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Phosphorus is one of the most important macronutrients for the primary production. The transformation of dissolved organic phosphorus in the environment and its contribution to biological production in the different ecosystems is still a mystery. Recently, it was demonstrated that phosphate ester can be rapidly hydrolyzed in solutions containing iron oxide nanoparticles with enzyme kinetics. The catalyst is sensitive to temperature and pH changes and inhibited by tetrahedral oxyanions with an order of PO4 < MoO4 < WO4. The oxo-Fe structure in the iron oxide nanoparticles, like the metal center of natural phosphatase (e.g., purple acid phosphatase, PAP), might contribute to the observed catalytic activity. Iron oxide nanoparticles are very common and widely exist in the current earth environment, and phosphate esters are the main component of dissolved organic phosphorus in soil and waters. It is expected that iron oxide nanoparticles in aqueous environments, as an inorganic phosphatase, play a critical role for the phosphorus transformation from the view of the phosphorus cycle.
*Address all correspondence to: xiaolan.huang@ymail.com
1. Introduction
Phosphorus is one of the most important macronutrients for the primary production, which is primarily taken up by plants in the form of phosphate ions (HPO42− and H2PO4−). Most of the knowledge of phosphorus in the environment, including the phosphorus geochemistry cycle, comes from inorganic phosphates [1, 2, 3, 4]. The dissolved organic phosphorus transformation and its contribution to the biological production in the different ecosystems, e.g., soil, lake, estuary and ocean, is still a mystery [5, 6, 7]. Recently some limited works have indicated that different phosphate esters, especially monoesters are the main components in the dissolved organic phosphorus in soils [8, 9, 10, 11] and waters [12, 13, 14, 15, 16, 17], which might be an important source of P phytoavailability and a potential source of water eutrophication. The phosphomonoesters in supra-/macro-molecular structures were found to account for the majority (61–73%) of soil organic P in diverse agricultural soils across the world and the monoester P pool was estimated to account for 33% of the total phosphorus (587 ± 32 kg ha−1) by a recently review [18].
In general, the phosphate ester hydrolysis is catalyzed by various enzymes, including purple acid phosphatases (PAPs), which have been identified and characterized from plant, animal and bacterial organisms [19]. On the other hand, several studies have already demonstrated that the phosphate ester can be hydrolyzed with the interaction of minerals in the aqueous environments [5, 20, 21, 22, 23, 24, 25]. Here, the results of laboratory study on the hydrolysis of phosphorus esters, promoted by the iron oxide nanoparticles in water, including the aged nanomolar inorganic iron ion solutions [26, 27, 28], were summarized. Additionally, the potential role of inorganic iron oxide nanoparticle for the phosphorus cycles due to the intrinsic phosphoesterase activity is postulated.
2. Promotion effect on the phosphate esters hydrolysis
Usually, phosphate ester in water is quite stable. As an example, hydrolysis Glucose 6-phosphate (G6P), a very common phosphate ester in nature, is a slow process without enzyme in the medium of deionized water (DIW), and becomes even slower in the fresh nanomolar inorganic iron solutions. Inorganic orthophosphate (Pi) in the DIW with the addition of 100 μM G6P at room temperature (22 ± 2°C) was initially 0.90 ± 0.04 μM, which became 4.86 ± 0.26 and 10.35 ± 1.19 μM at 4 and 12 days, respectively. The corresponding Pi in the fresh nanomole inorganic iron solutions (0.5–50 nM Fe(NO3)3) were 1.35 ± 0.09 and 2.55 ± 0.15 μM.
After G6P was added into an aged 14-month 16.5 nM Fe(NO3)3 solution (pH 6.30) at room temperature, made by acid-forced hydrolysis [27], the Pi was rapidly released (e.g. the initial 20 μM G6P, as presented in Figure 1). Like metal ions as well as natural and biomimetic enzymes, the kinetics of G6P hydrolysis in the aged iron solution can be described as a pseudo-first-order reaction for a fixed concentration of G6P [29, 30, 31, 32, 33, 34, 35, 36]. For the initial 20 μM G6P, the decrease in G6P concentration, [G6P]t, due to its hydrolysis can be expressed as a function of hydrolysis time, t, as
Figure 1.
Hydrolysis of 20 μM G6P in a 16.5 nM Fe(NO3)3 solution aged 14 months at room temperature (22 ± 2°C). (a) Time courses of formation of phosphorantimonylmolybdenum blue complex from phosphate released from hydrolysis of 20 μM G6P at times of 0, 1, 3, and 6 h, respectively; (b) concentration of Pi and G6P during G6P hydrolysis; and (c) pseudo first-order reaction kinetics of G6P.
logG6Pt=−1.31×10−5t−4.718r2=0.999E1
where [G6P]t is in M and t is in second.
The corresponding reaction rate constant (k) was 3.02 × 10−6 s−1, and the half-life (t1/2) was 6.38 h. Similar to the initial 20 μM of G6P, the Pi concentration of a initial 100 μM of G6P in the aged inorganic iron solution at 1, 3 and 6.7 h was 4.95, 10.74 and 20.62 μM, respectively. The corresponding k was 8.83 × 10−6 s−1, and the t1/2 was 21.8 h. It is highlighted that these k in the aged iron solution were much higher than the previously reported rates in the presence of the fresh unaged nanomolar inorganic iron [26] and millimole metals [30, 31, 32] solutions.
Like aged inorganic iron solution, the concentration of phosphate esters and condensed inorganic phosphate decreased, and inorganic orthophosphate (Pi) increased in a solution bearing iron oxide (IO) nanoparticles, which consists of a dialysis membrane tube (DMT, e.g., Spectra/Por 1 membranes, molecular weight cut-off (MWCO) 6000–8000 Da) filled with iron oxide (DMT-IO). The iron oxide (D) was synthesized by Fe(NO3)3 following the basic protocol of Atkinson [37] and aged at 80°C [28]. The k for 100 μM G6P, Glycerol-2-phosphate (3-carbon, G2P), and three energy metabolism compounds, i.e., adenosine monophosphate (AMP), adenosine diphosphate (ADP), adenosine triphosphate (ATP), as well as two inorganic condensed phosphates, i.e., polyphosphate (poly-Pi), and pyrophosphate (PPi) at room temperature (22°C) was 2.69 × 10−5, 1.68 × 10−5, 1.54 × 10−5, 5.73 × 10−6, 5.76 × 10−6, 3.8 × 10−6, and 5.09 × 10−6 s−1, respectively. The corresponding t1/2 of these phosphorus esters and inorganic condensed phosphates was 7.1, 11.5, 12.5, 33.6, 33.4, 50.7, and 37.8 h, respectively.
Measured k of the initial 20 μM G6P with different sources of iron, either the aged inorganic iron solutions or the solutions bearing inorganic iron oxide nanoparticles (DMT-IO), are listed in Table 1. The half-life for aged 4-month Fe(NO3)3 (16.5 nM), FeCl3 (10 nM) and Fe(ClO4)3(10 nM) was 37.8, 58.6 and 78.4 h, respectively, whereas the half-life of IO from the same source (Fe(NO3)3, JT Baker), aged at 5–80°C was 11, 2.7, 3.2 and 2.8 h, though they were in the same order of magnitude. The same patterns were observed for the ATP as well [28]. These results further indicate, as expected, that the behavior of catalysis depends on the sources of iron oxides nanoparticles in solutions—whether FeCl3, or Fe(NO3)3, and even on the different manufacturers, as well as with the different aging temperatures for IO (5–80°C) [37, 38]. No clear relationships between ferric ion (III) sources, age processing, and catalytic activity, with the hydrolysis rate constant, were observed.
Fe source
Manufacturer
Aged time (mo.)
Aged temperature (°C)
IO nanoparticles or total Fe concentration (nM)
20 μM G6P
k (10−6 s−1)
t0.5 (h)
Iron oxide nanoparticles (IO)
Fe(NO3)3
JT Baker
0.25
5
A
16.9
11
Fe(NO3)3
JT Baker
0.25
22
B
70.3
2.7
Fe(NO3)3
JT Baker
0.25
50
C
59.5
3.2
Fe(NO3)3
JT Baker
0.25
80
D
106
1.8
FeCl3
JT Baker
0.25
25
E
13.8
14
Fe(NO3)3
Riedel-de Haën
0.25
50
H
18.5
4.0
FeCl3
Riedel-de Haën
0.25
50
F
27.4
7.0
Fe(NO3)3
Riedel-de Haën
0.25
80
L
80.7
2.4
FeCl3
Riedel-de Haën
0.25
80
G
54.1
3.6
Aged acidic forced hydrolysis inorganic Fe solution
Fe(NO3)3
JT Baker
14
22
16.5
30.17
6.4
Riedel-de Haën
4
22
16.5
5.08
37.8
22
100
2.96
65.6
6
22
1000
18.77
10.3
Iron standard solution (metal Fe in 0.3 M HNO3)
JT Baker
4
22
1
2.38
81.0
2.5
4.85
39.7
7.5
7.22
26.7
50
6.38
30.2
100
6.55
29.4
200
6.58
29.2
500
8.14
23.6
1000
5.86
32.8
FeCl3
JT Baker
16
22
2
6.59
29.2
10
4.95
38.9
Riedel-de Haën
4
22
10
3.28
58.6
100
0.83
231.9
FeClO4
Aldrich
4
22
10
2.46
78.4
100
0.61
318.3
Fe(NH4)2(SO4)2
EM Science
16
22
16.5
9.49
20.3
Table 1.
Hydrolysis rate constant of 20 μM G6P in inorganic iron solutions.a
The hydrolysis rate constant of 20 μM G6P in the DIW is 1.84 × 10−8 s−1, and the corresponding half time is 10,450 h.
These inorganic iron solutions also have the same promotion effects on hydrolysis of different sugar phosphates, including G2P, ribose-5-phosphate (5-carbon, R5P), and fructose 1-phosphate (6-carbon, F1P) (Table 2). As expected, the promotion effect was also found on the hydrolysis of AMP, ADP and ATP, and inorganic condense phosphates (poly-Pi and PPi) as well as the RNA model compound (4-nitrophenyl phosphate ester, pNPP). However, no promotion effects were observed for the hydrolysis of phosphonates (C-P bonded compounds, e.g., 2-aminoethylphosphonic acid, phosphono-formic acid) and inositol hexakisphosphate (IP6) (data not shown).
Phosphate ester
Fe source
Initial OP (μM)
Rate constant k (10−6 s−1)
Half-life t0.5 (h)
Glycerol-2-phosphate (G2P)
Fe standard solution, 7.5 nM, 4 mo.
10
12.69
15.2
20
6.4
30.1
50
3.45
55.8
500
0.51
374.3
Fe(NO3)3, 1000 nM, 6 mo.
20
30.12
6.4
FeCl3, 2 nM, 16 mo.
20
5.29
36.4
Fe(NH4)2(SO4)2, 16.5 nM, 16 mo.
20
11.44
16.8
IO-D (made by Fe(NO3)3, aged a week at 80°C, soak 1 month at 22°C)
10
85.02
2.26
50
26.91
7.15
100
16.39
11.74
Ribose-5-phosphate (R5P)
Fe standard solution, 7.5 nM, 4 mo.
10
13.92
13.8
20
8.15
23.6
Fe(NO3)3, 1000 nM, 6 mo.
20
25.19
7.6
FeCl3, 2 nM, 16 mo.
20
7.24
26.6
Fe(NH4)2(SO4)2, 16.5 nM, 16 mo.
20
16.16
11.9
Fuctose-1-phosphate (F1P)
Fe standard solution, 7.5 nM, 4 mo.
10
8.66
22.2
20
5.25
36.4
Fe(NO3)3, 1000 nM, 6 mo.
20
17.08
11.3
FeCl3, 2 nM, 16 mo.
20
5.29
36.4
Fe(NH4)2(SO4)2, 16.5 nM, 16 mo.
20
8.5
22.6
Adenosine monophosphate (AMP)
IO-D (made by Fe(NO3)3, aged a week at 80°C, soak 1 month at 22°C)
10
79
2.44
100
15.4
12.5
250
6.2
31.1
Adenosine diphosphate (ADP)
IO-D (made by Fe(NO3)3, aged a week at 80°C, soak 1 month at 22°C)
10
134
1.44
100
5.73
33.6
250
1.59
121
Adenosine triphosphate (ATP)
IO-D (made by Fe(NO3)3, aged a week at 80°C, soak 1 month at 22°C)
10
61.5
3.13
25
30.2
6.38
100
4.4
43.8
IO-A(made by Fe(NO3)3, aged a week at 5°C, soak 1 month at 22°C)
20
19.6
9.8
100
10.8
17.9
IO-B (made by Fe(NO3)3, aged a week at 22°C, soak 1 month at 22°C)
20
40.4
4.8
100
8.46
22.7
IO-G (made by FeCl3, aged a week at 80°C, soak 1 month at 22°C)
20
38.7
5.0
100
3.55
54.3
Polyphosphate (poly-Pi)
IO-D (made by Fe(NO3)3, aged a week at 80°C, soak 1 month at 22°C)
10
67.5
2.85
100
3.8
50.7
250
0.39
492
Pyrophosphate (PPi)
IO-D (made by Fe(NO3)3, aged a week at 80°C, soak 1 month at 22°C)
10
162
1.19
100
5.09
37.8
250
0.71
270
Table 2.
Phosphate ester hydrolysis in the different inorganic iron solutions.
As expected, the catalytic activity is related to the soaked time of DIW with DMT-IO and the nature of IO, which can be described by the hydrolysis reaction rate constant. The kinetics of k of 100 μM G6P and ATP in three different IOs is presented in Figure 2. These results can be explained by the changes of the nanoparticles concentration in the water. It was expected that the concentration of the IO nanoparticles in these solutions would initially increase up to 10 days and then reach equilibrium. However, the total dissolved iron concentrations in these solutions were still beneath the detection limits of iron (0.1 nM) [39].
Figure 2.
Relationship between the soaked time of IO and hydrolysis rate of phosphorus in different DMT-IO solutions: (a) 100 μM G6P, and (b) 100 μM ATP (for details of IOs see Table 1).
As presented in Table 2, the hydrolysis reaction rate constant at different initial concentrations of phosphate esters in these aged inorganic iron salt solutions or inorganic iron oxides solutions were not constant. Surprisingly, the k from 5 to 250 μM G6P in the 16.5 nM Fe(NO3)3 solution aged for 14 months at room temperature can be further described by the Michaelis-Menten equation (Figure 5a and b), as the typical behavior of biocatalysts. This is contrast to previously reported promotion effects by metals [30, 31, 32, 40] and minerals [20, 22, 23, 41, 42]. The maximum k of G6P hydrolysis was about 1 nM s−1, or 3.6 μM h−1, and the Michaelis-Menten constant (Km) was 13.7 μM of this aged inorganic iron solution.
1v=9.985×108+1.371×109G6Por2=0.997E2
In fact, the promotion effect of G6P hydrolysis can be extended to 2500 μM in this aged iron solution with a k of 6.53 × 10−7 s−1, and t1/2 of 295 h. It should be pointed out that the concentration of total phosphorus in the solution was 103–105 higher than that of iron in the solution (e.g., 16.5 nM Fe and 2500 μM G6P).
The same patterns were also observed in the solution bearing inorganic iron oxide nanoparticles. Like the aged inorganic iron solution, the k of various organic phosphate esters or condensed phosphates at different concentrations were not constant (Table 2). The catalytic activity of the different concentration of phosphorus also can be described by the typical Michaelis-Menten equations (Figure 3c). Based on the Lineweaver-Burk linear equation (1/V is a linear function of 1/[S]), the Michaelis-Menten constant (Km) and maximum velocity (Vm), as well as the range of concentration of phosphorous among these compounds, were determined (Table 3). Meanwhile, the catalysis activity was still observed even when the total phosphorus esters exceeded the range of the Michaelis-Menten equations, as with many of the natural enzymes, including the PAP [43].
Figure 3.
Kinetics of hydrolysis of phosphate esters in inorganic iron solutions at room temperature (22 ± 2°C). (a) Double reciprocal (initial velocity and initial concentration of G6P) plot of G6P in the 14 month aged 16.5 nM Fe(NO3)3 solution, (b) initial velocity of G6P hydrolysis (v0) as a function of the initial concentration of G6P in the aged iron solution, and (c) Lineweaver-Burk plot of different phosphate compounds in a DMT-IO solutions (IO-D).
Phosphorus source
Vm (nM S−1)
Km (μM)
Range (μM)
r2
G2P
2.0
7.0
6–200
0.99
G6P
3.2
8.3
5–100
0.99
ATP
0.9
9.2
5–50
0.99
Polyphosphate (poly-Pi)
1.1
5.5
5–25
1.00
Pyrophosphate (PPi)
2.2
1.3
5–25
0.98
Table 3.
Michaelis-Menten constant (Km) and maximum velocity (Vm) of different phosphorus in a DMT-IO solution (made by Fe(NO3)3·9H2O and NaOH, aged a week at 80°C, IO-D, soaked a month).
It should further be pointed out that the similar enzyme kinetics (Michaelis-Menten equations) were observed recently by many inorganic nanoparticles studies, which have been described as nanozyme [44, 45, 46, 47]. For example, Fe3O4 [44], α-Fe2O3 [48], γ-Fe2O3 [49], γ-FeOOH [50], Co3O4 [51], MnFe2O4 [52, 53], MFe2O4 (M = Mg, Ni, Cu) [54], ZnFe2O4 [55], NiO [56], and MnO2 [57] have been observed to have peroxidase-like or catalase-like activity, whereas the vanadium pentoxide (V2O5) was demonstrated to have antioxidant enzyme-like (glutathione peroxidase) activity [58, 59, 60, 61] and molybdenum trioxide (MoO3) nanoparticles to have sulfite oxidase activity [62].
The hydrolysis of phosphorus ester was significantly inhibited when the tetrahedral oxyanions were introduced into inorganic iron oxides nanoparticle solution, e.g., G6P in a 10-month aged iron solution (Figure 4), as the natural PAPs. Both the catalytic and the inhibition behaviors of the catalysis in the presence of 5–125 μM G6P with different tetrahedral oxyanions can be described by a Michaelis-Menten equation (Eqs. (3)–(7)) as follows:
Figure 4.
Inhibiting behavior of different tetrahedral oxyanions on the hydrolysis of Glucose-6-phosphate in an aged 10-month, 1000 nM Fe(NO3)3 solution at room temperature (22 ± 2°C). (a) Effect of initial concentration of G6P on the initial hydrolysis velocity of G6P, and (b) Lineweaver-Burk plot of aged iron solution in the absence and presence of tetrahedral oxyanions.
The results indicated that the catalysis sites from these catalyst, i.e., the inorganic iron oxide nanoparticles, may be only bound to either the tetrahedral oxyanions (PO4, MoO4, and WO4) or phosphate esters to form an intermediate, but cannot bind both of them at any given moment. The modes of tetrahedral oxyanions and G6P are competitive (Figure 5). The Km, the G6P concentration at which the reaction rate reaches one-half of maximum velocity (vmax/2), was about 2.7 μM G6P in this aged iron solutions with no inhibitors. The KMapp with addition 1 μM WO4, MoO4, and 5 and 10 μM PO4 was 46.2, 14.1, 11.1 and 17.1 μM G6P, respectively. Therefore, the Ki of WO4, MoO4, and PO4 are 0.06, 0.24 and 1.6–1.9 μM, respectively. It is interesting to compare the catalytic behavior of these inorganic iron oxides nanoparticles solution to natural PAPs and their biomimetics, though the velocities of hydrolysis G6P in the inorganic catalyst are still lower than that of natural phosphoesterase. For natural PAPs, Km and Ki of PO4 is usually in the millimolar range [63, 64, 65, 66, 67, 68, 69], only Ki of WO4 and MoO4 is in the micromolar range [65, 66, 70, 71, 72]. The value of Km of G6P is 920 μM for PAP extracted from sweet potato [33] and 300–310 μM for those from soybean seed [73]. Besides, the modes of molybdate and tungstate inhibition are noncompetitive [65, 66, 70, 71, 72, 73, 74]. Only orthophosphate for natural PAPs are competitive [65, 66] in most cases.
Figure 5.
Diagram of catalysis process of G6P hydrolysis in the presence of the tetrahedral anions in the aged inorganic iron solutions. (a) Reaction without tetrahedral anions; (b) Inhibition with the competitive tetrahedral anions.
A more significant difference between the inorganic catalyst and the natural phosphoesterase is revealed in their response to the fluoride ion. The activity of all known natural phosphoesterase is very sensitive to fluoride, even at the micromolar level [67, 72, 73, 74, 75, 76, 77, 78], while the catalytic activity of the inorganic iron oxides solutions still remain, even when the final concentration of fluoride in the solutions were up to 0.5 M.
The catalyst on the hydrolysis of phosphate ester is sensitive to temperature, as natural enzymes. The optimum temperature for the phosphate ester hydrolysis reaction by these inorganic catalysts was around 50°C (Figure 6), which is comparable to recent observations on the natural enzymes [79, 80, 81, 82]. However, catalytic activity of the IO nanoparticles in solution was lost as the temperature was raised to 90°C for an hour or to 72°C for 16 h. This behavior is similar to the thermal denaturation of the natural enzyme. Moreover, the temperature coefficient, Q10, a measure of the hydrolysis velocity, is also decreased as a consequence of increasing the temperature by 10°C. This effect too, is comparable to the general patterns of enzyme behavior in biological systems [80, 81]. Taken together, these observations also carry the implication that moderate, i.e., 50°C, and not high temperatures, were likely favorable to the catalytic reactions from the view of efficiency and speed of the catalyst.
Figure 6.
Relationship between environment temperature and the hydrolysis rate of phosphorus. (a) G6P, (b) ATP, (c) polyphosphate, and (d) the temperature coefficient Q10 (for details of IOs see Table 1).
In actuality, the catalytic activity of the nanoparticles remained high after removal from their source (IO) for days, even when stored at −18°C, demonstrated by a storage experiment (Table 4) [29], which further suggested that IO nanoparticles can be displaced to a considerable distance from their source and still maintain catalytic activities for a considerable time. Meanwhile, low temperatures, even frozen conditions, also favor the persistence of catalytic activity from these IO nanoparticles. These are important from the view of astrobiology (origin of life) [28], but also for plant acquisition, nanoengineering and the potential application for industrial production.
Treatment
20 μM G6P
20 μM ATP
1 h Pi (μM)
5 h Pi (μM)
t0.5 (h)
1 h Pi (μM)
5 h Pi (μM)
t0.5 (h)
11 days at 22°C
11R
5.49 ± 0.004
13.89 ± 0.064
3.2
4.47 ± 0.016
9.87 ± 0.255
6.0
11 days at 4°C
11 L
5.51 ± 0.010
13.64 ± 0.042
3.3
4.36 ± 0.005
9.71 ± 0.066
6.3
5 days frozen (−18°C) and 6 days at 4°C
5F6L
4.57 ± 0.013
11.48 ± 0.030
4.5
3.76 ± 0.009
7.61 ± 0.043
9.4
5 days at 4°C and 6 days at 22°C
5L6R
5.85 ± 0.011
14.10 ± 0.211
3.1
4.51 ± 0.018
10.30 ± 0.123
5.7
5 days at 50°C and 6 days at 22°C
5H6R
2.93 ± 0.01
6.68 ± 0.020
11
2.71 ± 0.012
4.92 ± 0.032
19
5 days at 50°C and 6 days at 4°C
5H6L
2.62 ± 0.002
5.44 ± 0.001
16
2.48 ± 0.002
3.72 ± 0.04
36
9 days at 50°C and 2 days at 22°C
9H2R
2.43 ± 0.005
4.07 ± 0.005
26
2.38 ± 0.016
3.08 ± 0.025
60
Table 4.
Effect of storage conditions on the catalysis activity of iron oxide (IO-F) nanoparticle solutions.a
The Pi of the 20 μM G6P (DIW, control) after 120 h at the room temperature was changed from 1.67 to 1.83 μM. The corresponding half-life was 10,450 h. The Pi of the 20 μM ATP (DIW, control) after 120 h at the room temperature was changed from 1.89 to 2.07 μM. The corresponding half-life was 9290 h.
pH is another key factor for enzyme activity. The aged inorganic iron solution or the water bearing iron oxide nanoparticles, e.g., DMT-IO, are generally mildly acidic (pH 5.5–6.5). Various concentrations of bicarbonate were introduced in the DMT-IO system, but in all cases enzyme-like activity for phosphate ester hydrolysis remained quite high (Figure 7a). In general, the most favorable pH of the enzyme-like activity was found to be between 6 and 7, though the phosphorus source, the concentrations of bicarbonate, and the type of DMT-IO also influenced its activity (Figure 7b and c). When pH was raised beyond 7 (e.g., pH 7, 7.2 and 8), the catalysis coefficient, k, decreased as the concentration of HCO3 increased, especially for the DMT-IO-D. When pH in solution was <7 (e.g., pH 6.2, 6.4, and 6.8), however, there were no clear patterns of k with respect to the concentration of HCO3 and both the ATP and G6P in these two nanoparticles-bearing solutions. At the same time, k at weak acidic conditions (pH 6.2–6.8) was much higher than at weak base conditions (pH 7–8). This conclusion was further supported by an additional experiment involving the hydrolysis of ATP, whereby the pH values of DMT-IO solution were extended from 4 to 9.3 units by employing four different buffer systems (1.0 M acetate buffer (pH 4.0–5.6), 0.2 M dimethylglutaric acid buffer (pH 4.2–6.8), 20 mM NaHCO3 (pH 7.6–9.3), and 40 mM NaHCO3 (pH 5.8–9.3)) (Figure 7d).
Figure 7.
Relationship between pH and the hydrolysis rate of phosphorus. (a) 100 μM four phosphorus in DMT-IO-G; (b) and (c) bicarbonate concentration on 20 μM G6P DMT-IO-D and F; (d) different buffers for 20 μM ATP in DMT-IO-F (for details of IOs see Table 1).
It should be pointed out that the catalysis capacity of these solutions bearing inorganic iron oxide nanoparticles is closely related to the buffer used in the system. The catalytic activity dropped precipitously after a small amount of citrate buffer (pH 4.0–6.2) or tris(hydroxymethyl)-aminomethane (TRIS) (pH 5.8–7.2) was introduced into an inorganic iron solution (Table 5). Both citrate [83, 84] and TRIS [85] can react with Fe (III) in solution to form the aqueous Fe-complex, particularly at high ratios of citrate or TRIS to Fe (>>10,000:1 molar ratio). But the catalysis of these solutions does not change when the acetic acid-acetate buffer system was introduced, the final acetate concentration in the solution was up to 0.25 M. All of these responses imply that the significant change was not due to the pH itself, but to the interactions between nanoparticles in the solution and chemicals in the environment. It has been reported that some buffer systems can significantly inhibit the activity of natural enzymes, for example, citrate on special PAPs [86] and alkaline phosphatase [87] and TRIS on aminopeptidase and RimO methylthiotransferase [88, 89] due to structure changes and metal-complex formation [84, 85, 90].
Aged 14 mo., Fe(NO3)3, 1000 nM and tris–HCl buffer (10 mM, pH 7.0), 1:1
20
0
0.22
1.72
111.8
1
0.35
2
0.41
6
0.93
DIW and aged 14 mo., 1000 nM, Fe(NO3)3, (1:1)
50
0
0.44
11.3
17.1
1
2.45
2
4.58
6
11.14
Aged 14 mo., Fe(NO3)3, 1000 nM and tris–HCl buffer (10 mM, pH 7.0), 1:1
50
0
0.44
1.93
99.8
1
0.71
2
0.99
6
2.45
Table 5.
Interaction between Tris-HCl buffer and aged inorganic iron solution on the hydrolysis rate of G6P.a
Buffer experiments were conducted with a 1000 nM aged (14-month) inorganic iron solution. The iron solution diluted by DIW (1:1) was used as a control. Either 4 ml of 10 mM Tris-HCl (pH 7.0) or 4 ml of DIW was mixed with a 4 ml of aged iron solution, then 0.1 ml of 1.6 or 4.0 mM G6P stock solution was added to make a final solution containing 20 or 50 μM G6P. Pi concentration was determined at 0, 0.17, 1, 2 and 6 h, respectively, after the addition of G6P. The results of Pi in the table was an average of three replications. The rate constant and half-life were calculated based on the first order kinetics.
Recall the natural phosphatase, a binuclear metal center (di-iron Fe-Fe or Fe-M (M as Mn and Zn)) that produces orthophosphate due to the net transfer of the phosphoryl group to water, is essential for its catalysis (Figure 8a) [19, 66, 91, 92, 93, 94]. The μ-(hydr)oxo ligand bridges in the metal center—the key of “phosphoesterase motif”—are a universal feature in binuclear phosphoesterase [19, 94]. They are responsible for the cleavage of phosphoester bonds; including acid and alkaline phosphatases; bacterial exonucleases; diadenosine tetraphosphatase; 5′-nucleotidase; phosphodiesterase; sphingomyelin phosphodiesterase, an enzyme involved in RNA debranching; and a phosphatase in the bacteriophage genome as well as for the family of Ser/Thr protein phosphatase (PP1, PP2A, and calcineurin) [95, 96]. Based on the μ-(hydr)oxo metal bridge structure, different artificial phosphatases have been synthesized by using different organic ligands to stabilize the metal center [19, 97, 98].
Figure 8.
The metal center of phosphatase. (a) The μ-(hydr)oxo-bridges in purple acid phosphatase (PAP), and (b) Fe-Fe structure in different iron oxides phases.
It is well known that iron speciation changes due to ion (III) hydrolysis in the solution during the aging process, diiron or polyirons oxide with the oxo-bridge or hydroxo-bridge (bond) might be formed [99, 100, 101, 102, 103]. Based on the quantum-chemical calculations by density-functional theory, dihydroxobridging binuclear compounds can be present in aqueous solutions, as binuclear dihydroxobridging [Fe(H2O)4(μ-OH)2Fe(H2O)4]n+ and oxobridging [Fe(H2O)5(μ-O)Fe·(H2O)5]n+ (n = 2, 4) cations in the hydrolysis products of cations [Fe(H2O)6]m+ (m = 2, 3) [104]. The hydroxo-bridged Fe-(OH)2-Fe dimers are the structure units in the polymetric hydroxo complex, which are dependent on pH and aging time [105, 106]. Molecular dynamics simulation further demonstrated the presence of aqueous di-iron or poly-irons, in which the Fe-Fe distance is 3.0–3.5 Å, with bonds by oxo-bridge or hydroxo-bridge [107]. Meanwhile, the (hydr)oxo-bridged Fe-Fe structure has been confirmed by experiments in the interface of iron oxide (IO, solid) to water [108, 109, 110, 111]. The μ-oxo iron ion have been identified in-situ in the high concentrated inorganic iron solution (e.g., 0.1 M Fe(NO3)3 [101], and 0.1 M FeCl3 [112]. The solubility of IOs further indicates that the critical ferrihydrite nucleus with an equivalent diameter of ∼15 Å and containing only ∼30 Fe atoms is stable in aqueous solution [113]. The 10-angstrom discrete iron-oxo cluster (known as the Keggin ion, Fe13) is also soluble [114], as a constitute structure of ferrihydrite nanoparticles [102]. Consequently, iron oxide nanoparticles with 3.5 Å oxo-Fe bindings (e.g., doubly shared iron octahedra) such as ferrihydrite, goethite, hematite, magnetite, and even green rust (fougerite) can be presented in the natural environment (Figure 8b) [115, 116, 117, 118, 119, 120, 121]. Therefore, it is reasonable to suggest that the oxo bridged Fe-Fe structure in the aqueous IO nanoparticles contribute to the catalysis of phosphate ester hydrolysis [28]. This compares to the activity of the aged nanomolar inorganic iron ion solutions [26, 27] and mimics of the artificial phosphatases [19, 97, 98]. The common feature between these IO nanoparticles, either from the DMT-IO or the aged inorganic iron ion solutions, as well as the natural or synthesized biomimetic phosphoesterase, constitute a kind of acceleration of electron transfer rate in the structure of the μ-(hydr)oxo ligand between the metals, particularly iron [19, 26, 27, 28, 92, 94, 122, 123]. In other words, the hydrolysis of phosphate ester is entirely dependent on its catalysis on this special Fe-oxo-Fe structure [27, 28]. Experiments and chemical models have also demonstrated that temperature impacts the stability of the aqueous poly-iron formation [124] and the nanostructure of IO in the solution [117, 125], which can explain the thermal denaturation behavior of the inorganic phosphatase (Figure 6). The Fe-Fe structure in the nanoparticles due to the nanosize-induced phase transformation and changes in the IO nanoparticle solution with the dissolved CO2 [126] further supported the response of the inorganic phosphatase at different pH (Figure 7).
Similar to phosphatases, the active metal centers of most peroxidase and catalases in nature also comprise the transition metals, for example, horseradish peroxidase, HRP [127], heme catalases [128], uroerythrin [129] with Fe, manganese peroxidase [130], manganese catalases [131, 132] with Mn or haloperoxidases [133] with V, all exhibit the oxo ligand structure. This unique structure might be also accountable for the “intrinsic peroxidase or catalases” from different inorganic metal oxides nanoparticles [44, 48, 49, 51, 53, 54, 58, 59, 60, 61, 134, 135]. It was noted that some PAPs were also reported to have activity of peroxidases [136, 137]. The Km in Table 3, which denotes the affinities of the phosphate ester to catalysis, are significantly (up to three orders of magnitude) lower than that of natural PAPs [33, 66, 69, 91, 138, 139]. The same patterns were also observed for these inorganic peroxidases compared to its corresponding HRP [28]. This finding further indicates that the IO nanoparticles are either much more sensitive to the low concentration of phosphate ester or H2O2 in the environment, or they have a much higher affinity for phosphate esters or H2O2 compared to the natural enzymes, although the maximum velocity of the hydrolysis was relatively low with these IO nanoparticles, especially for high phosphate ester or H2O2 concentrations in the environment. Like the nanoparticles of IO and vanadium pentoxide, the intrinsic sulfite oxidase activity of molybdenum trioxide nanoparticles is also due to the oxo ligand of Mo, as revealed in the metal center of sulfite oxidase [62, 140, 141]. Essentially, the catalytic activities depend to some degree on the surface area of these nanoparticles, but not just merely on particle size [48, 51, 52, 134, 142, 143]. The in situ Raman spectroscopy on the changes of V-oxo (V=O) bond in the different V2O5 nanomaterials during H2O2 catalysis cycle further demonstrated that the catalytic characteristics in these nanoparticles is directly related to the metal structure in the nanoparticle surface [61], which supports the concept of inorganic enzyme [27, 28].
Several recently studies from Europe have suggested that iron-rich nanoparticles (<20 nm) are the main carriers of phosphorus in forest streams and soil solution [10, 11, 144, 145] and monoesters are the main composition of dissolved organic phosphorus in soil and water [10, 15, 16, 18]. This further imply that iron oxide nanoparticles might play a significantly role for the organic phosphorus transformation from the view of phosphorus biogeochemistry, although sorption and precipitation is still the dominant view of the current soil and environmental science on the interaction of iron oxides and dissolved organic phosphorus in soil and sediment [21, 146, 147, 148, 149]. A couple of studies still noticed that orthophosphate can be released during the processing of the interactions [5, 20, 21, 22, 23, 24, 25]. As iron oxide nanoparticles are very common and widely exist in the soil, sediment, dust, and water [125, 150, 151, 152, 153], such enzyme-like catalytic propensities on phosphate esters in the current earth environment may provide an undiscovered feedback of organic phosphorus and play a critical role in the phosphorus cycles.
On the other hand, many effects have been made to improve inorganic nanozyme, both its catalysis capacity and substrate specificity, particularly for the “engineering peroxidase” related to iron oxide for its analytical, biomedical, and environmental applications from the view of nanoengineering [46, 47, 154, 155]. Various polymers or other organic compounds, e.g., porphyrin rings, the backbones of short peptides, amino acids, and even DNA, have been employed in the stabilization of the oxo bridged Fe-metal center in different iron oxides [156, 157, 158, 159, 160]. Similar effects should be made for the inorganic phosphatase as well. These “engineering phosphatase” can be employed for environmental monitors after standardization to assess the availability of dissolved organic phosphorus in waters and its potential risk for water eutrophication due to its higher stability and lower cost than protein enzymes, supported by the fact that natural phosphatase has been used for the tool to assess water or soil phosphorus availability [161, 162, 163, 164]. Another possibility for industry is to use these high efficiencies engineered phosphatase to release the orthophosphate from the wastewater directly for agriculture.
Laboratory experiments on the hydrolysis of phosphate ester in water demonstrated that inorganic phosphoesterase-like activity, using various inorganic iron oxide nanoparticles, significantly promotes the hydrolysis of phosphate ester, including G6P, PPi, and ATP. These findings and the fact that this and other inorganic nanoparticles can act effectively as enzymes: for example, iron oxide as peroxidase, vanadium pentoxide as bromoperoxidase, and molybdenum trioxide nanoparticles as sulfite oxidase; further support the concept of inorganic enzymes. The catalytic property of these nanoparticles is likely due to the structure of the metal oxides or metal bonds in the oxides and not merely to the nanoparticle surfaces. As iron oxide nanoparticles are very common and widely exist in the soil, sediment, and water, such enzyme-like catalytic propensities on phosphate esters, the main composition of dissolved organic phosphorus, in the current earth environment may play a critical role in the phosphorus cycles.
This work is dedicated to my beloved parents (Dr. Jing-Xiong Ji and late Dr. Shi-Xiong Huang) and my family (Wei Sun and Jack Jixiang Huang) for their love, endless support, encouragement & sacrifices. X.L.H. greatly appreciates the precious comments from the late Dr. R.J.P. Williams in the past years, and the kindly permissions to use the structure of iron oxide (Figure 8b) from Dr. Jean Pierre Jolivet as well as the personal encouragements from Drs. Robert Atlas, Gerhard Schenk, Michael J. Russell, Jia-Zhong Zhang, Raghuraman Venkatapathy and Peter B. Ortner. The experiment part of this work was initially conducted by X.L H from 2007 to 2008 at the AOML, NOAA, supported by the National Oceanic and Atmospheric Administration’s (NOAA) Coastal Ocean Program and Climate and Global Change Program. The research was carried out, in part, under the auspices of the Cooperative Institute of Marine and Atmospheric Studies (CIMAS), a joint institute of the University of Miami and NOAA, cooperative agreement #NA67RJ0149. The statements, findings, conclusions, and recommendations are those of the author and do not necessarily reflect the views of CIMAS, NOAA or the U.S. Department of Commerce.
The author declares no competing financial interest.
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Written By
Xiao-Lan Huang
Submitted: 21 May 2018Reviewed: 21 November 2018Published: 10 July 2019
Open access peer-reviewed chapter
