Origins of Life and Evolution of Biospheres

, Volume 48, Issue 4, pp 373–393 | Cite as

The Birthplace of Proto-Life: Role of Secondary Minerals in Forming Metallo-Proteins through Water-Rock Interaction of Hadean Rocks

  • Kazumi YoshiyaEmail author
  • Tomohiko Sato
  • Soichi Omori
  • Shigenori Maruyama
Prebiotic Chemistry


The surface of Hadean Earth was mainly covered with three types of rocks—komatiite, KREEP basalt and anorthosite—which were remarkably different from those on the modern Earth. The water-rock interaction between these rocks and water provided a highly reducing environment and formed secondary minerals on the surface of the rocks that are important for producing metallo-enzymes for the emergence of primordial life. Previous studies suggested a correlation between the active site of metallo-enzymes and sulfide minerals based on the affinity of their structures, but they did not discuss the origin of metallic elements contained in these minerals which is critical to understanding where life began. We investigated secondary minerals formed through water-rock interactions of komatiite in a subaerial geyser system, then discussed the relationship between the active site of metallo-enzymes and secondary minerals. Instead of komatiite, we used serpentinite collected from the Hakuba Happo area, Nagano Prefecture in central-north Japan, which is thought to be a modern analog for the Hadean environment. We found several minor minerals, such as magnetite, chromite, pyrite and pentlandite in addition to serpentine minerals. Pentlandite has not been mentioned in previous studies as one of the candidates that could supply important metallic elements to build metallo-enzymes. It has been shown to be a catalyst for hydrogen generation possibly, because of structural similarity to the active site of hydrogenases. We consider the possibility that nickel-iron sulfide, pentlandite, could be important minerals for the origin of life. In addition, we estimated what kinds of minor minerals would be obtained from the water-rock interaction of these rocks using thermodynamic calculations. KREEP basalt contains a large amount of iron and it could be useful for producing metallo-enzymes, especially ferredoxins—electron transfer enzymes, which may have assisted in the emergence of life.


Birthplace of life Serpentinite KREEP basalt Metallo-enzymes Metal sulfide 



We thank Chief Editor Alan W. Schwartz and anonymous reviewer whose faithful and constructive comments improved our manuscript. We thank Dr. Jim Cleaves for discussion and comments, Ms. Reiko Hattori for technical assistance completing this paper and Ms. Lucy Kwok for improving our English. This work was supported by JSPS grants (No. 26106001, 26106002) from the Ministry of Education, Culture, Sports, Science and Technology of Japan.


  1. Arndt NT, Nisbet EG (2012) Processes on the young earth and the habitats of early life. Annu Rev Earth Planet Sci 40:521–549CrossRefGoogle Scholar
  2. Arndt NT, Czamanske GK, Walker RJ, Chauvel C, Fedorenko VA (2003) Geochemistry and origin of the intrusive hosts of the Noril’sk-Talnakh cu-Ni-PGE sulfide deposits. Econ Geol 98:495–515Google Scholar
  3. Baross JA, Hoffman SE (1985) Submarine hydrothermal vents and associated gradient environments as sites for the origin and evolution of life. Orig Life Evol Biosph 15:327–345CrossRefGoogle Scholar
  4. Bottke WF, Vokrouhlický D, Minton D, Nesvorný D, Morbidelli A, Brasser R, Simonson B, Levison HF (2012) An Archaean heavy bombardment from a destabilized extension of the asteroid belt. Nature 485:78–81CrossRefGoogle Scholar
  5. Brazelton WJ, Ludwig KA, Sogin ML, Andreishcheva EN, Kelley DS, Shen CC, Edwards RL, Baross JA (2010) Archaea and bacteria with surprising microdiversity show shifts in dominance over 1,000-year time scales in hydrothermal chimneys. Proc Natl Acad Sci 107:1612–1617CrossRefGoogle Scholar
  6. Brazelton WJ, Thornton CN, Hyer A, Twing KI, Longino AA, Lang SQ, Lilley MD, Früh-Green GL, Schrenk MO (2017) Metagenomic identification of active methanogens and methanotrophs in serpentinite springs of the Voltri massif, Italy. PeerJ 5:e2945CrossRefGoogle Scholar
  7. Byerly BL, Lowe DR, Drabon N, Coble MA, Burns DH, Byerly GR (2018) Hadean zircon from a 3.3 Ga sandstone, Barberton greenstone belt, South Africa. Geology 46:967–970CrossRefGoogle Scholar
  8. Crowley JL, Myers JS, Sylvester PJ, Cox RA (2005) Detrital zircon from the Jack Hills and mount Narryer, Western Australia: evidence for diverse> 4.0 Ga source rocks. J Geol 113:239–263CrossRefGoogle Scholar
  9. Damer B, Deamer D (2015) Coupled phases and combinatorial selection in fluctuating hydrothermal pools: a scenario to guide experimental approaches to the origin of cellular life. Life 5:872–887CrossRefGoogle Scholar
  10. Darnault C, Volbeda A, Kim EJ, Legrand P, Vernède X, Lindahl PA, Fontecilla-Camps JC (2003) Ni-Zn-[Fe4-S4] and Ni-Ni-[Fe4-S4] clusters in closed and open α subunits of acetyl-CoA synthase/carbon monooxide dehydrogenase. Nat Struct Biol 10:271–279CrossRefGoogle Scholar
  11. Dobbek H, Svetlitchnyi V, Gremer L, Huber R, Meyer O (2001) Crystal structure of a carbon monoxide dehydrogenase reveals a [Ni-4Fe-5S] cluster. Science 293:1281–1285CrossRefGoogle Scholar
  12. Dohm JM, Maruyama S (2015) Habitable trinity. Geosci Front 6:95–101CrossRefGoogle Scholar
  13. Ebisuzaki T, Maruyama S (2017) Nuclear geyser model of the origin of life: driving force to promote the synthesis of building blocks of life. Geosci Front 8:275–298CrossRefGoogle Scholar
  14. Eck RV, Dayhoff MO (1966) Evolution of the structure of ferredoxin based on living relics of primitive amino acid sequences. Science 152:363–366CrossRefGoogle Scholar
  15. Fontecilla-Camps JC, Amara P, Cavazza C, Nicolet Y, Volbeda A (2009) Structure–function relationships of anaerobic gas-processing metalloenzymes. Nature 460:814–822CrossRefGoogle Scholar
  16. Frost BR (1985) On the stability of sulfides, oxides, and native metals in serpentinite. J Petrol 26:31–63CrossRefGoogle Scholar
  17. Froude DO, Ireland TR, Kinny PD, Williams IS, Compston W, Williams IR, Myers JS (1983) Ion microprobe identification of 4,100–4,200 Myr-old terrestrial zircons. Nature 304:616–618CrossRefGoogle Scholar
  18. Geological Survey of Japan, AIST (ed.) (2015) Seamless digital geological map of Japan 1: 200,000. May 29, 2015 version. Geological Survey of Japan, National Institute of Advanced Industrial Science and Technology.Google Scholar
  19. Hall DO, Cammack R, Rao KK (1971) Role for ferredoxins in the origin of life and biological evolution. Nature 233:136–138CrossRefGoogle Scholar
  20. Harrison TM, Blichert-Toft J, Müller W, Albarede F, Holden P, Mojzsis SJ (2005) Heterogeneous hadean hafnium: evidence of continental crust at 4.4 to 4.5 Ga. Science 310:1947–1950CrossRefGoogle Scholar
  21. Hughes SS, Delano JW, Schmitt RA (1989) Petrogenetic modeling of 74220 high-Ti orange volcanic glasses and the Apollo 11 and 17 high-Ti mare basalts. In Lunar and Planetary Science Conference Proceedings 19:175–188Google Scholar
  22. Iizuka T, Horie K, Komiya T, Maruyama S, Hirata T, Hidaka H, Windley BF (2006) 4.2 Ga zircon xenocryst in an Acasta gneiss from northwestern Canada: evidence for early continental crust. Geology 34:245–248CrossRefGoogle Scholar
  23. Johnson JW, Oelkers EH, Helgeson HC (1992) SUPCRT92: a software package for calculating the standard molal thermodynamic properties of minerals, gases, aqueous species, and reactions from 1 to 5000 bar and 0 to 1000°C. Comput Geosci 18:899–947CrossRefGoogle Scholar
  24. Kamber BS (2015) The evolving nature of terrestrial crust from the hadean, through the Archaean, into the Proterozoic. Precambrian Res 258:48–82CrossRefGoogle Scholar
  25. Kasting JF (1989) Long-term stability of the Earth's climate. Glob Planet Chang 1:83–95CrossRefGoogle Scholar
  26. Kawabe I (1974) Transition metal contents of Paleozoic geosynclinal basalts in Southwest Japan and their geological significance. J Geol Sot Jpn 80:539–554 (in Japanese with English abstract)CrossRefGoogle Scholar
  27. Kemp AIS, Wilde SA, Hawkesworth CJ, Coath DD, Nemchin A, Pidgeon RT, Vervoort JD, DuFrane SA (2010) Hadean crustal evolution revisited: new constraints from Pb-Hf isotope systematics of the Jack Hills zircons. Earth Planet Sci Lett 296:45–56CrossRefGoogle Scholar
  28. Konkena B, Junge Puring K, Sinev I, Piontek S, Khavryuchenko O, Dürholt JP, Schmid R, Tüysüz H, Muhler M, Schuhmann W, Apfel UP (2016) Pentlandite rocks as sustainable and stable efficient electrocatalysts for hydrogen generation. Nat Commun 7:12269–12276CrossRefGoogle Scholar
  29. Korenaga J (2007) Thermal cracking and the deep hydration of oceanic lithosphere: a key to the generation of plate tectonics. J Geophys Res 112:B05408CrossRefGoogle Scholar
  30. Kulik DA, Wagner T, Dmytrieva SV, Kosakowski G, Hingerl FF, Chudnenko KV, Berner UR (2013) GEM-Selektor geochemical modeling package: revised algorithm and GEMS3K numerical kernel for coupled simulation codes. Comput Geosci 17:1–24Google Scholar
  31. Lill R (2009) Function and biogenesis of iron–Sulphur proteins. Nature 460:831–838CrossRefGoogle Scholar
  32. Ljungdhal LG (1986) The autotrophic pathway of acetate synthesis in acetogenic bacteria. Annu Rev Microbiol 40:415–450CrossRefGoogle Scholar
  33. Lubitz W, Ogata H, Rüdiger O, Reijerse E (2014) Hydrogenases. Chem Rev 114:4081–4148CrossRefGoogle Scholar
  34. Lyon EJ, Shima S, Boecher R, Thauer RK, Grevels FW, Bill E, Albracht SP (2004) Carbon monoxide as an intrinsic ligand to iron in the active site of the iron− sulfur-cluster-free hydrogenase H2-forming methylenetetrahydromethanopterin dehydrogenase as revealed by infrared spectroscopy. J Am Chem Soc 126:14239–14248CrossRefGoogle Scholar
  35. Malkin R, Rabinowitz JC (1966) The reconstitution of clostridial ferredoxin. Biochem Biophys Res Commun 23:822–827CrossRefGoogle Scholar
  36. Maruyama S, Ikoma M, Genda H, Hirose K, Yokoyama T, Santosh M (2013) The naked planet earth: Most essential pre-requisite for the origin and evolution of life. Geosci Front 4:141–165CrossRefGoogle Scholar
  37. Matsumoto T (2009) Acetyl CoA synthase, a key player of carbon fixation in nature. Bulletin of Japan Society of Coordination Chemistry 54:38–51Google Scholar
  38. McDonough WF, Sun SS (1995) The composition of the earth. Chem Geol 120:223–253CrossRefGoogle Scholar
  39. Meyer, C., 2010. The lunar sample compendium. Accessed 27 Nov 2017
  40. Miller SL (1953) A production of amino acids under possible primitive earth conditions. Science 117:528–529CrossRefGoogle Scholar
  41. Mulkidjanian AY, Bychkov AY, Dibrova DV, Galperin MY, Koonin EV (2012) Origin of first cells at terrestrial, anoxic geothermal fields. Proc Natl Acad Sci 109:E821–E830CrossRefGoogle Scholar
  42. Nakamizu M, Okada M, Yamazaki T, Komatsu M (1989) Metamorphic rocks in the Omi-Renge serpentinite mélange, Hida marginal Tectonic Belt, Central Japan. Mem Geol Soc Jpn 33:21–35 (in Japanese with English abstract)Google Scholar
  43. Nesbitt RW, Sun SS, Purvis AC (1979) Komatiites; geochemistry and genesis. Can Mineral 17:165–186Google Scholar
  44. Neubeck A, Duc NT, Hellevang H, Oze C, Bastviken D, Bacsik Z, Holm NG (2014) Olivine alteration and H2 production in carbonate-rich, low temperature aqueous environments. Planet Space Sci 96:51–61CrossRefGoogle Scholar
  45. Nicolet Y, Piras C, Legrand P, Hatchikian CE, Fontecilla-Camps JC (1999) Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center. Structure 7:13–23CrossRefGoogle Scholar
  46. Nitschke W, McGlynn SE, Milner-White EJ, Russell MJ (2013) On the antiquity of metalloenzymes and their substrates in bioenergetics. Biochim Biophys Acta (BBA)-Bioenergetics 1827:871–881CrossRefGoogle Scholar
  47. Nozaka T (2012) Petrological constraints on hydrogen production during serpentinization: a review. Japanese Magazine of Mineralogical and Petrological Sciences 41:174–184CrossRefGoogle Scholar
  48. O’Neil J, Carlson RW, Francis D, Stevenson RK (2008) Neodymium-142 evidence for hadean mafic crust. Science 321:1828–1831CrossRefGoogle Scholar
  49. Ogata H, Nishikawa K, Lubitz W (2015) Hydrogens detected by subatomic resolution protein crystallography in a [NiFe] hydrogenase. Nature 520:571–574CrossRefGoogle Scholar
  50. Ohta H, Maruyama S, Takahashi E, Watanabe Y, Kato Y (1996) Field occurrence, geochemistry and petrogenesis of the Archean mid-oceanic ridge basalts (AMORBs) of the Cleaverville area, Pilbara craton, Western Australia. Lithos 37:199–221CrossRefGoogle Scholar
  51. Ohtake M, Matsunaga T, Haruyama J, Yokota Y, Morota T, Honda C, Hirata N (2009) The global distribution of pure anorthosite on the moon. Nature 461:236–240CrossRefGoogle Scholar
  52. Pizzarello S, Cronin JR (2000) Non-racemic amino acids in the Murray and Murchison meteorites. Geochim Cosmochim Acta 64:329–338CrossRefGoogle Scholar
  53. Ragsdale SW (2004) Life with carbon monoxide. Crit Rev Biochem Mol Biol 39:165–195CrossRefGoogle Scholar
  54. Rempfert KR, Miller HM, Bompard N, Nothaft D, Matter JM, Kelemen P, Fierer N, Templeton AS (2017) Geological and geochemical controls on subsurface microbial life in the Samail ophiolite, Oman. Front Microbiol 8:56CrossRefGoogle Scholar
  55. Rhodes, J. M., Rodgers, K. V., Bansal, B. M., Wiesmann, H., Shih, C., Nyquist, L. E., Hubbard, N. J., 1974. The relationships between geology and soil chemistry at the Apollo 17 landing site. In Lunar and planetary science conference proceedings (Vol. 5, pp. 1097–1117)Google Scholar
  56. Rodriguez-Garcia M, Surman AJ, Cooper GJ, Suárez-Marina I, Hosni Z, Lee MP, Cronin L (2015) Formation of oligopeptides in high yield under simple programmable conditions. Nat Commun 6:8385CrossRefGoogle Scholar
  57. Russell MJ, Hall AJ (1997) The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front. J Geol Soc Lond 154:377–402CrossRefGoogle Scholar
  58. Russell, M. J., Hall, A. J., 2006. The onset and early evolution of life. In: evolution of early Earth’s atmosphere hydrosphere, and biosphere-constraints from ore deposits (eds. S. E. Kesler and H. Ohmoto), Geochemical Society of America Memoir 198, 1–32Google Scholar
  59. Russell MJ, Martin W (2004) The rocky roots of the acetyl coenzyme-a pathway. Trends Biochem Sci 24:358–363CrossRefGoogle Scholar
  60. Russell MJ, Barge LM, Bhartia R, Bocanegra D, Bracher PJ, Branscomb E, Kidd R, McGlynn S, Meier DH, Nitschke W, Shibuya T, Vance S, White L, Kanik I (2014) The drive to life on wet and icy worlds. Astrobiology 14:308–343CrossRefGoogle Scholar
  61. Sakata K, Yabuta H, Kondo T (2014) Effects of metal ions and pH on the formation and decomposition rates of di-and tri-peptides in aqueous solution. Geochem J 48:219–230CrossRefGoogle Scholar
  62. Santosh M, Arai T, Maruyama S (2017) Hadean earth and primordial continents: the cradle of prebiotic life. Geosci Front 8:309–327CrossRefGoogle Scholar
  63. Sato T, Yoshiya K, Maruyama S (2019) History of the hadean “living microfossil” and ultra-reducing environments. J Geogr (Chigaku Zasshi), (in Japanese with English abstract), acceptedGoogle Scholar
  64. Sleep NH (2010) The hadean-archaean environment. Cold Spring Harb Perspect Biol 2:a002527CrossRefGoogle Scholar
  65. Sossi PA, Eggins SM, Nesbitt RW, Nebel O, Hergt JM, Campbell IH, O’Neill HC, Kranendonk MV, Davies DR (2016) Petrogenesis and geochemistry of Archean komatiites. J Petrol 57:147–184CrossRefGoogle Scholar
  66. Suda K, Ueno U, Yoshizaki M, Nakamura H, Kurokawa K, Nishiyama E, Yoshino K, Hongoh Y, Kawachi K, Omori S, Yamada K, Yoshida N, Maruyama S (2014) Origin of methane in serpentinite-hosted hydrothermal systems: the CH4–H2–H2O hydrogen isotope systematics of the Hakuba Happo hot spring. Earth Planet Sci Lett 386:112–125CrossRefGoogle Scholar
  67. Suzuki S, Ishii S, Wu A, Cheung A, Tenney A, Wanger G, Kuenen JG, Nealson KH (2013) Microbial diversity in the cedars, an ultrabasic, ultrareducing, and low salinity serpentinizing ecosystem. Proc Natl Acad Sci USA 110:15336–15341CrossRefGoogle Scholar
  68. Suzuki S, Ishii S, Hoshino T, Rietze A, Tenney A, Morrill PL, Inagaki F, Kuenen JG, Nealson KH (2017) Unusual metabolic diversity of hyperalkaliphilic microbial communities associated with subterranean serpentinization at the cedars. ISME J:1–15Google Scholar
  69. Svetlitchnyi V, Dobbeck H, Meyer-Klaucke W, Meins T, Thiele B, Römer P, Huber R, Meyer O (2004) A functional Ni–Ni–[4Fe4S] cluster in the monomeric acetyl-CoA synthase from Carboxydothermus hydrogenoformans. Proc Natl Acad Sci USA 101:446–451CrossRefGoogle Scholar
  70. Valley JW, Cavosie AJ, Ushikubo T, Reinhard DA, Lawrence DF, Larson DJ, Clifton PH, Kelly TF, Wilde SA, Moser DE, Spicuzza MJ (2014) Hadean age for a post-magma ocean zircon confirmed by atom-probe tomography. Nat Geosci 7:219–223CrossRefGoogle Scholar
  71. Vignais PM, Billoud B (2007) Occurrence, classification, and biological function of hydrogenases: an overview. Chem Rev 107:4206–4272CrossRefGoogle Scholar
  72. Volbeda A, Darnault C, Tan X, Lindahl PA, Fontecilla-Camps JC (2009) Novel domain arrangement in the crystal structure of a truncated acetyl-CoA synthase from Moorella thermoacetica. Biochemistry 48:7916–7926CrossRefGoogle Scholar
  73. Wänke, H., Baddenhausen, H., Dreibus, G., Jagoutz, E., Kruse, H., Palme, H., Teschke, F., 1973. Multielement analyses of Apollo 15, 16, and 17 samples and the bulk composition of the moon. In Lunar and planetary science conference proceedings (Vol. 4, p. 1461)Google Scholar
  74. Weiss MC, Sousa FL, Mrnjavac N, Neukirchen S, Roettger M, Nelson-Sathi S, Martin WF (2016) The physiology and habitat of the last universal common ancestor. Nat Microbiol 1:16116CrossRefGoogle Scholar
  75. Westall F, Hickman-Lewis K, Hinman N, Gautret P, Campbell KA, Bréhéret JG, Foucher F, Hubert A, Sorieul S, Dass AV, Kee TP, Georgelin T, Brack A (2018) A hydrothermal-sedimentary context for the origin of life. Astrobiology 18:259–293CrossRefGoogle Scholar
  76. Wilde SA, Valley JW, Peck WH, Graham CM (2001) Evidence from detrital zircons for the existence of continental crust and oceans on the earth 4.4 Gyr ago. Nature 409:175–178CrossRefGoogle Scholar
  77. Zahnle K, Arndt N, Cockell C, Halliday A, Nisbet E, Selsis F, Sleep NH (2007) Emergence of a habitable planet. Space Sci Rev 129:35–78CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Kazumi Yoshiya
    • 1
    Email author
  • Tomohiko Sato
    • 1
  • Soichi Omori
    • 2
  • Shigenori Maruyama
    • 1
    • 3
  1. 1.Earth-Life Science InstituteTokyo Institute of TechnologyTokyoJapan
  2. 2.The Open University of JapanChibaJapan
  3. 3.Novosibirsk State UniversityNovosibirskRussia

Personalised recommendations