SCIENCE ADVANCES | RESEARCH ARTICLE

GEOCHEMISTRY Copyright © 2018

The Authors, some

Geoelectrochemical CO production: Implications for rights reserved;

exclusive licensee
the autotrophic origin of life American Association
for the Advancement
of Science. No claim to
Norio Kitadai,1* Ryuhei Nakamura,1,2 Masahiro Yamamoto,3 Ken Takai,1,3 Yamei Li,2 original U.S. Government
Akira Yamaguchi,4 Alexis Gilbert,1,5 Yuichiro Ueno,1,5 Naohiro Yoshida,1,6 Yoshi Oono7 Works. Distributed
under a Creative
Wächtershäuser’s proposal of the autotrophic origin of life theory and subsequent laboratory demonstrations Commons Attribution
of relevant organic reactions have opened a new gate for the exploration of the origin of life. However, this scenario NonCommercial
remains controversial because, at present, it requires a high pressure of CO as a source of carbon and reducing License 4.0 (CC BY-NC).
energy, although CO must have been a trace C species on the Hadean Earth. We show that, simulating a geoelec-
trochemical environment in deep-sea hydrothermal fields, CO production with up to ~40% Faraday efficiency was
attainable on CdS in CO2-saturated NaCl solution at ≤–1 V (versus the standard hydrogen electrode). The threshold
potential is readily generated in the H2-rich, high-temperature, and alkaline hydrothermal vents that were probably
widespread on the early komatiitic and basaltic ocean crust. Thus, Wächtershäuser’s scenario starting from CO2 was
likely to be realized in the Hadean ocean hydrothermal systems.

INTRODUCTION A different mechanism of abiotic CO2 reduction in the early ocean

Since the first publication of Wächtershäuser’s theory of the autotrophic hydrothermal systems has been suggested (18–20), for which redox,
origin of life from primordial carbon fixation within a sulfide-rich hy- proton, and thermal gradients between the hydrothermal fluids and
drothermal vent (1, 2), a number of laboratory simulations for prebiotic seawater across the sulfide deposits provide a continuous supply of re-
organic synthesis have been performed within this scenario. Represent- ductive energy for inorganic carbon fixation. Using a sulfide chimney
ative examples were published in Science more than a decade ago by block obtained from a black smoker vent in the southern Lau Basin,
Huber and Wächtershäuser: Under mildly hot, anaerobic, and alkaline Nakamura et al. (18) observed a long-distance electric conduction across
aqueous conditions in the presence of metal sulfides (for example, FeS the rock [0.2 to 9.1 ohms cm–1 at 300 K; (21)] and its catalytic function
and NiS), they demonstrated the C–C bond formation that reminds us for redox reactions at the mineral-seawater interface. Yamamoto et al.

Downloaded from https://www.science.org on September 17, 2021

of the reductive acetyl–coenzyme A pathway (3), the reductive polym- (19) verified the electricity generation in the deep-sea hydrothermal
erization of HCN to a-hydroxy and a-amino acids (4), and the polym- environment using a fuel cell coupling the oxidation of hydrothermal
erization of a-amino acids to short peptides (5). Nevertheless, the H2S and the reduction of seawater O2 in an artificial hydrothermal vent.
significance of the autotrophic scenario has been questioned (6), be- In addition, the in situ electrochemical surveys of the Okinawa Trough
cause the proposed sulfide-pulled CO2 reduction has never been rea- hydrothermal fields (20) gave multiple lines of evidence for natural and
lized: Huber-Wächtershäuser’s organic syntheses required a high widespread electricity generation via sulfide deposits. These labora-
pressure of CO (1 bar or more) as a source of carbon and reducing en- tory and field investigations strongly suggest that geoelectrochemical
ergy. The CO concentrations in the atmosphere and volcanic emissions energy and reactive surfaces are ubiquitous in the present-day hydro-
on the Hadean Earth were likely to be trace (7) unless there was a huge thermal systems and were even more abundant and widespread across
supply of meteorite-derived reducing power (8) that would have inev- the early ocean floor.
itably destroyed the surface environment. Although Wächtershäuser Here, we present a laboratory demonstration of efficient electro-
maintained a life’s origin in a CO-rich volcanic environment in a later reduction of CO2 on metal sulfides and discuss its relevance to the auto-
addition to his theory (9), the setting is likely incompatible with the trophic scenario of the origin of life. We prepared low-crystalline sulfides
conditions crucial to the organic synthesis (3–5) because volcanic envi- of various metals (Ag, Cd, Co, Cu, Fe, Mn, Ni, Pb, or Zn) by mixing
ronments are inherently acidic to neutral (10). Russell and colleagues an alkaline solution of sodium sulfide and an acidic solution of the
(11–13) and, more recently, Lane and Martin (14, 15) have proposed corresponding metal chloride. This mixing-induced sulfide formation
an alternative theory that the primordial carbon assimilation took place likely occurred in the early alkaline hydrothermal vent environments
in the Hadean ocean alkaline hydrothermal systems through the direct and could comprise the main body of hydrothermal mineral deposits
coupling of seawater CO2 and hydrothermal H2 on metal sulfides, but as the geoelectrochemical reactors (13, 22). Notice that the following
no clear experimental support has yet been provided (16, 17). experiments considerably augment recent studies by our group (23) and
1
others (24), revealing the catalytic capability of some crystalline sul-
Earth-Life Science Institute, Tokyo Institute of Technology, 2-12-1 Ookayama, Meguro-ku, fides (for example, greigite). Here, we also studied molybdenum and
Tokyo 152-8550, Japan. 2Biofunctional Catalyst Research Team, RIKEN Center for
Sustainable Resource Science, 2-1 Hirosawa, Wako, Saitama 351-0198, Japan. tungsten sulfides (MoS2 and WS2) because of their importance in
3
Department of Subsurface Geobiological Analysis and Research, Japan Agency for microbial metabolic reactions (25–27).
Marine-Earth Science and Technology, 2-15 Natsushima-cho, Yokosuka 237-0061,
Japan. 4Department of Materials Science and Engineering, School of Materials and
Chemical Technology, Tokyo Institute of Technology, S7-9, 2-12-1 Ookayama, Meguro-ku,
Tokyo 152-8552, Japan. 5Department of Earth and Planetary Sciences, Tokyo Institute RESULTS
of Technology, 2-12-1 Ookayama, Meguro-ku, Tokyo 152-8551, Japan. 6Department of The CO2 electrolysis was conducted in an H-type electrochemical cell
Environmental Chemistry and Engineering, Tokyo Institute of Technology, 4259 Nagatsuta, that had two compartments separated by a proton exchange mem-
Midori-ku, Yokohama, Kanazawa 226-8503, Japan. 7Department of Physics, University
of Illinois at Urbana-Champaign, 1110 West Green Street, Urbana, IL 61801–3080, USA. brane, with a Ag/AgCl reference electrode and a carbon working elec-
*Corresponding author. Email: [email protected] trode placed at one side, and a Pt counter electrode at the other side

Kitadai et al., Sci. Adv. 2018; 4 : eaao7265 4 April 2018 1 of 7

SCIENCE ADVANCES | RESEARCH ARTICLE

(fig. S1). The metal sulfide–deposited carbon electrode was exposed to a controllable potential, which makes data interpretation difficult. The
constant potential for 24 hours in 100 mM NaCl saturated with 1 atm occurrence and combination of multiple reactions are likely to be
CO2 at room temperature (~25°C). Liquid-phase products were character- more realistic than single-pot reaction in natural hydrothermal vent
ized by high-performance liquid chromatography (HPLC) and proton environments. The complexity of the geochemical system could also
nuclear magnetic resonance (1H NMR) spectroscopy, and gas-phase allow the accumulation of organic compounds (29) that are gener-
products were characterized by gas chromatography (GC). Figure 1 shows ated under a continuous supply of CO by the sulfide-catalyzed CO2
the Faraday efficiencies (FEs) of CO2 reduction to CO (CO2 + 2H+ + electroreduction.
2e– → CO + H2O) and to formate (CO2 + H+ + 2e– → HCOO–) at –0.8,
–1.0, and –1.2 V [versus the standard hydrogen electrode (SHE)]. CO
and formate were the sole carbon products observed with the FE > DISCUSSION
0.1%, along with H2 that evolved from the competing proton reduction Were the experimental conditions examined above geologically and
(2H+ + 2e– → H2). The CO formation occurred effectively on CdS and geochemically feasible in the Hadean ocean hydrothermal systems?
Ag2S at –1.0 and –1.2 V (versus SHE), whereas negligible amounts of CO Our experiments revealed that CO production on metal sulfides occurs
were produced in other experimental conditions or in the absence of sul- at electric potentials below –0.8 V (versus SHE). In submarine hydro-
fide. Additional experiments with varied potential (Fig. 1C) revealed thermal vents, electrons are catalytically provided by the oxidation of
that CO was generated at an electric potential below –0.8 V (versus reductive chemicals at the fluid-mineral interface (20). If H2S is as-
SHE) on both sulfides. The FE shifted positively with decreasing po- sumed to be the sole electron source in the fluid, the potential is always
tential and attained around 40% on CdS and 30% on Ag2S at ≤–1.0 higher than the threshold (–0.8 V versus SHE) in a wide range of tem-
and ≤–1.1 V (versus SHE), respectively. For formate, active formation perature and pH (Fig. 2, A and B). However, if H2 is present at a con-
was observed only on CuS (FE ~4% at –1.0 and –1.2 V versus SHE; Fig. centration of 1 mmol kg–1 or higher (Fig. 2, C and D), H2 oxidation in
1B). These product characteristics were largely different from those on hot and alkaline pH conditions can provide the potential well below
the corresponding pure metals (28), indicating the significance of sulfur the desirable value [for example, –0.98 V (versus SHE) at 200°C and
to the surface-CO2-electron interactions. pH 12 in the presence of 1 mmol kg–1 H2]. The H2-enriched hydro-
To examine whether the electrochemically produced CO serves as a thermal fluid systems have been hypothesized to occur abundantly on
driving force for the subsequent abiotic organic synthesis, we collected the Hadean and early Archean ocean floor; two representative systems
the reductive gas generated on CdS at –1.0 V (versus SHE) that was are a komatiite-hosted high-temperature type at oceanic ridges and
primarily composed of CO (ca. 40%) and H2 (ca. 60%) (Fig. 1C), sealed plateaus (Fig. 3A) (30) and a low-temperature type hosted by koma-
it in a serum bottle containing a solution of simple carbon compounds tiite or peridotite at ridge flank regions (13). A recent hydrothermal

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(methanethiol, potassium cyanide, or glycine) and NiS, and incubated experiment of komatiite in CO2-saturated NaCl solution demon-
it in a similar manner as was reported by Huber and Wächtershäuser strated that high concentrations of CO2 suppress H2 generation dur-
(3–5) (see the Supplementary Materials). Our experiments largely re- ing low-temperature serpentinization (<250°C) owing to the
produced the original reports, although there were smaller yields with formation of Fe2+-bearing dolomite, whereas the high-temperature
fewer varieties of products owing to the lower initial CO concentra- serpentinization (>300°C) can generate extraordinarily high concen-
tion (fig. S2). We did not carry out a “one-pot” organic synthesis in an trations of H2 even with CO2-saturated seawater (31). Under such
electrochemical cell because dissolved neutral species inevitably pen- high-temperature conditions, the dehydration of epidote to anorthite
etrate into the counter electrode side and undergo oxidation at un- followed by the precipitation of calcite controls the pH and makes it

50 50

40
A C
30 40 Ag2S
CdS
20
Faraday efficiency (%)

Faraday efficiency (%)

–0.8 V (vs. SHE)

–1.0 V (vs. SHE)
10 –1.2 V (vs. SHE)
30

4
B 20

2 10

0 0
Ag2S CdS CoS CuS FeS MnS MoS2 NiS PbS WS2 ZnS –1.2 –1.1 –1.0 –0.9 –0.8 –0.7 –0.6
Potential (vs. SHE)
Fig. 1. Electrochemical CO2 reduction on various metal sulfides in 0.1 M NaCl saturated with 1 atm CO2 at room temperature (~25°C). (A and B) FEs for CO2
reduction to (A) CO (CO2 + 2H+ + 2e– → CO + H2O) and (B) HCOO– (CO2 + 2H+ + 2e– → HCOO–) at –0.8, –1.0, and –1.2 V versus the SHE. (C) CO production efficiencies
on CdS and Ag2S as a function of electric potential. Error bars correspond to the overall reproducibility of the experimental data that was evaluated from three
independent experiments.

Kitadai et al., Sci. Adv. 2018; 4 : eaao7265 4 April 2018 2 of 7

SCIENCE ADVANCES | RESEARCH ARTICLE

0.2 highly alkaline (pH ≥12), which has been demonstrated by a hydro-
A B C D thermal alteration experiment of basalt in CO2-rich seawater (32). It
0 seems likely that alkaline hydrothermal systems were widespread
across the early ocean crust and floor that were dominated by basalt
Potential (vs. SHE)

–0.2 and/or komatiite (33). Meanwhile, the early basalt-hosted hydro-

thermal systems with CO2-rich seawater may have also generated
–0.4
a variety of hydrothermal fluids with different H2 concentrations
and pH values. With a total large surface area of basalt-seawater
–0.6
reaction in the hydrothermal circulation from recharge to discharge,
–0.8
the seawater CO2 would be quickly removed, and the CO2-depleted
25ºC water/rock reaction could generate acidic to neutral, metal-rich
–1.0
100ºC (and occasionally H2-rich) black smoker fluids as observed today
200ºC
300ºC (Fig. 3B) (32).
–1.2 Metals from the present-day black smoker vents have been ob-
2 4 6 8 10 12 2 4 6 8 10 12 2 4 6 8 10 12 2 4 6 8 10 12
pH served to emanate over thousands-of-kilometers scale across hydro-
thermal plumes under soluble and/or colloidal forms with a limited
Fig. 2. Thermodynamically predicted electric potentials of fluids from deep-
vertical diffusion (34). Wider and denser metal distributions in the
sea hydrothermal systems. Redox potentials of (A) H2S (1 mmol kg–1), (B) H2S
(10 mmol kg–1), (C) H2 (1 mmol kg–1), and (D) H2 (10 mmol kg–1) as a function of pH at
early deep ocean are envisioned (35) because of the anaerobic, Fe-
25°, 100°, 200°, and 300°C calculated assuming the half reactions of S + 2H+ (or H+) + rich, and slightly acidic character of ancient seawater (36, 37) with much
2e– → H2S (or HS–) [for (A) and (B)] and 2H+ + 2e– → H2 [for (C) and (D)]. S (solid sulfur) greater global thermal convection than the present level (38). Cd2+ is a
was chosen as the H2S (or HS–) oxidation product because the H2S/S redox couple trace but ubiquitous hydrothermal dissolved metal ion (39) and has a
provides a major potential control on the sulfide-rich hydrothermal vent environments very poor solubility in alkaline sulfide conditions (40). Therefore, Cd2+
(19). See the Supplementary Materials for the calculation procedure. and CdS dispersed from the early basalt-hosted hydrothermal systems

B Metal-rich, high-T, H2-rich, high-T, C Alkaline Porous chimney wall Slightly acidic
acidic HS alkaline HS hydrothermal seawater
2+
Ni Cd2+ fluid CO
Cd2+ H2 O CO
pH >10 CO2

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Fe2+ Ag+
Fe2+ Metal-rich, + N -
T >300oC 3
HN O
high-T, Eh <–0.8 V O e– CO2
acidic HS H2S COS CO
CO2 H2 O
CO2 H2S Cd2+
2H+ +
HN
H2 H2S e– 3
O
- O e– CO2
H 2S H 2S H2 HO -
CO2 O
H2
CO2 Oceanic CN– Fe2+
crust 2H+ e–
Komatiite
H2 H2 CO CO
SH Ni2+
and basaltic
magma 0
H2
O O
e– CO2
S
Mantle CO CO
H2S e– O
-
S O
-

e– CO2

Fig. 3. Abiotic carbon fixation in the primitive hydrothermal system. (A) The hot and active mantle convection in the primitive Earth induced a lot of massive upwelling
of komatiite/basaltic melts beneath the ocean floor (30), (B) where interactions between the solidified (ultra)mafic rocks and the CO2-rich seawater with different water/rock
ratios led to a variety of end-member fluid chemistry, including the H2-rich, high-temperature (T), and alkaline type and the metal-rich, high-temperature, and acidic (or neutral)
ones (31, 32). (C) On the ocean floor, mixing of the hydrothermal fluids and seawater generated sulfide-rich chimneys (22), and the potential gradient across the chimney drove
a continuous electron flow. The electric potential at the chimney-seawater interface could reach less than –1 V (versus SHE) in alkaline hydrothermal vent environments. The
low potential, in the presence of sulfides rich in Cd2+ and Ag+, allowed the electrochemical CO2 reduction to CO with the FE as high as dozens of percent, together with H2
evolution. The produced CO served as a driving force for the subsequent abiotic organic synthesis that preceded the origin of life as schematically indicated in the figure.

Kitadai et al., Sci. Adv. 2018; 4 : eaao7265 4 April 2018 3 of 7

SCIENCE ADVANCES | RESEARCH ARTICLE

would have precipitated and incorporated in the sulfide deposits in have favored the production of reactive C1 compounds from natu-
the closely localized alkaline hydrothermal vent environments. rally ubiquitous carbon, nitrogen, and sulfur sources (for example,
There is no definitive constraint on the dissolved sulfide flux from CO2, N2O, and SO2) under naturally feasible conditions.
the early ocean alkaline hydrothermal vents. If the fluid sulfide con-
centrations were within or lower than the micromolal level, the fluid-
seawater mixing is expected to precipitate Cd, Zn, and Cu selectively MATERIALS AND METHODS
against Ni, Co, and Mn owing to their difference in sulfide solubil- Preparation of metal sulfides
ity (40). FeS precipitation would not have occurred even when a All metal sulfides except for WS2 and MoS2 were prepared by a drop-
high seawater Fe2+ level (50 mmol kg–1) had been attained (40). In wise addition of 100 mM Na2S(aq) [or 50 mM Na2S(aq) for the case of
the present-day and Paleozoic hydrothermal sulfide deposits, Cd is Ag2S] into a 100 mM aqueous solution of the corresponding metal chlo-
observed primarily as an isomorphous impurity in sphalerite (ZnS), ride (AgCl, CdCl2, CoCl2, CuCl2, FeCl2, MnCl2, NiCl2, PbCl2, or ZnCl2)
rather than a single CdS crystal, with the Cd/Zn substitution ratio of under vigorous stirring with a final volume ratio of 1:1. The valence
up to 13.2 weight % (41, 42). The Cd/Zn ratio tends to increase at higher states of metals are all stable under the estimated Hadean ocean redox
precipitation temperature and lower concentrations of dissolved sul- condition [0.432 V (versus SHE)] (56). Solid precipitates were then sep-
fide and chloride (43, 44); hence, hot and alkaline hydrothermal systems arated from the supernatant by centrifugation and were dried under
could favor the formation of Cd-enriched ZnS. Naturally generated vacuum. To prevent oxidation by atmospheric O2, the sample prepara-
multiple metal-sulfide precipitates in some cases exhibit higher cat- tion was conducted in a globe box filled with N2 gas (>99.9999%), with
alytic efficiencies for the electroreduction of CO2 than the individual 4% H2 being added (the COY system). In many cases, the synthesized
sulfides (23). Thus, some of the hydrothermal sulfide deposits of the sulfides showed broad x-ray diffraction signals, with low intensity
H2-rich, high-temperature, and alkaline hydrothermal systems that indicating low crystallinity (fig. S3). All chemicals were purchased from
were probably widespread in the early komatiitic and basaltic ocean Wako as reagent grade. Deaerated Milli-Q water (18.2 megohms) was
floor (Fig. 3, A and B) are considered to provide favorable conditions used as the solvent. WS2 and MoS2 were obtained from Sigma-Aldrich
for electrochemical CO production. This environmental situation is (99%, ~90 nm) and were used without further purification.
fully consistent with that assumed in Wächtershäuser’s abiotic or-
ganic synthesis (Fig. 3C) (3–5). Therefore, this study provides the Electrochemical experiments
first experimental evidence that the presence of the key player in Figure S1 schematically illustrates the electrochemical cell. For each
Wächtershäuser’s scenario for the autotrophic origin of life, CO, was experiment, about 50 mg of metal sulfide catalyst was deposited on
possible under a geologically and geochemically plausible setting on the carbon working electrode (5.7 cm2), deaerated 100 mM NaCl(aq)

Downloaded from https://www.science.org on September 17, 2021

the primitive Earth. was poured into the cell (60 ml to the working electrode side and 10 ml
The geoelectrochemical CO production demonstrated in this study to the opposite side), and pure CO2 gas (>99.995%) was allowed to
could also enhance the theory for the origin of membrane bioener- flow (20 ml min–1) into the solution for at least 1 hour before each ex-
getics (14). A number of microorganisms, in both archaea and bacteria, periment. While keeping the CO2 flowing, a constant potential was
are known to use CO and formate as energy and carbon sources (45, 46). applied on the carbon electrode by using a multi-potentiostat (PS-08;
With the redox potential of a CO/CO2 pair (E0 = –520 mV), which is Toho Technical Research). CO2 buffered the solution slightly acidic
even lower than that for H2/H+ (E0 = –414 mV), CO can solely reduce (pH = 5.75 ± 0.25) during the electrolysis. All potentials were mea-
ferredoxin (E0 = –400 mV) and generates a larger quantity of adenosine sured against an Ag/AgCl reference electrode in saturated KCl and
triphosphate (ATP) in the course of the autotrophic carbon assimilation converted to the SHE scale using the following equation
than the H2/CO2 pair does (46). The energetic advantage of the CO
metabolism would have brought an extra benefit for the origin and early E ðvs: SHEÞ ¼ E ðvs: Ag=AgClÞ þ 0:198 V ð1Þ
evolution of chemolithotrophic systems in the early ocean hydro-
thermal vent environments. After 24 hours of duration, the sample solution was filtered with a
At least two issues remain to be addressed: Why only Ag and Cd polytetrafluoroethylene (PTFE) membrane filter (pore size, 0.22 mm)
sulfides can effectively reduce CO2 to CO, and whether methanethiol and was analyzed by HPLC and 1H NMR spectroscopy. The gas-
and cyanide were really available. Ag2S and CdS are characterized by phase product was collected in a polypropylene gas trap immersed
a relatively high energy conduction band edge (47) and by a relatively in the solution and was analyzed by GC. The gas sampling was
weak metal-S bond strength (48) among the sulfides examined in this carried out for a certain fixed period (note that the sampling period
study. The former property likely facilitates electron transfer from was varied depending on the activity of the reductive gas generation),
the charged surface to the adsorbed oxidants (H2O and CO2) (49). for which bubbles generated on the metal sulfides were accumulated
The latter energetically favors the C–S bond formation through re- into the gas trap while intrusion of the flowed CO2 was carefully
connecting the metal-S bond, facilitating the CO2 conversion to CO avoided. The gas products collected after various durations of the
by stabilization of the reaction intermediate (50). Although these ad- electrochemical experiment showed mutually similar compositional
vantages qualitatively explain the high CO productivities of CdS and characteristics over the first 24 hours (within the overall reproduci-
Ag2S (Fig. 1), a definitive understanding of our results requires bility; ±10%). The FE was calculated from the following equations
detailed structural and electronic study of adsorbed species. The
availability of methanethiol and cyanide anion remains controversial charge required for the production
(51, 52), although several mechanisms have been proposed for their FE ¼ ð2Þ
abiotic formation in hydrothermal systems (53, 54). Because electro- total charge built up for the first 24 hours
chemistry is a frequently used process to synthesize organic compounds
with C–N and C–S bonds (55), the geoelectrochemical settings could for the liquid-phase products, and

Kitadai et al., Sci. Adv. 2018; 4 : eaao7265 4 April 2018 4 of 7

SCIENCE ADVANCES | RESEARCH ARTICLE

charge required for the production column (Shinwa). He (>99.99995%) was used as the carrier gas at a
FE ¼ ð3Þ flow rate of 24 ml min–1. The column temperature was initially kept at
total charge built up during the sample collection
40°C for 6 min, raised to 200°C at a rate of 20°C min–1, kept for 6 min,
raised to 250°C at a rate of 50°C min–1, and then kept for 20 min. H2,
for the gas-phase products. CO, CH4, CO2, C2H6, and C3H8 were observed with the retention times
of ca. 2.1, 5.0, 8.8, 11.8, 16.7, and 28.0 min, respectively. A pulsed dis-
Organic synthesis experiments charge detector was used to quantify the concentrations of CO, CH4,
Three types of organic synthesis experiments were conducted according C2H6, and C3H8, and a thermal conductivity detector for the H2 concen-
to the methods reported by Huber and Wächtershäuser (3–5), with tration. Some gas samples were also analyzed by a gas chromatog-
the electrochemically generated reductive gas on CdS at –1 V (versus raph mass spectrometer (GCMS-QP2020; Shimazu) equipped with
SHE) replacing pure CO gas. MICROPACKED-ST column (Shinwa). Results obtained by the differ-
(i) NiSO4 ⋅ 6H2O (131 mg, 0.5 mmol) was deaerated in a serum bot- ent systems were consistent with each other within the error (±10%).
tle (100 ml) sealed with a butyl rubber cap and an aluminum stopper, Amino acid and peptide products were analyzed using a Jasco HPLC
and 2.5 ml of aqueous solution containing Na2S (39 mg, 0.5 mmol), system equipped with post-column derivatization with o-phthalaldehyde
CH3SNa (1.8 mg, 25 mmol), and NaOH was added for the in situ and a fluorescence detector operated at 345 nm for excitation and at
precipitation of NiS. The bottle was then filled with the reductive 455 nm for emission. Five citrate buffer solutions of different citrate
gas (80 ml, 1 atm) and was heated at 100°C for 7 days. The sample sus- concentrations and pH values were used as eluents in a stepwise con-
pension was then filtered with a PTFE membrane filter and analyzed dition. A cation-exchange column (AApak Na II-S2, Jasco) was used
by liquid chromatography–mass spectrometry (LC-MS) for identifi- at 50°C.
cation of organic acid products and by HPLC for their quantification. LC-MS measurements were conducted with a Xevo Qtof MS plat-
The filtrate had a pH of 8.6, which was measured by a portable pH form (Waters) combined with a UPLC system (Acquity, Waters). To
meter (Seven2Go Pro, Mettler Toledo). enhance the ionization of small acids while suppressing the interfer-
(ii) A serum bottle (100 ml) was charged with Ca(OH)2 (0.5 g, ence with inorganic salts, positive-mode electrospray ionization
6.7 mmol), closed, deaerated, and then charged with 2.5 ml of aqueous combined with reversed-phase LC was performed after derivatiza-
solution containing NiSO4 (77 mg, 0.5 mmol) and KCN (33 mg, 0.5 mmol) tion with 2-nitrophenylhydrazine (57). In the LC separation using
together with the reductive gas (80 ml, 1 atm). After heating at 100°C a CORTECS UPLC C18 column (Waters), 0.1% trifluoroacetate and
for 5 days, the sample suspension was filtered and analyzed for organic acetonitrile were used as the eluents for binary gradient elution with
acid and amino acid products. The filtrate showed a pH of 12.6. the flow rate at 0.3 ml min−1 and the column temperature at 35°C. The

Downloaded from https://www.science.org on September 17, 2021

(iii) A serum bottle (100 ml) was charged with NiSO4 ⋅ 6H2O (131 mg, acetonitrile volumetric ratio was initially held at 10%, increased linearly
0.5 mmol), closed, deaerated, and then charged with 2.5 ml of aqueous to 40% and then to 90% for 2 to 6 min and 6 to 6.7 min, respectively, and
solution containing Na2S (78 mg, 1 mmol) and glycine (9.4 mg, 125 mmol) held at 15% for 7 min. The time-of-flight analyzer was set to a sensitivity
together with the reductive gas (80 ml, 1 atm). After heating at 100°C mode with a resolving power of 20,000 at the mass/charge ratio (m/z) of
for 1 day, the sample suspension was filtered and analyzed for glycine 556 corresponding to protonated leucine encephalin, and the m/z range
peptides. The filtrate showed a pH of 7.9. of 20 to 1500 was calibrated with sodium formate.

Sample analysis Thermodynamic calculation

Organic acid products were quantified by using a Shimadzu HPLC The redox potentials of H2S and H2 as a function of temperature and
system equipped with an electric conductivity detector and an anion pH (Fig. 2) were calculated, respectively, assuming the following half
exchange column (Shim-pack SCR-102H, Shimadzu) set at 40°C. The reactions
p-toluenesulfonic acid solution (5 mM) was used as the eluent at a rate
of 1.6 ml min–1. 2Hþ þ 2e → H2 ð4Þ
1
H NMR spectra were acquired using a Bruker Avance III spectrom-
eter (400 MHz) at the sample temperature of 303.0 K. Typically, 0.45 ml
of sample solutions was mixed with 0.05 ml of D2O (99.9%; Merck S þ 2Hþ ðor Hþ Þ þ 2e → H2 S ðor HS Þ ð5Þ
Millipore) containing 5 mM 3-(trimethylsilyl)-1-propanesulfonic
acid-d6 sodium (DSS-d6; Sigma-Aldrich) and was placed in an NMR using the equations
tube (5 mm outside diameter; Wilmad-LabGlass). DSS-d6 was used
for the calibration of the 0-ppm (parts per million) position and to 1  
quantify the product concentrations as an internal standard. A solvent Eh ¼ 2RTlnaHþ  RTaH2  Df Go ðH2 Þ ð6Þ
2F
suppression was run to minimize the solvent signal. The obtained
spectra of sample solutions after the CO2 electrolysis (fig. S4) showed 1 
an intense signal of HCOO– at 8.45 ppm when CuS was used as a cat- Eh ¼ ð1 þ xÞRTlnaHþ  xRTlnaH2 S  ð1  xÞRTlnaHS
alyst, whereas no significant peak except for H2O and DSS-d6 appeared
2F 
on the other spectral regions and in the other sample spectra. The quan- þ Df Go ðSÞ  xDf Go ðH2 SÞ  ð1  xÞDf Go ðHS Þ ð7Þ
tified concentrations of HCOO– coincided well with the corresponding
HPLC results (within ±10%); therefore, the FE was calculated using the In these equations, T, R, and F stand for temperature in kelvin, the
HPLC data and was presented in Fig. 1B. gas constant (8.31447 J mol–1 K–1), and the Faraday constant (96485 J
The GC measurements were conducted using a GC-4000 (GL Sciences) mol–1 V–1), respectively. ai represents the activity of the species i, and x
MH 2 S
equipped with a HayeSep Q column (GL Sciences) and a Shincarbon-ST signifies the mole fraction of H2S (¼ MH S þM HS
; MH2 S and MHS denote
2

Kitadai et al., Sci. Adv. 2018; 4 : eaao7265 4 April 2018 5 of 7

SCIENCE ADVANCES | RESEARCH ARTICLE

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 Geoelectrochemical CO production: Implications for the autotrophic origin of life
Norio KitadaiRyuhei NakamuraMasahiro YamamotoKen TakaiYamei LiAkira YamaguchiAlexis GilbertYuichiro
UenoNaohiro YoshidaYoshi Oono

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