#METABOLOMICS WORKBENCH lgafeira_20220714_113333 DATATRACK_ID:3341 STUDY_ID:ST002277 ANALYSIS_ID:AN003721 PROJECT_ID:PR001458
VERSION             	1
CREATED_ON             	September 1, 2022, 8:19 pm
#PROJECT
PR:PROJECT_TITLE                 	Skin-to-blood pH shift triggers metabolome and proteome global remodelling in
PR:PROJECT_TITLE                 	Staphylococcus epidermidis
PR:PROJECT_SUMMARY               	Staphylococcus epidermidis (SE) is one of the most common bacteria of the human
PR:PROJECT_SUMMARY               	skin microbiota. Despite its role as a commensal, SE has emerged as an
PR:PROJECT_SUMMARY               	opportunistic pathogen, associated with 80% of medical devices related
PR:PROJECT_SUMMARY               	infections. Moreover, these bacteria are extremely difficult to treat due to
PR:PROJECT_SUMMARY               	their ability to form biofilms and accumulate resistance to almost all classes
PR:PROJECT_SUMMARY               	of antimicrobials developed so far. Thus new preventive and therapeutic
PR:PROJECT_SUMMARY               	strategies are urgently needed. In spite of its clinical importance, the
PR:PROJECT_SUMMARY               	molecular mechanisms associated with SE colonisation and disease are still
PR:PROJECT_SUMMARY               	poorly understood. A deeper understanding of the metabolic and cellular
PR:PROJECT_SUMMARY               	processes associated with response to environmental factors characteristic of SE
PR:PROJECT_SUMMARY               	ecological niches in health and disease might provide new clues on colonisation
PR:PROJECT_SUMMARY               	and disease processes. Here we studied the impact of pH conditions, mimicking
PR:PROJECT_SUMMARY               	the skin pH (5.5) and blood pH (7.4), in a S. epidermidis commensal strain,
PR:PROJECT_SUMMARY               	belonging to the B clonal lineage, by means of next-generation proteomics and 1H
PR:PROJECT_SUMMARY               	NMR-based metabolomics. Moreover, we evaluated the metabolic changes occurring
PR:PROJECT_SUMMARY               	when a sudden pH change arise, simulating the skin barrier break produced by a
PR:PROJECT_SUMMARY               	catheter. We found that exposure of S. epidermidis to skin pH induced oxidative
PR:PROJECT_SUMMARY               	phosphorylation and biosynthesis of peptidoglycan, lipoteichoic acids and
PR:PROJECT_SUMMARY               	betaine. In contrast, at blood pH, the incorporation of monosaccharides and its
PR:PROJECT_SUMMARY               	oxidation by glycolysis and fermentation was promoted. Additionally, several
PR:PROJECT_SUMMARY               	proteins related to virulence and immune evasion, namely extracellular proteases
PR:PROJECT_SUMMARY               	and membrane iron transporters were more abundant at blood pH. In the situation
PR:PROJECT_SUMMARY               	of an abrupt skin-to-blood pH shift we observed the decrease in the osmolyte
PR:PROJECT_SUMMARY               	betaine and changes in the levels of several metabolites and proteins involved
PR:PROJECT_SUMMARY               	in redox cell homeostasis. Our results suggest that at the skin pH S.
PR:PROJECT_SUMMARY               	epidermidis cells are metabolically more active and adhesion is promoted, while
PR:PROJECT_SUMMARY               	at blood pH, metabolism is tuned down and cells have a more virulent profile. pH
PR:PROJECT_SUMMARY               	increase during commensal-to-pathogen conversion appears to be a critical
PR:PROJECT_SUMMARY               	environmental signal to the remodelling of the S. epidermidis metabolism towards
PR:PROJECT_SUMMARY               	a more pathogenic state. Targeting S. epidermidis proteins induced by a low
PR:PROJECT_SUMMARY               	alkaline pH and local acidification of medical devices microenvironment might be
PR:PROJECT_SUMMARY               	new strategies to treat and prevent S. epidermidis infections.
PR:INSTITUTE                     	ITQB NOVA
PR:LAST_NAME                     	Gonçalves
PR:FIRST_NAME                    	Luís
PR:ADDRESS                       	Avenida Republica, Oeiras, Not USCanada, 2780-157 Oeiras, Portugal
PR:EMAIL                         	lgafeira@itqb.unl.pt
PR:PHONE                         	214469464
#STUDY
ST:STUDY_TITLE                   	Skin-to-blood pH shift triggers metabolome and proteome global remodelling in
ST:STUDY_TITLE                   	Staphylococcus epidermidis
ST:STUDY_TYPE                    	NMR Metabolomics combine with proteomics to study pH adaptation of
ST:STUDY_TYPE                    	Staphylococcus epidermidis 19N
ST:STUDY_SUMMARY                 	Staphylococcus epidermidis (SE) is one of the most common bacteria of the human
ST:STUDY_SUMMARY                 	skin microbiota. Despite its role as a commensal, SE has emerged as an
ST:STUDY_SUMMARY                 	opportunistic pathogen, associated with 80% of medical devices related
ST:STUDY_SUMMARY                 	infections. Moreover, these bacteria are extremely difficult to treat due to
ST:STUDY_SUMMARY                 	their ability to form biofilms and accumulate resistance to almost all classes
ST:STUDY_SUMMARY                 	of antimicrobials developed so far. Thus new preventive and therapeutic
ST:STUDY_SUMMARY                 	strategies are urgently needed. In spite of its clinical importance, the
ST:STUDY_SUMMARY                 	molecular mechanisms associated with SE colonisation and disease are still
ST:STUDY_SUMMARY                 	poorly understood. A deeper understanding of the metabolic and cellular
ST:STUDY_SUMMARY                 	processes associated with response to environmental factors characteristic of SE
ST:STUDY_SUMMARY                 	ecological niches in health and disease might provide new clues on colonisation
ST:STUDY_SUMMARY                 	and disease processes. Here we studied the impact of pH conditions, mimicking
ST:STUDY_SUMMARY                 	the skin pH (5.5) and blood pH (7.4), in a S. epidermidis commensal strain,
ST:STUDY_SUMMARY                 	belonging to the B clonal lineage, by means of next-generation proteomics and 1H
ST:STUDY_SUMMARY                 	NMR-based metabolomics. Moreover, we evaluated the metabolic changes occurring
ST:STUDY_SUMMARY                 	when a sudden pH change arise, simulating the skin barrier break produced by a
ST:STUDY_SUMMARY                 	catheter. We found that exposure of S. epidermidis to skin pH induced oxidative
ST:STUDY_SUMMARY                 	phosphorylation and biosynthesis of peptidoglycan, lipoteichoic acids and
ST:STUDY_SUMMARY                 	betaine. In contrast, at blood pH, the incorporation of monosaccharides and its
ST:STUDY_SUMMARY                 	oxidation by glycolysis and fermentation was promoted. Additionally, several
ST:STUDY_SUMMARY                 	proteins related to virulence and immune evasion, namely extracellular proteases
ST:STUDY_SUMMARY                 	and membrane iron transporters were more abundant at blood pH. In the situation
ST:STUDY_SUMMARY                 	of an abrupt skin-to-blood pH shift we observed the decrease in the osmolyte
ST:STUDY_SUMMARY                 	betaine and changes in the levels of several metabolites and proteins involved
ST:STUDY_SUMMARY                 	in redox cell homeostasis. Our results suggest that at the skin pH S.
ST:STUDY_SUMMARY                 	epidermidis cells are metabolically more active and adhesion is promoted, while
ST:STUDY_SUMMARY                 	at blood pH, metabolism is tuned down and cells have a more virulent profile. pH
ST:STUDY_SUMMARY                 	increase during commensal-to-pathogen conversion appears to be a critical
ST:STUDY_SUMMARY                 	environmental signal to the remodelling of the S. epidermidis metabolism towards
ST:STUDY_SUMMARY                 	a more pathogenic state. Targeting S. epidermidis proteins induced by a low
ST:STUDY_SUMMARY                 	alkaline pH and local acidification of medical devices microenvironment might be
ST:STUDY_SUMMARY                 	new strategies to treat and prevent S. epidermidis infections.
ST:INSTITUTE                     	ITQB NOVA
ST:LABORATORY                    	Proteomics of Non-Model Organisms
ST:LAST_NAME                     	Gonçalves
ST:FIRST_NAME                    	Luís
ST:ADDRESS                       	Avenida Republica, Oeiras, Not USCanada, 2780-157 Oeiras, Portugal
ST:EMAIL                         	lgafeira@itqb.unl.pt
ST:PHONE                         	214469464
ST:NUM_GROUPS                    	3
#SUBJECT
SU:SUBJECT_TYPE                  	Bacteria
SU:SUBJECT_SPECIES               	Staphylococcus epidermidis
SU:TAXONOMY_ID                   	1282
SU:GENOTYPE_STRAIN               	Staphylococcus epidermidis 19N
#SUBJECT_SAMPLE_FACTORS:         	SUBJECT(optional)[tab]SAMPLE[tab]FACTORS(NAME:VALUE pairs separated by |)[tab]Raw file names and additional sample data
SUBJECT_SAMPLE_FACTORS           	-	SE_12	class:N55	RAW_FILE_NAME=SE_12
SUBJECT_SAMPLE_FACTORS           	-	SE_16	class:N57	RAW_FILE_NAME=SE_16
SUBJECT_SAMPLE_FACTORS           	-	SE_18	class:N57	RAW_FILE_NAME=SE_18
SUBJECT_SAMPLE_FACTORS           	-	SE_19	class:N57	RAW_FILE_NAME=SE_19
SUBJECT_SAMPLE_FACTORS           	-	SE_2	class:N77	RAW_FILE_NAME=SE_2
SUBJECT_SAMPLE_FACTORS           	-	SE_20	class:N57	RAW_FILE_NAME=SE_20
SUBJECT_SAMPLE_FACTORS           	-	SE_22	class:N55	RAW_FILE_NAME=SE_22
SUBJECT_SAMPLE_FACTORS           	-	SE_23	class:N57	RAW_FILE_NAME=SE_23
SUBJECT_SAMPLE_FACTORS           	-	SE_27	class:N57	RAW_FILE_NAME=SE_27
SUBJECT_SAMPLE_FACTORS           	-	SE_28	class:N57	RAW_FILE_NAME=SE_28
SUBJECT_SAMPLE_FACTORS           	-	SE_29	class:N55	RAW_FILE_NAME=SE_29
SUBJECT_SAMPLE_FACTORS           	-	SE_30	class:N77	RAW_FILE_NAME=SE_30
SUBJECT_SAMPLE_FACTORS           	-	SE_31	class:N55	RAW_FILE_NAME=SE_31
SUBJECT_SAMPLE_FACTORS           	-	SE_34	class:N57	RAW_FILE_NAME=SE_34
SUBJECT_SAMPLE_FACTORS           	-	SE_37	class:N77	RAW_FILE_NAME=SE_37
SUBJECT_SAMPLE_FACTORS           	-	SE_39	class:N55	RAW_FILE_NAME=SE_39
SUBJECT_SAMPLE_FACTORS           	-	SE_4	class:N77	RAW_FILE_NAME=SE_4
SUBJECT_SAMPLE_FACTORS           	-	SE_43	class:N77	RAW_FILE_NAME=SE_43
SUBJECT_SAMPLE_FACTORS           	-	SE_44	class:N55	RAW_FILE_NAME=SE_44
SUBJECT_SAMPLE_FACTORS           	-	SE_48	class:N55	RAW_FILE_NAME=SE_48
SUBJECT_SAMPLE_FACTORS           	-	SE_50	class:N77	RAW_FILE_NAME=SE_50
SUBJECT_SAMPLE_FACTORS           	-	SE_6	class:N77	RAW_FILE_NAME=SE_6
SUBJECT_SAMPLE_FACTORS           	-	SE_8	class:N77	RAW_FILE_NAME=SE_8
#COLLECTION
CO:COLLECTION_SUMMARY            	The Staphylococcus epidermidis 19N strain was collected from the anterior nares
CO:COLLECTION_SUMMARY            	of a healthy person in Portugal in 2001. This strain was previously
CO:COLLECTION_SUMMARY            	characterised by whole genome sequencing and belongs to clonal lineage B. A
CO:COLLECTION_SUMMARY            	single colony from a S. epidermidis 19N strain culture grown O/N at 37ºC (TSA,
CO:COLLECTION_SUMMARY            	BactoTM), was used to pre-inoculate Tryptic Soy Broth (TSB) medium with two
CO:COLLECTION_SUMMARY            	different pH (5.5 and 7.4) that was incubated overnight at 37ºC under
CO:COLLECTION_SUMMARY            	agitation. Pre-inoculums were adjusted either to pH 5.5 or pH 7.4, with
CO:COLLECTION_SUMMARY            	hydrochloric acid. In this work, three pH transitions from pre-inoculum to
CO:COLLECTION_SUMMARY            	inoculum were assayed. S. epidermidis pre-inoculums and the growth were
CO:COLLECTION_SUMMARY            	performed at medium with pH 7.4, to mimic the blood pH; and pH 5.5, to mimic the
CO:COLLECTION_SUMMARY            	skin pH. The pre-inoculum cellular density was adjusted to 0.06 (OD600)
CO:COLLECTION_SUMMARY            	(aprox.1.5x108 CFU/mL) and used to inoculate fresh medium in the three
CO:COLLECTION_SUMMARY            	conditions depicted in Figure 1, simulating S. epidermidis at skin and blood and
CO:COLLECTION_SUMMARY            	a pH shock endured by S. epidermidis during the infection process from skin to
CO:COLLECTION_SUMMARY            	blood transition. The cell cultures incubated at 37ºC with 225 rpm were
CO:COLLECTION_SUMMARY            	followed by OD600 and recovered at mid-exponential phase for further analysis.
CO:SAMPLE_TYPE                   	Staphylococcus epidermidis intracellular
CO:STORAGE_CONDITIONS            	-80℃
#TREATMENT
TR:TREATMENT_SUMMARY             	In this work, three pH transitions from pre-inoculum to inoculum were assayed.
TR:TREATMENT_SUMMARY             	S. epidermidis pre-inoculums and the growth were performed at medium with pH
TR:TREATMENT_SUMMARY             	7.4, to mimic the blood pH; and pH 5.5, to mimic the skin pH. The pre-inoculum
TR:TREATMENT_SUMMARY             	cellular density was adjusted to 0.06 (OD600) (aprox.1.5x108 CFU/mL) and used to
TR:TREATMENT_SUMMARY             	inoculate fresh medium in the three conditions depicted in Figure 1, simulating
TR:TREATMENT_SUMMARY             	S. epidermidis at skin and blood and a pH shock endured by S. epidermidis during
TR:TREATMENT_SUMMARY             	the infection process from skin to blood transition. The cell cultures incubated
TR:TREATMENT_SUMMARY             	at 37ºC with 225 rpm were followed by OD600 and recovered at mid-exponential
TR:TREATMENT_SUMMARY             	phase for further analysis. Pre-inocula were prepared in TSB medium at pH 5.5 or
TR:TREATMENT_SUMMARY             	7.4. Inocula at pH 5.5 was used for the cultures grown at 5.5 (N55) and 7.4
TR:TREATMENT_SUMMARY             	(N57), and the inoculum at pH 7.4 for the culture at the same pH (N77). The
TR:TREATMENT_SUMMARY             	cells were harvested at mid-exponential phase.
#SAMPLEPREP
SP:SAMPLEPREP_SUMMARY            	Cells were recovered at mid-exponential phase from 100 mL cultures following a
SP:SAMPLEPREP_SUMMARY            	protocol adapted from Somerville & Powers (Somerville and Powers 2014). Eight
SP:SAMPLEPREP_SUMMARY            	biological replicates of each independent growth condition were obtained. Cells
SP:SAMPLEPREP_SUMMARY            	were harvested by centrifugation at 5000 x g for 5 min at 4ºC. Cells were
SP:SAMPLEPREP_SUMMARY            	washed with 20 mM phosphate buffer pH 7.2-7.4 and centrifuged for 1 min at
SP:SAMPLEPREP_SUMMARY            	13,000 rpm. Cell pellet was suspended in the same buffer with a final OD600 of
SP:SAMPLEPREP_SUMMARY            	20 and stored at -80ºC for further metabolite extraction. Cells were thawed in
SP:SAMPLEPREP_SUMMARY            	a water bath at room temperature and 750 µL of 60% methanol were added and
SP:SAMPLEPREP_SUMMARY            	subjected to three freeze-thaw cycles using liquid nitrogen. Extracted samples
SP:SAMPLEPREP_SUMMARY            	were centrifuged at 21,000 g for 5 min at 4ºC. The extraction process on the
SP:SAMPLEPREP_SUMMARY            	pellets was repeated twice. The supernatants were kept and stored together at
SP:SAMPLEPREP_SUMMARY            	-20ºC overnight and dried in a SpeedVac. Dried samples were dissolved in: 750
SP:SAMPLEPREP_SUMMARY            	µL phosphate buffer (33 mM, pH 7.0 in D2O with 2 mM of sodium azide) with 0.21
SP:SAMPLEPREP_SUMMARY            	mM of 3-(trimethylsilyl)propionic-2,2,3,3-d4 (TSP). The suspensions were
SP:SAMPLEPREP_SUMMARY            	centrifuged at 21,000 g for 5 min at 4ºC and the resulting supernatants were
SP:SAMPLEPREP_SUMMARY            	then transferred to 5 mm NMR tubes.
#ANALYSIS
AN:SOFTWARE_VERSION              	Bruker TopSpin 3.2
#NMR
NM:INSTRUMENT_NAME               	Bruker Avance II+ 800 MHz
NM:INSTRUMENT_TYPE               	FT-NMR
NM:NMR_EXPERIMENT_TYPE           	1D-1H
NM:SPECTROMETER_FREQUENCY        	800
NM:NMR_PROBE                     	5 mm TXI-Z H/C/N/-D
NM:NMR_SOLVENT                   	D2O
NM:NMR_TUBE_SIZE                 	5 mm
NM:SHIMMING_METHOD               	Topshim
NM:TEMPERATURE                   	25
NM:NUMBER_OF_SCANS               	256
NM:DUMMY_SCANS                   	4
NM:CHEMICAL_SHIFT_REF_STD        	TSP
NM:NMR_RESULTS_FILE              	NMR_SE
#NMR_METABOLITE_DATA
NMR_METABOLITE_DATA:UNITS	nanomoles
NMR_METABOLITE_DATA_START
Samples	SE_12	SE_16	SE_18	SE_19	SE_2	SE_20	SE_22	SE_23	SE_27	SE_28	SE_29	SE_30	SE_31	SE_34	SE_37	SE_39	SE_4	SE_43	SE_44	SE_48	SE_50	SE_6	SE_8
Factors	class:N55	class:N57	class:N57	class:N57	class:N77	class:N57	class:N55	class:N57	class:N57	class:N57	class:N55	class:N77	class:N55	class:N57	class:N77	class:N55	class:N77	class:N77	class:N55	class:N55	class:N77	class:N77	class:N77
2-Hydroxyisobutyrate	0.7	0.9	1.8	0.7	1.3	0.7	4.9	2	1.3	1.5	4.6	2.1	1.5	1	2.8	2.3	1.3	2.5	1.5	2.2	3	1.2	1.5
3-Hydroxyisovalerate	4.6	5.5	4.7	4.6	3.7	4.5	4.7	5.3	5.6	4.9	5.1	2.9	13.3	2.8	2.9	13.4	4	4.1	2.8	2.9	13.3	3.7	3.9
AMP	4.1	1.7	3.5	14.6	15.5	9.7	3.7	1.3	12.4	7.3	9	6.4	6	3.8	1.6	5.6	9.6	2	5.1	6.2	2.9	11.8	9.9
Acetate	51.5	77.1	72.4	39	131	49.8	61.8	63.7	47.5	65.1	47.9	90.6	59.2	57.6	174.1	62.6	157.9	111.2	67.2	74.9	133	114.7	161.7
Adenine	3.4	13.8	4.3	5.3	9.5	6.3	3	8.8	5.8	6.5	5.2	18.7	16.7	15.5	23.6	17.2	8.8	19.1	13.2	19	20.7	13.7	9.5
Adenosine	10.8	11.2	11.5	20.6	18.8	28.6	14.7	6.6	9.6	16.9	14.5	35.6	31.4	46.9	37.6	33.5	17.3	43	28.5	37.5	45.7	21.4	18
Alanine	22.5	19.7	18.7	26.4	34.7	36.6	17.6	15.3	13.1	32.7	37.1	60	56	54.7	82.7	51	32.2	68.9	59.7	68.5	62.5	40	30.6
Arabinose	12.7	16.9	16.5	26.9	15.5	9.8	11.4	10.9	1.9	12.7	17.9	19	14.4	12.3	17.6	22.8	6.3	21.7	21.7	20.1	17.7	18.9	14.1
Asparagine	39.7	90.7	124.6	68.5	80.8	70.6	47.4	103.6	7.7	86.7	58.3	71.6	22.3	40.3	120.3	22.4	95	96.9	23.3	15.7	110.6	77	95.5
Aspartate	101.5	216.5	250.8	191.1	386.5	275.6	119.7	201.7	149.6	211.7	133.2	475.2	162.1	262.1	509.2	159	355.8	493.5	153.3	168.5	503.7	409.8	340.4
Betaine	1106.8	541.6	765.4	206.3	1297.3	305.8	1413.3	628.5	134.5	489.9	1647.1	1257.8	1331.8	148	1331.2	1289.2	1150.8	1382.5	1198.6	1301.1	1225	1433.1	955.6
Choline	19.5	5.2	5.5	3.2	13.7	3.6	24.2	5	6.7	4.7	32.4	15.8	39.6	2.4	17.3	37	15.6	16.3	32.1	38.9	14.8	15.6	12.5
Coenzyme A	7.2	4.8	18.9	22.7	21	13.8	6.1	7.5	11.7	14.3	7.7	2.9	3.4	3.3	4.3	6.9	7.8	9.7	4	3.4	3.9	26.8	18.5
Cytidine monophosphate	4.1	2.2	6	27.2	32.5	15.2	6	3.5	12.8	6.1	4.4	32.7	28.2	25.4	13.2	29.1	29	16.5	23	28.6	27.5	35.8	27.6
Formate	25.2	33.6	24	29.3	17.5	27.7	31.5	31.7	30.3	27.4	34.6	130.1	156.7	87.9	105.1	177	16	121.7	90.5	147.9	115.3	15.9	15.8
Glucose	22.3		4	270.7		5.23	6.8	7	114.1	6.7		3.4	4.7										1.9
Glutamate	689.7	512.7	638.2	406.8	726.2	464.2	895.7	510.2	294.4	464.6	965	647.2	757.2	247.6	635.3	796.7	610.1	662.3	709.6	837.5	677.1	666.5	583.6
Glutamine	101.5	50.3	50.6		39.2	13.9	138.9	51.1	18.8	41	165.9	49.9	53.1		57.2	32.2	95.7	50.6	34.1	35.4	59.5	69.4	75.1
Glycine	7.7	1.7	1.7	102.1	0.6	5.1	6.3	1.8	32.7	24.7	7.2	0.9	1	1	1	1	4.6	1.3	0.9	1.7	1.1	9	0.8
Guanosine	3.9	1.3	2.6	5	5.1	4.7	2.4	1.7	2.8	2.1	3.4	7.8	6	11.9	5.7	7.8	5.4	8.9	6.7	8.1	7.9	3.3	5.3
Histidine	2.2	3.7	3.8	3.1	4.9	4.4	3	3.8	2.6	3.8	3	6.4	5.4	3.7	6.4	4.9	4.3	5.8	5.5	5.1	6.3	5	4
Isoleucine	3.4	4.6	5.6	2.7	6.5	4.7	4.5	5.4	1.6	4	5.5	5.8	2.5	1.9	6.7	2.1	5.1	5.9	1.7	2.9	7.3	6.1	5
Isovalerate	1.1	1	1	1.3	4.5	0.7	1.1	0.7	1.7	1.2	1.1	3	5.2	3.3	3.7	5.2	5.5	3.2	5.3	5	3.9	4.9	4.4
Lactate	29.9	25.3	24.7	7	56.1	19.8	28.8	18.1	9	15	37.4	30	12.8	13.4	90.3	10.1	79.9	55.1	12.6	5.4	55.8	55.3	68.7
Leucine	16.4	17.1	24.5	11.8	21.2	19	19.3	21.7	3.3	20.7	25.1	26.4	15.2	10.4	31.3	13.6	21.1	25.9	11.6	16.6	34	22.3	21.1
Lysine	11.5	16.1	18.2	15.3	21	16	10.2	20.3	7.8	16	15	26	25.8	20.8	33.1	26.6	20.2	28.5	28.9	28	31.8	22.5	19.9
NAD+	16.8	22.1	21.1	14.6	15.7	15.7	19.9	18.7	20.9	15.7	16.7	13.5	15	15.5	16.8	13.9	15.7	14.4	14	14.3	16	14.4	15.8
NADP+	2.4	4.1	3.8	2.7	2.2	2.4	2.9	3.1	7.3	3	2.3	2.5	2.1	3.2	3.1	1.8	2.3	2.2	2.2	1.8	3	2.7	2.9
Nicotinate	1.5			0.8		1.5	0.6		0.7	1.6	3.4	1.2	2.9	1.1	2	1.4	1.1	1.7	2.3	2.7	1.8	1.7	
Phenylalanine	6.8	9.8	13.2	8.3	13.1	10.2	8.8	10	5.2	9.1	10.6	13.8	9.9	6	14.5	9.9	12.5	12.9	8.6	10.2	13.7	12.8	12.1
Phosphoenolpyruvic acid	6.8	30.6	22	12.9	9.7	19.2	11.4	16.3	16.9	19.7	12.4	13.9	11.4	6.3	17.1	10.5	4.8	14.2	11.2	15	14.7	3.9	7.1
Succinate	7.6	8.3	11.2	8.8	16.8	9.5	9.7	9.2	13	8	12.7	20.3	24.4	16.5	22.8	24.3	15.5	20.2	24.9	26.8	18.8	18.2	15.5
Sucrose	18.8			180.8		30.2	1.2	1.9	66.2	143.5		1.6			4.8		2.8	3		0.9	3	21.4	2.2
Threonine	6.2	12.4	10.5	19.9	8.3	5.9	16.8	8.7	2.6	7	20.5	7.2	6.2	4	6.5	6.5	7.9	6.2	4.6	19.7	8.1	9.6	7.8
Tryptophan		2.1			1.2	2.5				1.2	0.8	2.7	1.6	2.2	3.8	1.7	1.8	3			3.3	1.8	0.6
Tyrosine	0.6	1.6	1.1	0.9	1.9	2.1	1.1	1.5	0.6	1.3	0.8	3.3	1.9	1.5	3.1	2	2.3	3.4	1.6	2.3	3.5	1.6	2.4
UMP	2	2.3	2.3	8.7	12.6	8.7	1.9	1.1	8.2	3.4	2.2	11.4	10.7	6.8	2.8	8.7	8.2	4	7.2	8.7	7.9	10.6	8.7
Uracil	1.4	1.3	1.4	4.2	8.3	4.5	1.5	1.7	2.8	1.8	1.2	13	14.9	12.1	14.2	16.1	7.9	13.4	12.9	17.3	14.7	8.7	8.4
Uridine	1.7	3.3	2.3	3.7	2.6	8.7	2.1	5.4	3	2.8	4.1	8.9	6.9	11.5	13.2	9.4	2.9	9.2	9.6	6.1	9	2.8	2.9
Valine	6.9	5.8	8.1	4.8	10.1	7.1	6.7	10.2	2.5	5.6	8.8	10.6	7.8	3.9	11.3	6.8	9.7	10	6.1	8	13.1	10.7	8.1
sn-Glycero-3-phosphocholine	117.5	35.2	45.4	16.5	29.3	17.3	137.4	38.9	12.1	30.1	151.4	32.8	94.7	13.7	34.2	95.1	28.9	32.3	85	107.4	36.3	30.7	26.1
beta-Alanine	2.8	5.3	6.6	4.7	10.6	10.5	5	7.6	2.1	4.1	11.3	13.5	15.9	9.6	16.5	10.6	7	15.9	9.8	13	12.7	7.7	5.6
Cystathionine	8.4	34.9	36.7	17.6	26.1	21.2	7.7	33.1	12.3	33.1	12	28.1	10	18.6	29	7.5	24.4	30	6.5	6.1	30	28.5	22.4
NMR_METABOLITE_DATA_END
#METABOLITES
METABOLITES_START
metabolite_name	PubChem	KEGG
2-Hydroxyisobutyrate	11671	NA
3-Hydroxyisovalerate	69362	C20827
AMP	6083	C00020
Acetate	176	C00033
Adenine	190	C00147
Adenosine	60961	C00212
Alanine	5950	C00041
Arabinose	439195	C02479
Asparagine	6267	C00152
Aspartate	5960	C00049
Betaine	247	C00719
Choline	305	C00114
Coenzyme A	87642	C00010
Cytidine monophosphate	6131	C00055
Formate	284	C00058
Glucose	5793	C00221
Glutamate	33032	C00025
Glutamine	5961	C00064
Glycine	750	C00037
Guanosine	6802	C00387
Histidine	6274	C00135
Isoleucine	6306	C00407
Isovalerate	10430	C08262
Lactate	107689	C00186
Leucine	6106	C00123
Lysine	5962	C00047
NAD+	5893	C00003
NADP+	5886	C00006
Nicotinate	938	C00253
Phenylalanine	6140	C00079
Phosphoenolpyruvic acid	1005	C00074
Succinate	1110	C00042
Sucrose	5988	C00089
Threonine	6288	C00188
Tryptophan	6305	C00078
Tyrosine	6057	C00082
UMP	6030	C00105
Uracil	1174	C00106
Uridine	6029	C00299
Valine	6287	C00183
sn-Glycero-3-phosphocholine	71920	C00670
beta-Alanine	239	C00099
Cystathionine	439258	C02291
METABOLITES_END
#END