Qingxiang ZHENG
Received:
2022-09-23
Published:
2022-11-21
郑庆祥
作者简介:
基金资助:
CLC Number:
Qingxiang ZHENG. Metabolic flux analysis of Shewanella sp. MR-4 with different terminal electron receptors[J]. Synthetic Biology Journal, DOI: 10.12211/2096-8280.2022-052.
郑庆祥. 希瓦氏菌Shewanella sp. MR-4在不同末端电子受体条件下的代谢通量分析[J]. 合成生物学, DOI: 10.12211/2096-8280.2022-052.
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URL: https://synbioj.cip.com.cn/EN/10.12211/2096-8280.2022-052
Basic Solution | |
---|---|
Component | Concentration (mM) |
PIPES | 30 |
NHdCl | 28.04 |
KCl | 1.34 |
NaH2PO4 2H2O | 4.35 |
NaCl | 30 |
Na2SO4 | 0.7 |
Mineral Solution | |
Component | Concentration (µM) |
C6H9NO6 | 78.49 |
MgSO4 7H2O | 121.71 |
MnSO4 H2O | 29.58 |
FeSO4 7H2O | 3.6 |
CaCl2 2H2O | 6.8 |
CoCl2 6H2O | 4.2 |
ZnCl2 | 9.54 |
CuSO4 5H2O | 0.4 |
AlK (SO4)2 12H2O | 0.21 |
H3BO3 | 1.62 |
Na2MoO4 2H2O | 1.03 |
NiCl2 6H2O | 1.01 |
Na2WO4 2H2O | 0.76 |
Vitamin Solution | |
Component | Concentration (µM) |
biotin (d-biotin) | 81.87 |
folic acid | 45.34 |
pyridoxine HCl | 486.38 |
riboflavin | 132.84 |
thiamine HCl | 140.73 |
nicotinic acid | 406.17 |
d-pantothenic acid, hemi calcium salt | 209.82 |
B12 | 7.4 |
p-amino benzoic acid | 364.62 |
thioctic acid | 242.37 |
choline chloride | 14.3246 |
Table 1 Modified M1 minimal medium
Basic Solution | |
---|---|
Component | Concentration (mM) |
PIPES | 30 |
NHdCl | 28.04 |
KCl | 1.34 |
NaH2PO4 2H2O | 4.35 |
NaCl | 30 |
Na2SO4 | 0.7 |
Mineral Solution | |
Component | Concentration (µM) |
C6H9NO6 | 78.49 |
MgSO4 7H2O | 121.71 |
MnSO4 H2O | 29.58 |
FeSO4 7H2O | 3.6 |
CaCl2 2H2O | 6.8 |
CoCl2 6H2O | 4.2 |
ZnCl2 | 9.54 |
CuSO4 5H2O | 0.4 |
AlK (SO4)2 12H2O | 0.21 |
H3BO3 | 1.62 |
Na2MoO4 2H2O | 1.03 |
NiCl2 6H2O | 1.01 |
Na2WO4 2H2O | 0.76 |
Vitamin Solution | |
Component | Concentration (µM) |
biotin (d-biotin) | 81.87 |
folic acid | 45.34 |
pyridoxine HCl | 486.38 |
riboflavin | 132.84 |
thiamine HCl | 140.73 |
nicotinic acid | 406.17 |
d-pantothenic acid, hemi calcium salt | 209.82 |
B12 | 7.4 |
p-amino benzoic acid | 364.62 |
thioctic acid | 242.37 |
choline chloride | 14.3246 |
Lactate | Lactate | Glucose | Glucose | |
---|---|---|---|---|
Oxygen | Fumarate | Fumarate | Fe-NTA | |
(aerobic) | (anaerobic) | (anaerobic) | (anaerobic) | |
Shewanella putrefaciens CN-32 | + | + | + | - |
Shewanella loihica PV-4 | + | + | + | + |
Shewanella sp. MR-4 | + | + | + | + |
Shewanella amazonensis SB2B | + | + | + | + |
Shewanella sp. W3-18-1 | + | + | + | - |
Shewanella baltica OS155 | + | + | + | + |
Shewanella denitrificans OS217 | + | + | - | - |
Shewanella oneidensis MR-1 | + | + | - | - |
Shewanella sp. MR-7 | + | + | - | + |
Shewanella sp. ANA-3 | + | + | + | + |
Shewanella pealeana ANG-SQ1 | + | - | - | - |
Shewanella frigidimarina NCIMB400 | + | + | - | - |
Table 2 Growth phenotype of 12 Shewanella sp. strains
Lactate | Lactate | Glucose | Glucose | |
---|---|---|---|---|
Oxygen | Fumarate | Fumarate | Fe-NTA | |
(aerobic) | (anaerobic) | (anaerobic) | (anaerobic) | |
Shewanella putrefaciens CN-32 | + | + | + | - |
Shewanella loihica PV-4 | + | + | + | + |
Shewanella sp. MR-4 | + | + | + | + |
Shewanella amazonensis SB2B | + | + | + | + |
Shewanella sp. W3-18-1 | + | + | + | - |
Shewanella baltica OS155 | + | + | + | + |
Shewanella denitrificans OS217 | + | + | - | - |
Shewanella oneidensis MR-1 | + | + | - | - |
Shewanella sp. MR-7 | + | + | - | + |
Shewanella sp. ANA-3 | + | + | + | + |
Shewanella pealeana ANG-SQ1 | + | - | - | - |
Shewanella frigidimarina NCIMB400 | + | + | - | - |
Specific rate (mmol/gCDW/h) | ||||||
---|---|---|---|---|---|---|
Electron acceptor | % of glucose for biomass synthesis | Glucose uptake | Acetate secretion | EPS formation | Net CO2 formation | Carbon balance (%) |
Nitrate | 12.2 ± 0.5 | 8.27 ± 0.24 | 4.19 ± 0.21 | 2.49 ± 0.11 | 17.47 ± 0.94 | 94.5 |
Fe | 5.1 ± 0.2 | 4.86 ± 0.20 | 3.74 ± 0.19 | 1.28 ± 0.04 | 10.72 ± 0.35 | 93.9 |
Fumarate | 11.7 ± 0.4 | 5.04 ± 0.17 | 8.33 ± 0.54 | 0.31 ± 0.01 | 7.23 ± 0.38 | 96.8 |
DMSO | 5.9 ± 0.2 | 5.38 ± 0.15 | 9.48 ± 0.47 | 0.47 ± 0.02 | 6.92 ± 0.21 | 94.9 |
Table 3 Anaerobic growth parameters of Shewanella sp. MR-4 exposed to various terminal electron acceptors
Specific rate (mmol/gCDW/h) | ||||||
---|---|---|---|---|---|---|
Electron acceptor | % of glucose for biomass synthesis | Glucose uptake | Acetate secretion | EPS formation | Net CO2 formation | Carbon balance (%) |
Nitrate | 12.2 ± 0.5 | 8.27 ± 0.24 | 4.19 ± 0.21 | 2.49 ± 0.11 | 17.47 ± 0.94 | 94.5 |
Fe | 5.1 ± 0.2 | 4.86 ± 0.20 | 3.74 ± 0.19 | 1.28 ± 0.04 | 10.72 ± 0.35 | 93.9 |
Fumarate | 11.7 ± 0.4 | 5.04 ± 0.17 | 8.33 ± 0.54 | 0.31 ± 0.01 | 7.23 ± 0.38 | 96.8 |
DMSO | 5.9 ± 0.2 | 5.38 ± 0.15 | 9.48 ± 0.47 | 0.47 ± 0.02 | 6.92 ± 0.21 | 94.9 |
Reaction No. | Enzyme | Gene | Stoichiometric reaction | Carbon atom transition |
---|---|---|---|---|
v1 | glucokinase | Shewmr4_1763 | Glucose => G6P | #ABCDEF => #ABCDEF |
v2 | glucose-6-phosphate 1-dehydrogenase | Shewmr4_2046 | G6P => 6PG | #ABCDEF => #ABCDEF |
6-phosphogluconolactonase | Shewmr4_2045 | |||
v3 | phosphogluconate dehydratase | Shewmr4_2044 | 6PG => KDPG | #ABCDEF => #ABCDEF |
2-keto-3-deoxy-phosphogluconate aldolase | Shewmr4_2043 | KDPG => GAP + PYR | #ABCDEF => #DEF + #ABC | |
v4 | glucose-6-phosphate isomerase | Shewmr4_2968 | G6P <=> F6P | #ABCDEF <=> #ABCDEF |
v5 | 6-phosphogluconate dehydrogenase | Shewmr4_1609 | 6PG => P5P + CO2 | #ABCDEF => #BCDEF + #A |
v6 | transketolase | Shewmr4_0773 | S7P + GAP <=> P5P + P5P | #abcdefg + #ABC <=> #cdefg + #abABC |
v7 | transaldolase | Shewmr4_2967 | S7P + GAP <=> F6P + E4P | #abcdefg + #ABC <=> #abcABC + #defg |
v8 | transketolase | Shewmr4_0773 | F6P + GAP <=> P5P + E4P | #abcdef + #ABC <=> #abABC + #cdef |
v9 | glyceraldehy-3-phosphate dehydrogenase | Shewmr4_0536 | GAP <=> 1,3-BPG | #ABC <=> #ABC |
phosphoglycerate kinase | Shewmr4_0775 | 1,3-BPG <=> 3PG | #ABC <=> #ABC | |
phosphoglyceromutase | Shewmr4_0045 | 3PG <=> 2PG | #ABC <=> #ABC | |
enolase | Shewmr4_1115 | 2PG <=> PEP | #ABC <=> #ABC | |
v10 | pyruvate kinase | Shewmr4_2048 | PEP => PYR | #ABC => #ABC |
v11 | phosphoenolpyruvate carboxylase | Shewmr4_3710 | PEP + CO2 => OAA | #ABC + #D => #ABCD |
v12 | phosphoenolpyruvate carboxykinase | Shewmr4_0152 | OAA => PEP + CO2 | #ABCD => #ABC + #D |
v13 | NAD-dependent malic enzyme | Shewmr4_3188 | MAL <=> PYR + CO2 | #ABCD <=> #ABC + #D |
NADP-dependent malic enzyme | Shewmr4_3492 | |||
v14 | pyruvate dehydrogenase subunit E1 | Shewmr4_0428 | PYR =>ACoA + CO2 | #ABC=>#BC + #A |
pyruvate dehydrogenase complex dihydrolipoamide acetyltransferase | Shewmr4_0429 | |||
dihydrolipoamide dehydrogenase | Shewmr4_0430 | |||
v15 | type II citrate synthase | Shewmr4_1630 | ACoA + OAA => ICT | #abcd+#AB => #dcbaBA |
bifunctional aconitate hydratase | Shewmr4_0437 | |||
v16 | isocitrate dehydrogenase, NADP-dependent | Shewmr4_1606 | ICT => AKG + CO2 | #abcdef => #abcef + #d |
isocitrate dehydrogenase [NAD] | Shewmr4_2720 | |||
v17 | 2-oxoglutarate dehydrogenase E1 component | Shewmr4_1635 | AKG => FUM + CO2 | #ABCDE => #BCDE+#A |
dihydrolipoamide dehydrogenase | Shewmr4_0430 | |||
2-oxoglutarate dehydrogenase E2 component | Shewmr4_1636 | |||
succinyl-CoA synthetase subunit beta | Shewmr4_1637 | |||
fumarate reductase cytochrome b-556 subunit | Shewmr4_0402 | |||
fumarase | Shewmr4_2124 | FUM <=> MAL | #ABCD <=> #ABCD #ABCD => #DCBA | |
v18 | malate dehydrogenase | Shewmr4_3339 | MAL <=> OAA | #ABCD <=> #ABCD |
v19 | biomass synthesis | |||
v20 | acetate formation | ACoA => Ace | ||
v21 | EPS synthesis | G6P => EPS |
Table 4 Central metabolic network in Shewanella sp. MR-4 with the stoichiometric reactions and the corresponding carbon atom transitions
Reaction No. | Enzyme | Gene | Stoichiometric reaction | Carbon atom transition |
---|---|---|---|---|
v1 | glucokinase | Shewmr4_1763 | Glucose => G6P | #ABCDEF => #ABCDEF |
v2 | glucose-6-phosphate 1-dehydrogenase | Shewmr4_2046 | G6P => 6PG | #ABCDEF => #ABCDEF |
6-phosphogluconolactonase | Shewmr4_2045 | |||
v3 | phosphogluconate dehydratase | Shewmr4_2044 | 6PG => KDPG | #ABCDEF => #ABCDEF |
2-keto-3-deoxy-phosphogluconate aldolase | Shewmr4_2043 | KDPG => GAP + PYR | #ABCDEF => #DEF + #ABC | |
v4 | glucose-6-phosphate isomerase | Shewmr4_2968 | G6P <=> F6P | #ABCDEF <=> #ABCDEF |
v5 | 6-phosphogluconate dehydrogenase | Shewmr4_1609 | 6PG => P5P + CO2 | #ABCDEF => #BCDEF + #A |
v6 | transketolase | Shewmr4_0773 | S7P + GAP <=> P5P + P5P | #abcdefg + #ABC <=> #cdefg + #abABC |
v7 | transaldolase | Shewmr4_2967 | S7P + GAP <=> F6P + E4P | #abcdefg + #ABC <=> #abcABC + #defg |
v8 | transketolase | Shewmr4_0773 | F6P + GAP <=> P5P + E4P | #abcdef + #ABC <=> #abABC + #cdef |
v9 | glyceraldehy-3-phosphate dehydrogenase | Shewmr4_0536 | GAP <=> 1,3-BPG | #ABC <=> #ABC |
phosphoglycerate kinase | Shewmr4_0775 | 1,3-BPG <=> 3PG | #ABC <=> #ABC | |
phosphoglyceromutase | Shewmr4_0045 | 3PG <=> 2PG | #ABC <=> #ABC | |
enolase | Shewmr4_1115 | 2PG <=> PEP | #ABC <=> #ABC | |
v10 | pyruvate kinase | Shewmr4_2048 | PEP => PYR | #ABC => #ABC |
v11 | phosphoenolpyruvate carboxylase | Shewmr4_3710 | PEP + CO2 => OAA | #ABC + #D => #ABCD |
v12 | phosphoenolpyruvate carboxykinase | Shewmr4_0152 | OAA => PEP + CO2 | #ABCD => #ABC + #D |
v13 | NAD-dependent malic enzyme | Shewmr4_3188 | MAL <=> PYR + CO2 | #ABCD <=> #ABC + #D |
NADP-dependent malic enzyme | Shewmr4_3492 | |||
v14 | pyruvate dehydrogenase subunit E1 | Shewmr4_0428 | PYR =>ACoA + CO2 | #ABC=>#BC + #A |
pyruvate dehydrogenase complex dihydrolipoamide acetyltransferase | Shewmr4_0429 | |||
dihydrolipoamide dehydrogenase | Shewmr4_0430 | |||
v15 | type II citrate synthase | Shewmr4_1630 | ACoA + OAA => ICT | #abcd+#AB => #dcbaBA |
bifunctional aconitate hydratase | Shewmr4_0437 | |||
v16 | isocitrate dehydrogenase, NADP-dependent | Shewmr4_1606 | ICT => AKG + CO2 | #abcdef => #abcef + #d |
isocitrate dehydrogenase [NAD] | Shewmr4_2720 | |||
v17 | 2-oxoglutarate dehydrogenase E1 component | Shewmr4_1635 | AKG => FUM + CO2 | #ABCDE => #BCDE+#A |
dihydrolipoamide dehydrogenase | Shewmr4_0430 | |||
2-oxoglutarate dehydrogenase E2 component | Shewmr4_1636 | |||
succinyl-CoA synthetase subunit beta | Shewmr4_1637 | |||
fumarate reductase cytochrome b-556 subunit | Shewmr4_0402 | |||
fumarase | Shewmr4_2124 | FUM <=> MAL | #ABCD <=> #ABCD #ABCD => #DCBA | |
v18 | malate dehydrogenase | Shewmr4_3339 | MAL <=> OAA | #ABCD <=> #ABCD |
v19 | biomass synthesis | |||
v20 | acetate formation | ACoA => Ace | ||
v21 | EPS synthesis | G6P => EPS |
Fig. 1 Bioreaction network of central carbon metabolism of Shewanella sp. MR-4. Dashed arrows indicate reactions or pathways identified to be inactive in this study. Double-headed arrows indicate reactions assumed to be reversible.
% of total pool in Shewanella sp. MR-4 | ||||
---|---|---|---|---|
Metabolite | Nitrate | Fe | DMSO | Fumarate |
PEP from PP pathway (ub) | 2.2 | 3.2 | 6.7 | 1.9 |
PEP from OAA (ub) | 2.7 | 2.7 | 6.7 | 0.0 |
PYR from OAA (ub) | 7.2 | 11.8 | 29.8 | 0.5 |
PYR from OAA (lb) | 3.4 | 9.7 | 11.7 | 0.5 |
OAA from PEP | 0.0 | 0.0 | 80.7 | 93.1 |
MAL from PYR | 33.5 | 84.3 | 0.0 | 0.0 |
OAA from glyoxylate shunt | 0.0 | 0.0 | 0.0 | 0.0 |
Ser from Gly | 0.0 | 28.6 | 18.6 | 23.0 |
Gly from Ser | 84.2 | 77.0 | 100.0 | 86.1 |
Table 5 Origins of metabolic intermediates determined by flux ratio analysis
% of total pool in Shewanella sp. MR-4 | ||||
---|---|---|---|---|
Metabolite | Nitrate | Fe | DMSO | Fumarate |
PEP from PP pathway (ub) | 2.2 | 3.2 | 6.7 | 1.9 |
PEP from OAA (ub) | 2.7 | 2.7 | 6.7 | 0.0 |
PYR from OAA (ub) | 7.2 | 11.8 | 29.8 | 0.5 |
PYR from OAA (lb) | 3.4 | 9.7 | 11.7 | 0.5 |
OAA from PEP | 0.0 | 0.0 | 80.7 | 93.1 |
MAL from PYR | 33.5 | 84.3 | 0.0 | 0.0 |
OAA from glyoxylate shunt | 0.0 | 0.0 | 0.0 | 0.0 |
Ser from Gly | 0.0 | 28.6 | 18.6 | 23.0 |
Gly from Ser | 84.2 | 77.0 | 100.0 | 86.1 |
Fig. 2 Intracellular metabolic flux distributions in Shewanella sp. MR-4 with (a) nitrate, Fe3+, (b) fumarate or DMSO as terminal electron acceptor. The number beside a metabolic reaction denotes its net flux, which was normalized by specific rate of glucose uptake. Pairs of number: (a) top, nitrate; bottom, Fe3+. (b) Top, fumarate; bottom, DMSO.
Fig. 3 NADH balancing based on metabolic flux distributions. NADH formed by PDH complex, the TCA cycle and biomass synthesis. NADH was consumed via electron acceptor reduction. NADH consumption rate cannot be determined with nitrate as terminal electron acceptor.
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