Certain subterranean environments of Earth have naturally accumulated long-lived radionuclides, such as 238U, 232Th, and 40K, near the presence of liquid water. In these natural radioactive environments, water radiolysis can produce chemical species of biological importance, such as H2. Although the proposal of radioactive decay as an alternative source of energy for living systems has existed for >30 years, this hypothesis gained strength after the recent discovery of a peculiar ecosystem in a gold mine in South Africa, whose existence is dependent on chemical species produced by water radiolysis. In this study, we calculate the chemical disequilibrium generated locally by water radiolysis due to gamma radiation. We then analyze the possible contribution of this disequilibrium for the emergence of life, considering conditions of early Earth and having as reference the alkaline hydrothermal vent theory. Results from our kinetic model point out the similarities between the conditions caused by water radiolysis and those found on alkaline hydrothermal systems. Our model produces a steady increase of pH with time, which favors the formation of a natural electrochemical gradient and the precipitation of minerals with catalytic activity for protometabolism in this aqueous environment. We conclude by describing a possible free-energy conversion mechanism based on protometabolism, which could be a requisite for the emergence of life in Hadean Earth.
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References
1.
AdamZ. (2007) Actinides and life's origins. Astrobiology, 7:852–872.
2.
AdamZR, HongoY, CleavesHJ, et al. (2018) Estimating the capacity for production of formamide by radioactive minerals on the prebiotic earth. Sci Rep, 8:265.
3.
AltairT, de AvellarMGBB, RodriguesF, et al. (2018) Microbial habitability of europa sustained by radioactive sources. Sci Rep, 8:260.
4.
AngR, KhanAU, TsujiiN, et al. (2015) Thermoelectricity generation and electron-magnon scattering in a natural chalcopyrite mineral from a deep-sea hydrothermal vent. Angew Chem Int Ed, 54:12909–12913.
5.
AtriD. (2016) On the possibility of galactic cosmic ray-induced radiolysis-powered life in subsurface environments in the universe. J R Soc Interface, 13:20160459.
6.
BargeLM, DoloboffIJ, WhiteLM, et al. (2012) Characterization of iron–phosphate–silicate chemical garden structures. Langmuir, 28:3714–3721.
7.
BargeLM, KrauseFC, JonesJ-P, et al. (2018) Geo-electrodes and fuel cells for simulating hydrothermal vent environments. Astrobiology, 18:1147–1158.
8.
BlairCC, D'HondtS, SpivackAJ, et al. (2007) Radiolytic hydrogen and microbial respiration in subsurface sediments. Astrobiology, 7:951–970.
9.
BouquetA, GleinCR, WyrickD, et al. (2017) Alternative energy: production of H2 by radiolysis of water in the rocky cores of icy bodies. Astrophys J, 840:L8.
10.
BoyerPD. (1997) The ATP synthase—a splendid molecular machine. Annu Rev Biochem, 66:717–749.
11.
BranscombE and RussellMJ. (2013) Turnstiles and bifurcators: the disequilibrium converting engines that put metabolism on the road. Biochim Biophys Acta Bioenerg, 1827:62–78.
12.
BranscombE and RussellMJ. (2018a) Frankenstein or a submarine alkaline vent: who is responsible for abiogenesis? Part 1: what is life–that it might create itself?. Bioessays, 40:1–8.
13.
BranscombE and RussellMJ. (2018b) Frankenstein or a submarine alkaline vent: who is responsible for abiogenesis?. Bioessays, 40:1700182.
14.
BranscombE, BiancalaniT, GoldenfeldN, et al. (2017) Escapement mechanisms and the conversion of disequilibria; the engines of creation. Phys Rep, 677:1–60.
15.
CataldoF and Iglesias-GrothS. (2017) Radiation chemical aspects of the origins of life. J Radioanal Nucl Chem, 311:1081–1097.
16.
ChivianD, BrodieEL, AlmEJ, et al. (2008) Environmental genomics reveals a single-species ecosystem deep within earth. Science, 322:275–278.
17.
ColmanDR, PoudelS, StampsBW, et al. (2017) The deep, hot biosphere: twenty-five years of retrospection. Proc Natl Acad Sci U S A, 114:6895–6903.
18.
CrankJ. (1975) The Mathematics of Diffusion, 2nd ed., Clarendon, Oxford, United Kingdom, p 414.
19.
DraganicIG and DraganicZD (1971) The Radiation Chemistry of Water. Academic Press, Inc., New York.
20.
DraganićIG, DraganićZD, and AltiparmakovD (1983) Natural nuclear reactors and ionizing radiation in the precambrian. Precambrian Res, 20:283–298.
21.
DraganićIG, BjergbakkeE, DraganićZD, and SehestedK (1991) Decomposition of ocean waters by potassium-40 radiation 3800 Ma ago as a source of oxygen and oxidizing species. Precambrian Res, 52:337–345.
22.
DraganicIG, DraganićIG, DraganicIG, et al. (2005) Radiolysis of water: a look at its origin and occurrence in the nature. Radiat Phys Chem, 72:181–186.
23.
DubessyJ, PagelM, BenyJ, et al. (1988) Radiolysis evidenced by H2O2 and H2-bearing fluid inclusions in three uranium deposits. Geochim Cosmochim Acta, 52:1155–1167.
24.
DuvalS, BaymannF, Schoepp-cothenetB, et al. (2019) Fougerite: the not so simple progenitor of the first cells. Interface Focus, 9:16–20.
25.
EbisuzakiT and MaruyamaS. (2017) Nuclear Geyser model of the origin of life: driving force to promote the synthesis of building blocks of life. Geosci Front, 8:275–298.
26.
FreitasSR, LongoKM, and RodriguesLF. (2009) Numerical modeling of the chemical composition of the atmosphere and its impacts on time, climate and air quality (translated from portuguese). Rev Brasil Meteorol, 24:188–207.
27.
GarrelsRM and ChristC. (1965) Solutions, Minerals, and Equilibria. Harper & Row, New York.
28.
GoodsellDS. (2009) The Machinery of Life. Springer New York, New York.
29.
GrassetO, DoughertyMKK, CoustenisA, et al. (2013) JUpiter ICy moons explorer (JUICE): an ESA mission to orbit ganymede and to characterise the jupiter system. Planet Space Sci, 78:1–21.
30.
HairerE and WannerG. (1996) Solving Ordinary Differential Equations II. Springer Series in Computational Mathematics, Springer Berlin Heidelberg, Berlin, Heidelberg, Germany.
31.
HallbauerDK. (1986) The Mineralogy and Geochemistry of Witwatersrand Pyrite, Gold and Uranium, and carbonaceous matter. In Mineral Deposits of Southern Africa, edited by AnhaeusserCR and MaskeSGeological Society of South Africa, Johannesbourg, South Africa, pp 731–752.
32.
HoffmannBA. (1992) Isolated reduction phenomenon in red beds: a result of porewater radiolysis. In Water-Rock Interaction, edited by KharakaYK and MaestAS, Springer Berlin Heidelberg, Berlin, Heidelberg, Germany, pp 503–506.
33.
HuberC and WachterhauserG. (1997) Activated acetic acid by carbon fixation on (Fe, Ni) S under primordial conditions. Science, 276:245–248.
34.
JavoyM. (1995) The integral enstatite chondrite model of the earth. Geophys Res Lett, 22:2219–2222.
35.
KelleyDS. (2005) A serpentinite-hosted ecosystem: the lost city hydrothermal field. Science, 307:1428–1434.
36.
LabontéJM, FieldEK, LauM, et al. (2015) Single cell genomics indicates horizontal gene transfer and viral infections in a deep subsurface Firmicutes population. Front Microbiol, 6:1–11.
37.
LaneN, AllenJF, and MartinW (2010) How did LUCA make a living? Chemiosmosis in the origin of life. Bioessays, 32:271–280.
38.
LaneN and MartinWF (2012) The origin of membrane bioenergetics. Cell, 151:1406–1416.
39.
LefticariuL, PrattLA, LaVerneJA, et al. (2010) Anoxic pyrite oxidation by water radiolysis products—a potential source of biosustaining energy. Earth Planet Sci Lett, 292:57–67.
40.
LideDR (2003) CRC Handbook of Chemistry and Physics. CRC Press, Boca Raton, FL.
41.
LinL-H, HallJ, Lippmann-PipkeJ, et al. (2005) Radiolytic H2 in continental crust: nuclear power for deep subsurface microbial communities. Geochem Geophys Geosyst, 6, doi: 10.1029/2004GC000907.
42.
LinL-H, WangP-L, RumbleD, et al. (2006) Long-term sustainability of a high-energy, low-diversity crustal biome. Science, 314:479–482.
43.
LippmannJ, StuteM, TorgersenT, et al. (2003) Dating ultra-deep mine waters with noble gases and 36Cl, Witwatersrand Basin, South Africa. Geochim Cosmochim Acta, 67:4597–4619.
44.
LowellRP (2002) Seafloor hydrothermal systems driven by the serpentinization of peridotite. Geophys Res Lett, 29:1531.
45.
MartinW, BarossJ, KelleyD, et al. (2008) Hydrothermal vents and the origin of life. Nat Rev Microbiol, 6:805–814.
46.
MaruyamaS and EbisuzakiT (2017) Origin of the earth: a proposal of new model called ABEL. Geosci Front, 8:253–274.
47.
MaruyamaS, KurokawaK, EbisuzakiT, et al. (2019) Nine requirements for the origin of Earth's life: not at the hydrothermal vent, but in a nuclear geyser system. Geosci Front, 10:1337–1357.
48.
MöllerFM, KriegelF, KießM, et al. (2017) Steep pH gradients and directed colloid transport in a microfluidic alkaline hydrothermal pore. Angew Chem Int Ed, 56:2340–2344.
49.
MuchowskaKB, VarmaSJ, Chevallot-BerouxE, et al. (2017) Metals promote sequences of the reverse Krebs cycle. Nat Ecol Evol, 1:1716–1721.
50.
Muñoz-SantiburcioD and MarxD. (2016) On the complex structural diffusion of proton holes in nanoconfined alkaline solutions within slit pores. Nat Commun, 7:12625.
51.
MurphyMP and O'NeillLAJ (1995) Order from disorder: the thermodynamics of complexity in biology. In What Is Life? The Next Fifty Years, edited by MurphyMP and ONeillLAJ, Cambridge University Press, Cambridge, United Kingdom, pp 161–174.
52.
NitschkeW, McGlynnSE, Milner-WhiteEJ, et al. (2013) On the antiquity of metalloenzymes and their substrates in bioenergetics. Biochim Biophys Acta Bioenerg, 1827:871–881.
53.
OmarGI, OnstottTC, and HoekJ (2003) The Origin of deep subsurface microbial communities in the Witwatersrand Basin, South Africa as deduced from apatite fission track analyses. Geofluids, 3:69–80.
54.
OokaH, McGlynnSE, and NakamuraR (2019) Electrochemistry at deep-sea hydrothermal vents: utilization of the thermodynamic driving force toward the autotrophic origin of life. ChemElectroChem, 6:1316–1323.
55.
PastinaB and LaverneJA (2001) Effect of molecular hydrogen on hydrogen peroxide in water radiolysis. J Phys Chem A, 105:9316–9322.
56.
RichardA, RozsypalC, MercadierJ, et al. (2012) Giant uranium deposits formed from exceptionally uranium-rich acidic brines. Nat Geosci, 5:142–146.
57.
RickardD and LutherGW (2007) Chemistry of iron sulfides. Chem Rev, 107:514–562.
58.
RobbLJ and MeyerFM (1995) The Witwatersrand Basin, South Africa: geological framework and mineralization processes. Ore Geol Rev, 10:67–94.
59.
RussellMJ and ArndtNT (2004) Geodynamic and metabolic cycles in the Hadean. Biogeosci Discuss, 1:591–624.
60.
RussellMJ and HallAJ (1997) The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front. J Geol Soc, 154:377–402.
61.
RussellMJ and MartinW (2004) The rocky roots of the acetyl-CoA pathway. Trends Biochem Sci, 29:358–363.
62.
RussellMJ, HallAJ, and TurnerD (1989) In vitro growth of iron sulphide chimneys: possible culture chambers for origin-of-life experiments. Terra Nova, 1:238–241.
63.
RussellMJ, NitschkeW, and BranscombE (2013) The inevitable journey to being. Philos Trans R Soc B Biol Sci, 368:20120254.
64.
SartoriLM (2014) Métodos Para Resolução de EDOs Stiff Resultantes de Modelos Químicos Atmosféricos. Universidade de São Paulo, São Paulo, Brazil.
65.
SavaryV and PagelM (1997) The effects of water radiolysis on local redox conditions in the Oklo, Gabon, natural fission reactors 10 and 16. Geochim Cosmochim Acta, 61:4479–4494.
66.
SchrodingerE (1946) What Is Life?. Cambridge University Press, Cambridge, United Kingdom.
67.
SojoV, HerschyB, WhicherA, et al. (2016) The origin of life in alkaline hydrothermal vents. Astrobiology, 16:181–197.
68.
SousaFL, ThiergartT, LandanG, et al. (2013) Early bioenergetic evolution. Philos Trans R Soc B Biol Sci, 368:20130088.
69.
SpinksJWT and WoodsRJ (1964) An Introduction to Radiation Chemistry, 1st ed., Wiley, New York.
70.
VanceS, HarnmeijerJ, KimuraJ, et al. (2007) Hydrothermal systems in small ocean planets. Astrobiology, 7:987–1005.
71.
VarmaSJ, MuchowskaKB, ChatelainP, et al. (2017) Metals enable a non-enzymatic acetyl CoA pathway. bioRxiv. 235523.
72.
WächtershäuserG (1990) Evolution of the first metabolic cycles (chemoautotrophy/reductive citric acid cycle/origin of life/pyrite). Proc Natl Acad Sci U S A, 87:200–204.
73.
WaiteJH, GleinCR, PerrymanRS, et al. (2017) Cassini finds molecular hydrogen in the Enceladus plume: evidence for hydrothermal processes. Science, 356:155–159.
74.
WhitmanWB, ColemanDC, and WiebeWJ (1998) Prokaryotes: the unseen majority. Proc Natl Acad Sci U S A, 95:6578–6583.
75.
YamamotoM, NakamuraR, KasayaT, et al. (2017) Spontaneous and widespread electricity generation in natural deep-sea hydrothermal fields. Angew Chem Int Ed, 56:5725–5728.
76.
ZhouJ, HeQ, HemmeCL, et al. (2011) How sulphate-reducing microorganisms cope with stress: lessons from systems biology. Nat Rev Microbiol, 9:452–466.
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