Amino Acid Catabolism During Nitrogen Limitation in Phaeodactylum tricornutum

Abstract

Diatoms can accumulate high levels of triacylglycerols (TAGs) under nitrogen depletion and have attracted increasing attention as a potential system for biofuel production. In Phaeodactylum tricornutum, a model diatom, about 40% of lipid is synthesized from the breakdown of cellular components under nitrogen starvation. Our previous studies indicated that carbon skeletons from enhanced branched-chain amino acid (BCAA) degradation under nitrogen deficiency contribute to TAG biosynthesis in P. tricornutum. In this review, we outlined the catabolic pathways of all 20 amino acids based on the genome, transcriptome, proteome, and metabolome data. The contribution of these amino acid catabolic pathways to TAG accumulation was also analyzed.

Keywords: amino acid; catabolism; diatom; nitrogen; triacylglycerols.

FIGURE 1

Amino acid catabolic pathways in P. tricornutum. The yellow text box represents amino acids, the orange text boxes indicate metabolites that could enter the TCA cycle, the white text boxes with green borders indicate other metabolites, and the white text boxes with black borders indicate the enzymes. The different font colors of enzymes represent different predicted subcellular locations: plastid localization in green font; mitochondria location in blue font; multiple isoenzymes with the plastid and mitochondria localization in orange font; those with mitochondria and other location in brown font; those with plastid and other localization in purple font; and those with plastid, mitochondria, and other localization in red font. Up-regulated genes are indicated with red lines, and down-regulated genes with blue lines. (A) Catabolic pathways of all 20 amino acids. (B) Catabolic pathways of BCAAs. (C) Catabolic pathways of lysine. (D) Catabolic pathways of tyrosine. (E) Catabolic pathways of serine, methionine, cysteine, and glycine. ACAT, acetyl-CoA C-acyltransferase (EC2.3.1.16); ACD, acyl-CoA dehydrogenase (EC1.3.8.1); AGX, alanine–glyoxylate aminotransferase (EC:2.6.1.44); AHCYL, adenosylhomocysteinase (EC3.3.1.1); ALDH, aldehyde dehydrogenase (EC1.2.1.31); ALDH18A1, delta-1-pyrroline-5-carboxylate synthetase (EC2.7.2.11 and EC1.2.1.41); ALDH4A1, 1-pyrroline-5-carboxylate dehydrogenase (EC1.2.1.88); ALS, acetolactate synthase (EC2.2.1.6); ALT, alanine transaminase (EC2.6.1.2); Arg, arginase (EC3.5.3.1); ASA, aspartate–ammonia ligase (EC6.3.1.1); ASL, argininosuccinate lyase (EC4.3.2.1); ASNase, asparaginase (EC3.5.1.1); ASNS, asparagine synthase (EC6.3.5.4); ASS, argininosuccinate synthase (EC6.3.4.5); AST, aspartate aminotransferase (EC2.6.1.1); BCAT, branched-chain amino acid transaminase (EC2.6.1.42); BCKDH, branched-chain α-keto acid dehydrogenase (EC1.2.4.4); CBL, cysteine-S-conjugate beta-lyase (EC4.4.1.13); Cbs, cystathionine beta-synthase (EC4.2.1.22); CMT, DNA (cytosine-5)-methyltransferase (EC2.1.1.37); CPSII, carbamoyl-phosphate synthase II (EC6.3.5.5); CTH, cystathionine gamma-lyase (EC4.4.1.1); CysK, cysteine synthase (EC2.5.1.47); DHAD, dihydroxy-acid dehydratase (EC4.2.1.9); DHLTA, dihydrolipoyllysine-residue (2-methylpropanoyl) transferase (EC2.3.1.168); DLDH, dihydrolipoyl dehydrogenase (EC1.8.1.4); DLST, dihydrolipoamide succinyltransferase; ECHS, enoyl-CoA hydratase (EC4.2.1.17); FAH, fumarylacetoacetase (EC3.7.1.2); GCDH, glutaryl-CoA dehydrogenase (EC1.3.8.6); GDCH, glycine cleavage system H protein; GDCP, glycine decarboxylase p-protein (EC1.4.4.2); GDCT, glycine decarboxylase t-protein (EC2.1.2.10); GLDH, glutamate dehydrogenase (EC1.4.1.2 and EC1.4.1.4); GOGAT, glutamine 2-oxoglutarate aminotransferase (EC1.4.1.13, EC1.4.1.14, and EC1.4.7.1); GS, glutamine synthetase (EC6.3.1.2); HAD, 3-hydroxyacyl-CoA dehydrogenase (EC1.1.1.35); HCL, hydroxymethylglutaryl-CoA lyase (EC4.1.3.4); HDC, histidine decarboxylase (EC:4.1.1.22); HGD, homogentisate 1,2-dioxygenase (EC1.13.11.5); HIBADH, 3-hydroxyisobutyrate dehydrogenase (EC1.1.1.31); HIBCH, 3-hydroxyisobutyryl-CoA hydrolase (EC3.1.2.4); HisAT, histidine transaminase (EC2.6.1.38); HPD, 4-hydroxyphenylpyruvate dioxygenase (EC1.13.11.27); IVD, isovaleryl-CoA dehydrogenase (EC1.3.8.4); KARI, ketol-acid reductoisomerase (EC1.1.1.86); KAT, kynurenine aminotransferase (EC2.6.1.39); LKR, lysine-2-oxoglutarate reductase (EC1.5.1.8); L-SD, L-serine ammonia-lyase (EC4.3.1.17); MAAI, maleylacetoacetate isomerase (EC5.2.1.2); MAT, S-adenosylmethionine synthetase (EC2.5.1.6); MCC, methylcrotonyl-CoA carboxylase (EC6.4.1.4); MCD, 2-methylacyl-CoA dehydrogenase (EC1.3.99.12); MCEE, methylmalonyl-CoA epimerase (EC5.1.99.1); MCM, methylmalonyl-CoA mutase (EC5.4.99.2); METH, methionine synthase (EC2.1.1.13); MGCHS, methylglutaconyl-CoA hydratase (EC4.2.1.18); MGL, methionine gamma-lyase (EC4.4.1.11); MMSDH, methylmalonate semialdehyde dehydrogenase (EC1.2.1.27); MPST, 3-mercaptopyruvate sulfurtransferase (EC2.8.1.2); MS, malate synthase (EC2.3.3.9); OAT, ornithine aminotransferase (EC2.6.1.13); OCD, ornithine cyclodeaminase (EC4.3.1.12); Odc, ornithine decarboxylase (EC4.1.1.17); OTC, ornithine carbamoyltransferase (EC2.1.3.3); PAH, phenylalanine hydroxylase (EC1.14.16.1); PCC, propionyl-CoA carboxylase (EC6.4.1.3); PRODH, proline dehydrogenase (EC1.5.5.2); PYCR, pyrroline-5-carboxylate reductase (EC1.5.1.2); SATase, serine O-acetyltransferase (EC2.3.1.30); SDH, saccharopine dehydrogenase (EC1.5.1.9); SHMT, serine hydroxymethyltransferase (EC2.1.2.1); TA, threonine aldolase (EC4.1.2.5); TAT, tyrosine aminotransferase (EC2.6.1.5); TDA, threonine deaminase (EC4.3.1.19); Tpase, tryptophanase (EC4.1.99.1); TS, tryptophan synthase (EC4.2.1.20)..

FIGURE 2

Expression levels of amino acid catabolism-related genes in P. tricornutum. Transcriptome data of 15 min, 45 min, and 18 h were cited from Smith et al. (2019). Fold changes of 15 min, 45 min, and 18 h were re-calculated by N-4, N-5, and N-6 contrasting with pre_3, respectively. Transcriptome data of 4, 8, and 20 h were cited from Matthijs et al. (2016, . Transcriptome data of 48 h were cited from Levitan et al. (2015). The transcriptome data and the proteome data of SSL (nitrogen stress to steady state in the light period) and SSD (nitrogen stress to steady state in the dark period) were cited from Remmers et al. (2018). T-Pt, transcriptome of P. tricornutum; P-Pt, proteome of P. tricornutum. The homologous genes in T. pseudonana and the fold changes and RPKM data were shown in Supplementary Tables 1, 2, respectively. All the experimental conditions were shown in the Supplementary Material. The abbreviations of related enzymes are the same as those in Figure 1.