Photocatalytic reversible amination of α-keto acids on a ZnS surface: Implications for the prebiotic metabolism

Article abstract of DOI:10.1039/c2cc15665b

We report the enzyme-like reversible amination of four intermediates pertinent to the reductive tricarboxylic acid cycle on a photo-irradiated surface of mineral sphalerite (ZnS). Given its prevalence in the waters of early Earth, we suggest that the mineral-based photochemistry might have catalyzed the homeostasis of prebiotic metabolic systems.

Full text of DOI:10.1039/c2cc15665b

View Article Online / Journal Homepage / Table of Contents for this issue
Evaluation Only. Created with Aspose.PDF. Copyright 2002-2021 Aspose Pty Ltd.
Dynamic Article Links
ChemComm
Cite this: Chem. Commun., 2012, 48, 2146–2148
www.rsc.org/chemcomm
COMMUNICATION
Photocatalytic reversible amination of a-keto acids on a ZnS surface:
implications for the prebiotic metabolismw
Wei Wang,*a Qiliang Li,b Bin Yang,a Xiaoyang Liu,b Yanqiang Yanga and Wenhui Sua
Received 13th September 2011, Accepted 12th December 2011
DOI: 10.1039/c2cc15665b
We report the enzyme-like reversible amination of four inter-
mediates pertinent to the reductive tricarboxylic acid cycle on a
photo-irradiated surface of mineral sphalerite (ZnS). Given its
prevalence in the waters of early Earth, we suggest that the
mineral-based photochemistry might have catalyzed the homeostasis
of prebiotic metabolic systems.
Redox homeostasis is a set of enzyme-assisted metabolic reactions
that happen in living organisms to maintain life. How such
equilibrium systems could have evolved and functioned before
the emergence of enzymatic networks remains a critically
important challenge in the context of the origins of life. An
intriguing scenario claimed that the outgrowth of the primordial
metabolism may be postulated as a continuum from Earth’s
geochemical processes to chemoautotrophic biochemical procedures
on a sulfide mineral surface.1–7 It makes sense and rapidly
gained ground partly because in all extant life forms transition
metal sulfide cluster complexes play a crucial role in certain
enzymes.8–10 In order to reconstruct the possible outline, some
surface reactions in aqueous metal sulfide systems have been
developed to mimic basic biochemical steps, and many interesting
results have been achieved. However, the previous studies have
mainly focused on the fixation of gas molecules,11–13 the reduction
of metabolic intermediates,5,6 and the extension of molecular
chains.5,14–16 Up to now, little attention has been paid to the
archaic redox homeostasis.7
Scheme 1 The reversible amination of a-keto acids on a photo-
irradiated ZnS semiconductor particle.
shorter than 344 nm to trigger prebiotic redox reactions via the
interaction of an adsorbate with a conduction band (CB)
photoelectron (eÀ) or a valence band (VB) hole (h+, Scheme 1).
For example, the reductive tricarboxylic acid (rTCA) cycle,
which is employed by a number of extant chemoautotrophs
for carbon fixation, has been suggested to be the central part
of the primordial metabolism.20,21 Through a series of photo-
driven reactions, not only can ZnS play a role in abiotic
anaplerosis and replenish the rTCA cycle using CO2 as the initial
inorganic material, but also drive the cycle forward (Scheme 2).
Once a steady matter flow enters into the rTCA cycle, it
is equally important to remove the anions to avoid their
accumulation.22 An archetypical pathway for this so-called
cataplerotic metabolism in extant organisms is the reductive
amination of a-ketoglutarate (a-KG, 1d) catalyzed by glutamate
dehydrogenase (GDH) (Scheme 2),23
Herein we describe a model for the prebiotic redox chemistry,
i.e., the photocatalyzed reversible amination of a-keto acids on
ZnS particles. The mineral sphalerite (ZnS) is a common semi-
conductor and is believed to have been a typical constituent of
shallow-water hot springs on early Earth, within reach of solar
light.17,18 Previous research on ancient rocks demonstrated that
there was negligible oxygen and resulting ozone in the primordial
atmosphere.19 So the solar light reaching Earth contained a
UV component that was several orders of magnitude stronger
than it is today.17 ZnS can adsorb the UV light with a wavelength
NH3 + a-ketoglutarate + NAD(P)H + H+
2 glutamate + NAD(P)+ + H2O
(1)
This is a reversible process of homeostasis. The back reaction
can utilize external glutamate (3d) to produce the intermediate
a-KG for the rTCA cycle and make the pathway homeostatic.
The aim of this work is to simulate such an enzyme-assisted
process on a photo-irradiated ZnS surface. ZnS colloidal
suspensions were in situ prepared in a quartz conical flask by
mixing O2-free Na2S and ZnSO4 solutions. For the reductive
amination experiments, one mmol a-KG and 100 mmol
NH4Cl were added. Na2SO3 was used as the hole scavenger
when required. The pH value was adjusted to 9 since the seepage
water from sulfide minerals was suggested to be ultramafic.1,24
a CCMST, Academy of Fundamental and Interdisciplinary Sciences,
Harbin Institute of Technology, Harbin 150080, China.
E-mail: wwang_ol@hit.edu.cn; Fax: +86 451-86418440;
Tel: +86 451-86418430
b State Key Lab of Inorganic Synthesis and Preparative Chemistry,
College of Chemistry, Jilin University, Changchun 130012, China
w Electronic supplementary information (ESI) available: XRD, SEM,
SSA, and experimental details. See DOI: 10.1039/c2cc15665b
c
2146 Chem. Commun., 2012, 48, 2146–2148
This journal is The Royal Society of Chemistry 2012

Evaluation Only. Created with Aspose.PDF. Copyright 2002-2021 Aspose Pty Ltd.
View Article Online
then heat-treated under a nitrogen atmosphere at different
temperatures. It was found that the calcination process significantly
improved the catalytic efficiency of ZnS. In the presence of
Na2SO3, the maximum yield of glutamate was observed for a
catalyst heated at 100 1C (runs 5–8). It is more than 2.5 times
that formed by the in situ precipitated ZnS (run 5 vs. run 2).
This difference in efficiencies may be due to the improved
crystallinity of the calcined ZnS with fewer crystal defects
(Fig. S3, ESIw), but is not a result of the difference in specific
surface area (Table S1, ESIw). Such an improvement decreases
the possibility of photoelectron–hole recombination, thereby
leading to higher catalytic activity. This explanation can be
more unequivocally conformed by the controls in the absence
of a hole scavenger. Without the use of Na2SO3, the yield of
glutamate catalyzed by calcined ZnS (run 9) was almost eight
times higher than that formed by in situ precipitated ZnS
(run 1). The control in the absence of irradiation again
demonstrated that heterogeneous photochemistry was the reaction
mechanism (run 10). That the activities of ZnS samples were
reduced with the further enhancement of treated temperature may
be due to their surface alteration at higher temperatures (>300 1C)
(Fig. S4, ESIw).
Alpha-KG is one cataplerotic exit point out of the rTCA
cycle (Scheme 2). In biochemistry, this tunnel is not one-way
but bidirectional to guarantee the homeostasis of metabolic
intermediates. In other words, a-KG, as the deamination
product of external glutamate, may revisit the cycle through
the reverse pathway. ZnS can catalyze such an anaplerotic
reaction (Fig. S5d, ESIw). A summary of the results is presented
in the lower moiety of Table 1. Thermal treatment remarkably
raised the deamination efficiency of glutamate by ZnS (runs
11 and 12), just as it has behaved in the amination reaction.
Unlike the reduction process, however, the oxidative deamination
reaction occurred at the hole sites on the surface of ZnS particles
(Scheme 1). The presence of Na2SO3 entirely inhibited the
formation of a-KG (run 13), since it forcefully competed with
glutamate to be oxidized by the hole. The complete set of control
experiments implies that the oxidation of glutamate is driven by
the ZnS-assisted photochemical reaction.
Scheme 2 The rTCA cycle (thin solid line) coupled to its anaplerotic
reactions (dashed line). The simulated reversible amination of keto
acids in this study (thick solid line) may balance the entry and exit to
the antique cycle and contribute to the prebiotic redox homeostasis.
Photocatalytic reactions were carried out under an argon
atmosphere by using a 500 W mercury–xenon lamp (see details
in Fig. S1, ESIw). The results are presented in Table 1 and
Fig. S2 (ESIw). It can be found that only 0.5% glutamate was
formed within 4 h (run 1) when no Na2SO3 was added, while in
the presence of the sacrificial agent, the yield was enhanced by
nearly six times (run 2). In the control runs without exposure
to irradiation (run 3) or in the absence of ZnS (run 4), no trace
of glutamate was found. Therefore, it can be concluded that
the photoelectron transfer from a ZnS surface to Schiff base
intermediate 2d was the mechanism for the formation of
glutamate (Scheme 1).
In hot springs water is always overheated, reaching a
maximum value of about 350 1C.17 We therefore examined
the influence of thermal treatment on the photocatalytic
activity of ZnS. The fresh ZnS precipitates were filtered and
Table 1 Reversible amination of a-KG assisted by the electron
shuttle on a ZnS surface
b
Na2SO3 (0.2 mM)
Run
ZnSa (2 mmol)
hn
Yieldsc (%)
In further experiments, a set of other three reversible redox
steps pertaining to the rTCA cycle (Scheme 2) was evaluated,
i.e., the reductive amination of glyoxylate (1a), pyruvate (1b), and
oxaloacetate (1c), and the corresponding oxidative deamination of
glycine (3a), alanine (3b), and aspartate (3c) (Fig. S5–S8, ESIw).
In Fig. 1, the amount of each product formed during the
photoreaction is expressed as a function of irradiation time.
The time-dependent results of 1d and 3d are also represented.
A general trend is that the stoichiometric yields of the products
increased along with time, and subsequently reached a constant
level or decreased because of their further reactions. Special
note should be taken of the data that the main reaction
products from 1c and 3c were 3b and 1b but not 3c and 1c,
respectively. For the amination of 1c, the yields of 3c did not
increase above the detection limit and were up to 0.1% even
after a prolonged time (24 h) (Fig. S7, ESIw); while in the
deamination products of 3c, no trace of 1c was detected
(Fig. S5c, ESIw). A decarboxylation process of 1c to 1b is
unequivocally involved in both reactions25 and may help to
explain the unexpected results. However, this question still remains
Amination of a-KG (1 mmol)
Glu
1
2
3
4
5
6
7
8
9
10
ZnSis
ZnSis
ZnSis
À
+
+
À
0.5 (0.0)
2.9 (0.3)
udd
+
+
+
+
+
+
+
À
À
+
+
+
+
+
+
À
ud
ZnS100
ZnS200
ZnS300
ZnS400
ZnS100
ZnS100
7.4 (0.7)
6.8 (0.6)
0.6 (0.1)
1.5 (0.1)
3.8 (0.2)
ud
a-KG
2.8 (0.2)
18.3 (1.0)
ud
+
Deamination of Glu (1 mmol)
11
12
13
14
15
ZnSis
ZnS100
ZnS100
ZnS100
—
À
À
+
À
À
+
+
+
À
ud
ud
+
a
For the subscripts of ZnS, please refer to the experimental section.
‘‘+’’ and ‘‘À’’ indicate the presence or absence of a species,
b
c
respectively. Each value is the average of three independent repeat
experiments; numbers in parentheses are standard deviations of the
d
mean. Reaction conditions: pH 9, 30 1C, 4 h. Undetectable.
c
This journal is The Royal Society of Chemistry 2012
Chem. Commun., 2012, 48, 2146–2148 2147

Evaluation Only. Created with Aspose.PDF. Copyright 2002-2021 Aspose Pty Ltd.
View Article Online
balance the entry and exit of rTCA cycle metabolites (Scheme 2).
The equilibrium point is controlled by the concentration of the
hole scavenger. This scenario envisages a primary role of
mineral-driven catalysis for the archaic redox homeostasis.
Taken together with the results in previous studies,5,6 the
minerals in the submarine hydrothermal systems make the
whole homeostasis possible by modulating a series of cascading
reactions (Scheme 2). Later on in the evolutionary context, the
enzyme-like chemistry of the minerals was replaced by extant
enzymatic networks.1
Given its activity in both reductive amination and oxidative
deamination, the ZnS-based model presented in this study implies
that it may also perform a similar function to that of transaminase.
Work along this line is in progress in this laboratory.
This work is financially supported by NSFC (40902014),
CPSF (20080430918), and HIT.NSRIF (200811).
Notes and references
1 M. J. Russell and A. J. Hall, J. Geol. Soc., 1997, 154, 377–402.
2 R. M. Hazen, Sci. Am., 2001, 284, 76–85.
3 W. Martin and M. J. Russell, Philos. Trans. R. Soc., B, 2003, 358,
59–83.
4 M. J. Russell and W. Martin, Trends Biochem. Sci., 2004, 29,
358–363.
5 X. V. Zhang and S. T. Martin, J. Am. Chem. Soc., 2006, 128,
16032–16033.
Fig. 1 Main reaction products from the reductive amination of 1a–1d
(a) and the deamination of 3a–3d (b) on ZnS100 surface vs. the
irradiated time. Uncertainties are shown by using error bars. For the
experimental conditions please refer to runs 5 and 12 in Table 1,
respectively.
6 G. Wachtershauser, Chem. Biodiversity, 2007, 4, 584–602.
7 W. Wang, B. Yang, Y. Qu, X. Liu and W. Su, Astrobiology, 2011,
11, 471–476.
¨
¨
8 H. Beinert, R. H. Holm and E. Munck, Science, 1997, 277,
653–659.
¨
9 A. Y. Mulkidjanian and M. Y. Galperin, Biol. Direct, 2009, 4, 27.
10 C. L. Dupont, A. Butcher, R. E. Valas, P. E. Bourne and
´
C. Caetano-Anolles, Proc. Natl. Acad. Sci. U. S. A., 2010, 107,
10567–10572.
11 B. R. Eggins, P. K. Robertson, J. H. Stewart and E. Woods, Chem.
Commun., 1993, 349–350.
12 J. A. Brandes, N. Z. Boctor, G. D. Cody, B. A. Cooper,
R. M. Hazen and H. S. Yoder Jr., Nature, 1998, 395, 365–367.
¨ ¨
13 M. Dorr, J. Kabbohrer, R. Grunert, G. Kreisel, W. A. Brand,
R. A. Werner, H. Geilmann, C. Apfel, C. Robl and W. Weigand,
to be specified. Another challenge is to explicate the differences
in the reaction efficiencies of different reactants. A possible
explanation is that the higher the nonpolarity, the more
accessible the reactants are to the hydrophobic surface of
ZnS and then the more available to participate in the photo-
chemical reaction. As a result of the differences in the side
chain groups, the nonpolarity of the reactants seems to follow
the trend 1b/3b > 1d/3d > 1a/3a > 1c/3c.
Angew. Chem., Int. Ed., 2003, 42, 1540–1543.
14 C. Huber and G. Wachtershauser, Science, 1997, 276, 245–247.
¨
¨
15 C. Huber and G. Wachtershauser, Science, 1998, 281, 670–672.
¨
¨
In summary, the simulated GDH-like chemistry (eqn (1))
demonstrates that the reversible amination of several a-keto
acid intermediates pertinent to the rTCA cycle can occur on
the photo-irradiated surface of mineral sphalerite. The yields
are not very high and studies upon reactivity changes of the
system as a function of a full range of experimental conditions
have not been investigated to determine the optimized yield.
However, since the presented experimental conditions were care-
fully designed to simulate the primeval hot spring environments as
closely as are presently known, the results can be related to how an
extant metabolic mechanism might have evolved on early Earth.
Not only do they provide a new pathway for the prebiotic synthesis
of amino acids, but also an abiotic archetype for the primeval
redox metabolism. The ZnS-photo-assisted redox chemistry could
16 M. I. Guzman and S. T. Martin, Chem. Commun., 2010, 46,
2265–2267.
17 A. Y. Mulkidjanian, Biol. Direct, 2009, 4, 26.
18 M. I. Guzman and S. T. Martin, Astrobiology, 2009, 9, 833–842.
19 L. R. Kump, Nature, 2008, 451, 277–278.
20 G. Wachtershauser, Proc. Natl. Acad. Sci. U. S. A., 1990, 87,
¨
200–204.
¨
21 H. J. Morowitz, J. D. Kostelnik, J. Yang and G. Cody, Proc. Natl.
Acad. Sci. U. S. A., 2000, 97, 7704–7708.
22 O. E. Owen, S. C. Kalhan and R. W. Hanson, J. Biol. Chem., 2002,
277, 30409–30412.
23 J. M. Berg, J. L. Tymoczko and L. Stryer, Biochemistry, W. H.
Freeman & Co., New York, 5th edn, 2002, Sec. 24.1.2.
24 W. Martin and M. J. Russell, Philos. Trans. R. Soc., B, 2007, 362,
1887–1925.
25 M. I. Guzman and S. T. Martin, Int. J. Astrobiol., 2008, 7,
271–278.
c
2148 Chem. Commun., 2012, 48, 2146–2148
This journal is The Royal Society of Chemistry 2012