Metabolomic, proteomic and lactylated proteomic analyses indicate lactate plays important roles in maintaining energy and C:N homeostasis in Phaeodactylum tricornutum

Huang, Aiyou; Li, Yuanxiang; Duan, Jiawen; Guo, Shiyi; Cai, Xiaoni; Zhang, Xiang; Long, Hao; Ren, Wei; Xie, Zhenyu

doi:10.1186/s13068-022-02152-8

Biotechnology for Biofuels and Bioproducts

Table 2 Different expressed proteins under LN/NC and HC/NC

From: Metabolomic, proteomic and lactylated proteomic analyses indicate lactate plays important roles in maintaining energy and C:N homeostasis in Phaeodactylum tricornutum

Pathway	No.^*	Protein accession	KEGG gene	HC/NC ratio	HC/NC P value	LN/NC ratio	LN/NC P value
Calvin cycle	36	A0T0E2	Ribulose-bisphosphate carboxylase small chain	0.69	0.21	0.47	0.03
	37	B5Y5F0	Phosphoribulokinase	0.97	0.72	0.47	0.00
	38	B7FRD1	Sedoheptulose-bisphosphatase	2.60	0.13	1.83	0.02
	39	B7FUH0	Alanine transaminase	0.63	0.10	0.54	0.04
	40	B7G9Y7	Aspartate aminotransferase	0.67	0.18	0.51	0.04
	50	B7G585	Pyruvate, orthophosphate dikinase	0.48	0.02	0.60	0.04
Calvin cycle, glycolysis	2	B7FSQ0	Triosephosphate isomerase	0.49	0.12	0.33	0.00
	3	B7FSI3	Glyceraldehyde 3-phosphate dehydrogenase	0.79	0.13	0.57	0.00
	5	B7G938	Phosphoglycerate kinase	0.79	0.11	0.69	0.00
	8	B7FSI4	Glyceraldehyde 3-phosphate dehydrogenase	0.72	0.16	0.50	0.01
	19	B7G5G4	Phosphoglycerate kinase	0.80	0.23	0.66	0.04
	21	B7G7C5	Glyceraldehyde 3-phosphate dehydrogenase	-	-	3.11	0.05
	23	B7GC94	Glyceraldehyde 3-phosphate dehydrogenase	1.56	0.04	1.50	0.05
Calvin cycle, glycolysis, OPPP	1	B7GE67	Fructose-bisphosphate aldolase	0.23	0.01	0.13	0.00
	6	B7G9G9	Fructose-bisphosphate aldolase	0.72	0.15	0.65	0.01
	12	B7G4R3	Fructose-bisphosphate aldolase	2.78	0.06	3.32	0.02
Calvin cycle, OPPP	29	B7FUU0	Transketolase	0.60	0.18	0.34	0.02
Calvin cycle, OPPP	31	B7FRG3	Ribulose-phosphate 3-epimerase	1.16	0.44	0.49	0.03
Calvin cycle, TCA cycle	30	B7GEG9	Malate dehydrogenase	1.05	0.82	1.50	0.01
Glycolysis	9	B7GD69	Probable phosphoglycerate mutase	1.85	0.07	2.51	0.01
	11	B7G9G7	Pyruvate kinase	0.64	0.15	0.41	0.02
	16	B7FNZ8	Alcohol dehydrogenase (NADP +)	0.94	0.69	1.67	0.03
	18	B7G8B7	Glucokinase	1.97	0.12	2.65	0.04
	20	B7FZG7	Pyruvate kinase	1.81	0.13	2.01	0.04
	22	B7FP91	S-(hydroxymethyl) glutathione dehydrogenase / alcohol dehydrogenase	0.74	0.11	1.44	0.05
	24	B7FRD3	Fructose-1,6-bisphosphatase I	0.71	0.06	0.75	0.07
	26	B7GA17	Glucose-6-phosphate 1-epimerase	1.97	0.02	1.21	0.16
	27	B7FT40	Alcohol dehydrogenase (NADP +)	0.62	0.05	0.76	0.18
Glycolysis, OPPP	4	B7GE27	6-Phosphofructokinase 1	0.50	0.09	0.28	0.00
	14	B7GCG9	6-phosphofructokinase 1	2.58	0.11	3.58	0.02
	15	B7GE28	6-Phosphofructokinase 1	1.37	0.44	1.99	0.03
Glycolysis, TCA cycle	7	B7S3L5	Pyruvate dehydrogenase E2 component (dihydrolipoamide acetyltransferase)	1.17	0.01	0.81	0.01
	10	B7GBE9	Dihydrolipoamide dehydrogenase	2.77	0.03	3.10	0.02
	13	B7G3I7	Pyruvate dehydrogenase E2 component (dihydrolipoamide acetyltransferase)	1.11	0.45	1.44	0.02
	17	B7FZN6	Pyruvate dehydrogenase E1 component beta subunit	1.34	0.14	1.58	0.03
	25	B7FZE1	Pyruvate dehydrogenase E1 component alpha subunit	4.16	0.00	1.72	0.08
	28	B7GDA9	Pyruvate dehydrogenase E2 component (dihydrolipoamide acetyltransferase)	1.44	0.05	1.16	0.22
Lactate metabolism	–	B7FZP8	D-2-hydroxyglutarate dehydrogenase	0.83	0.36	0.97	0.95
	–	B7G085	Lactoylglutathione lyase	0.97	0.98	0.73	0.27
	–	B7GDI1	Hydroxyacylglutathione hydrolase	1.28	0.19	1.31	0.10
	–	B7GDI2	Sulphur dioxygenase	1.51	0.21	1.51	0.11
Light-harvesting complex	62	B7G8E5	Light-harvesting complex I chlorophyll a/b binding protein 1	1.80	0.00	0.47	0.00
	63	B7G4U8	Light-harvesting complex I chlorophyll a/b binding protein 1	1.73	0.36	3.36	0.01
	64	B7GBK7	Light-harvesting complex I chlorophyll a/b binding protein 1	1.65	0.22	0.41	0.01
	65	B7FPL6	Light-harvesting complex I chlorophyll a/b binding protein 1	1.95	0.05	0.44	0.02
	66	B7GCV9	Light-harvesting complex I chlorophyll a/b binding protein 1	1.96	0.14	2.01	0.04
	67	B7FRW2	Light-harvesting complex I chlorophyll a/b binding protein 1	1.42	0.24	0.56	0.04
	68	B7G502	Light-harvesting complex I chlorophyll a/b binding protein 1	1.69	0.03	0.64	0.08
	69	B7GAS4	Light-harvesting complex I chlorophyll a/b binding protein 1	1.92	0.04	0.67	0.19
	70	B7G503	Light-harvesting complex I chlorophyll a/b binding protein 1	2.20	0.04	0.67	0.28
	71	B7FV42	Light-harvesting complex I chlorophyll a/b binding protein 1	2.38	0.04	1.02	0.75
Nitrogen metabolism	51	B7FNU0	Carbonic anhydrase	0.58	0.13	0.34	0.01
	52	B7FRE8	Cyanate lyase	0.99	0.91	0.53	0.05
	53	B7FXP8	Carbonic anhydrase	0.69	0.22	0.44	0.02
	54	B7FYS6	Formamidase	1.48	0.31	2.67	0.02
	55	B7FZB0	Glutamate synthase (NADH)	1.45	0.16	2.05	0.02
	56	B7G0L4	Ferredoxin-nitrite reductase	0.20	0.03	0.11	0.00
	57	B7G3X3	Glutamate dehydrogenase (NADP +)	1.29	0.54	1.76	0.03
	58	B7G5A1	Glutamine synthetase	2.56	0.01	3.14	0.00
	59	B7G997	Nitrate reductase (NAD(P)H)	0.09	0.00	0.19	0.02
	60	B7GA80	Carbonic anhydrase	0.38	0.14	0.33	0.02
	61	B7GAZ5	Glutamate synthase (NADH)	1.31	0.22	2.47	0.00
Oxidative phosphorylation	93	B7FVX2	NADH dehydrogenase (ubiquinone) 1 alpha subcomplex subunit 12	1.09	0.63	0.60	0.03
Oxidative phosphorylation	94	B7FRC2	NADH dehydrogenase (ubiquinone) 1 alpha/beta subcomplex 1, acyl-carrier protein	0.76	0.11	0.26	0.00
	95	B7GES5	NADH dehydrogenase (ubiquinone) Fe-S protein 7	1.14	0.47	1.79	0.02
	96	B7G964	NADH dehydrogenase (ubiquinone) flavoprotein 2	0.99	0.82	1.35	0.01
	98	B7G063	Ubiquinol-cytochrome c reductase subunit 7	0.99	0.99	0.56	0.01
	99	B7G3I2	V-type H + -transporting ATPase subunit a	1.18	0.32	2.68	0.00
	100	B7G162	V-type H⁺-transporting ATPase subunit A	1.04	0.80	1.58	0.04
	101	B7FQQ8	V-type H⁺-transporting ATPase subunit B	1.36	0.23	2.01	0.00
	102	B7FTS7	V-type H⁺-transporting ATPase subunit C	1.77	0.08	2.87	0.00
	103	B7G360	V-type H⁺-transporting ATPase subunit D	1.18	0.52	1.73	0.01
	104	B7G7X7	V-type H⁺-transporting ATPase subunit E	1.47	0.14	2.02	0.00
	105	B7G9S7	V-type H⁺-transporting ATPase subunit H	1.42	0.27	2.86	0.00
	106	B7GE53	H⁺-transporting ATPase	1.04	0.90	1.97	0.02
	107	B7FT09	inorganic pyrophosphatase	0.92	0.36	0.58	0.00
	97	B7GDY0	V-type H⁺-transporting ATPase subunit F	1.48	0.04	0.93	0.17
Photosynthesis	72	A0T0A3	Photosystem II cytochrome b559 subunit alpha	1.16	0.70	0.30	0.00
	73	A0T0A9	Photosystem II PsbH protein	1.17	0.68	0.27	0.00
	74	A0T0B2	Photosystem II CP47 chlorophyll apoprotein	0.91	0.58	0.69	0.01
	75	A0T0C6	Photosystem II cytochrome c550	0.89	0.60	0.27	0.00
	76	B7FUR5	Photosystem II PsbU protein	0.71	0.35	0.16	0.00
	77	B7FZ96	Photosystem II oxygen-evolving enhancer protein 1	0.77	0.30	0.27	0.00
	78	B7G9T8	Ferredoxin–NADP⁺ reductase	1.17	0.48	1.60	0.03
	79	B7GCT8	Ferredoxin-NADP⁺ reductase	0.63	0.15	0.40	0.01
	80	A0T0B8	Cytochrome b6	1.20	0.15	1.59	0.01
	81	B5Y578	Cytochrome c6	0.80	0.47	0.28	0.00
	82	B5Y3C9	Cytochrome b6-f complex iron-sulphur subunit	1.68	0.00	0.67	0.02
	83	A0T0M6	Photosystem I subunit XI	2.11	0.02	0.88	0.66
	84	A0T0B9	Photosystem I subunit II	1.01	0.96	0.48	0.01
	85	A0T0F3	Photosystem I subunit IV	0.91	0.60	0.42	0.00
	86	A0T0L2	Photosystem I subunit VII	1.24	0.19	0.35	0.00
Photosynthesis, Oxidative phosphorylation	87	A0T0D1	F-type H⁺/Na⁺-transporting ATPase subunit beta	0.86	0.54	0.39	0.01
	88	A0T0D2	F-type H⁺/Na⁺-transporting ATPase subunit beta	0.85	0.44	0.50	0.01
	89	A0T0F0	F-type H⁺-transporting ATPase subunit delta	1.44	0.10	0.66	0.01
	90	A0T0F1	F-type H⁺/Na⁺-transporting ATPase subunit alpha	0.82	0.38	0.54	0.02
	91	B7G0M9	F-type H⁺-transporting ATPase subunit gamma	0.74	0.23	0.44	0.01
	92	B7FRE6	F-type H⁺/Na⁺-transporting ATPase subunit alpha	0.77	0.01	0.77	0.01
OPPP	32	B5Y3S6	transaldolase	1.44	0.15	1.51	0.00
	33	B7FPL4	6-Phosphogluconolactonase	1.26	0.50	1.53	0.05
	34	B7FQV1	rRbose-phosphate pyrophosphokinase	0.97	0.72	0.67	0.01
	35	B7GDN8	Transaldolase	0.97	0.75	0.37	0.00
TCA cycle	42	B7FUR4	Aconitate hydratase 2 / 2-methylisocitrate dehydratase	1.81	0.06	2.54	0.00
	43	B7FWX5	Fumarate hydratase, class I	1.55	0.10	2.11	0.00
	44	B7FXA2	Succinyl-CoA synthetase beta subunit	1.18	0.16	1.47	0.00
	45	B7G4T8	2-Oxoglutarate dehydrogenase E1 component	1.41	0.25	2.03	0.05
	46	B7G620	Isocitrate dehydrogenase	1.21	0.54	1.86	0.03
	47	B7G9P5	Citrate synthase	1.60	0.10	1.81	0.00
	48	B7GA05	Phosphoenolpyruvate carboxykinase	0.72	0.01	0.51	0.00
	49	B7GA98	Pyruvate carboxylase	0.67	0.01	1.04	0.68
TCA cycle, Oxidative phosphorylation	41	B5Y4R0	Succinate dehydrogenase (ubiquinone) cytochrome b560 subunit	1.86	0.11	2.95	0.01
Chrysolaminarin metabolism	–	B7FWJ8	Beta-glucosidase	1.91	0.01	1.64	0.01
	–	B7GB76		1.69	0.09	3.26	0.01
	–	B7GBX3	Xylan 1,4-beta-xylosidase	1.31	0.54	2.14	0.03
Phosphatidylinositol signaling system	–	B7FSY9	Inositol polyphosphate 5-phosphatase INPP5B/F	1.03	0.79	1.90	0.04
	–	B7G377	1-Phosphatidylinositol-4-phosphate 5-kinase	1.17	0.32	1.81	0.00
	–	B7G4M3	Diacylglycerol kinase (ATP)]	3.46	0.11	5.70	0.00
	–	B7GBU7	Phosphatidylinositol phospholipase C, delta	1.40	0.06	2.53	0.00
	–	B7GCH9	Phosphatidylinositol 4-kinase B	1.24	0.47	2.29	0.02
	–	B7GD06	Calmodulin	1.73	0.00	1.61	0.00
Other proteins showing similar expression patterns under LN and HC	–	B7G9R3	–	17.07	0.01	44.89	0.00
	–	B7G9B2	–	0.02	0.03	0.00	0.00
	–	B7G9B0	–	0.03	0.00	0.01	0.00
	–	B7G9B1	–	0.01	0.01	0.01	0.01

^*Protein No. in Fig. 3

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