…”

Metatranscriptomes reveal functional variation in diatom communities from the Antarctic Peninsula

“…Although diatom genomes encode the enzymes necessary for classical C4 metabolism (Reinfelder, 2011), subcellular localizations predict futile inorganic carbon cycling and ATP consumption, and a possible role in excess energy dissipation and/or cellular pH homeostasis (Kroth et al, 2008;Haimovich-Dayan et al, 2012). Although not abundant, the key C4 enzyme pyruvateorthophosphate dikinase (PPDK) was uniquely expressed in WKI, and phosphoenol pyruvate carboxylase (PEPC) was also over-represented (Supplementary Table S1).…”

“…In contrast to ammonium and urea transporters discussed in the previous section, nitrate transporters were less abundant in the more oceanic BFS community, despite high NO 3 − levels in the water column (Figure 1b). The Calvin cycle marker genes sedoheptulose bisphosphatase (SBP) and fructose bisphosphatase (FBP) (Parker and Armbrust, 2005;Kroth et al, 2008) were both most abundant in BFS ( Figure 5) indicating that N availability is not affecting these processes. These enrichment patterns therefore appear to reflect a physiological stance towards the uptake of reduced N sources, consistent with experimental evidence that NH 4 + limits phytoplankton growth in Fesufficient areas of the Southern Ocean (Agustí et al, 2009), such as the BFS and the Antarctic Peninsula (Martin et al, 1990;Sañudo-Wilhelmy et al, 2002).…”