Origin of first cells at terrestrial, anoxic geothermal fields
Armen Y. Mulkidjanian a,b,1,
Andrew Yu. Bychkov c,
Daria V. Dibrova a,d,
Michael Y. Galperin e, and Eugene V. Koonin e,1
Author Affiliations
aSchool of Physics, University of Osnabrück, D-49069 Osnabrück, Germany;
bA. N. Belozersky Institute of Physico-Chemical Biology and Schools of
cGeology and
dBioengineering and Bioinformatics, Moscow State University, Moscow 119992, Russia; and
eNational Center for Biotechnology Information, National Library of Medicine, National Institutes of Health, Bethesda, MD 20894
Edited by Norman H. Sleep, Stanford University, Stanford, CA, and approved January 17, 2012 (received for review October 28, 2011)
Abstract
All cells contain much more potassium, phosphate, and transition metals than modern (or reconstructed primeval) oceans, lakes, or rivers. Cells maintain ion gradients by using sophisticated, energy-dependent membrane enzymes (membrane pumps) that are embedded in elaborate ion-tight membranes. The first cells could possess neither ion-tight membranes nor membrane pumps, so the concentrations of small inorganic molecules and ions within protocells and in their environment would equilibrate. Hence, the ion composition of modern cells might reflect the inorganic ion composition of the habitats of protocells. We attempted to reconstruct the “hatcheries” of the first cells by combining geochemical analysis with phylogenomic scrutiny of the inorganic ion requirements of universal components of modern cells. These ubiquitous, and by inference primordial, proteins and functional systems show affinity to and functional requirement for K+, Zn2+, Mn2+, and phosphate. Thus, protocells must have evolved in habitats with a high K+/Na+ ratio and relatively high concentrations of Zn, Mn, and phosphorous compounds. Geochemical reconstruction shows that the ionic composition conducive to the origin of cells could not have existed in marine settings but is compatible with emissions of vapor-dominated zones of inland geothermal systems. Under the anoxic, CO2-dominated primordial atmosphere, the chemistry of basins at geothermal fields would resemble the internal milieu of modern cells. The precellular stages of evolution might have transpired in shallow ponds of condensed and cooled geothermal vapor that were lined with porous silicate minerals mixed with metal sulfides and enriched in K+, Zn2+, and phosphorous compounds.
prebiotic chemistry, abiotic photosynthesis, hydrothermal alteration, origin of life, Na+/K+ gradient
Footnotes
1To whom correspondence may be addressed. E-mail:amulkid@uos.de or koonin@ncbi.nlm.nih.gov.
Author contributions: A.Y.M. designed research; A.Y.M., A.Y.B., D.V.D., M.Y.G., and E.V.K. performed research; A.Y.M., A.Y.B., and E.V.K. contributed new reagents/analytic tools; A.Y.M., A.Y.B., D.V.D., M.Y.G., and E.V.K. analyzed data; and A.Y.M., A.Y.B., D.V.D., M.Y.G., and E.V.K. wrote the paper.
The authors declare no conflict of interest.
*This Direct Submission article had a prearranged editor.
†“But if (and oh what a big if) we could conceive in some warm little pond with all sorts of ammonia and phosphoric salts, light, heat, electricity &c. present, that a protein compound was chemically formed, ready to undergo still more complex changes….” —from Darwin's 1871 letter to Joseph Hooker (17).
‡ZnS, broadly known as phosphor (from “phosphorescence”), shows a unique ability to convert diverse kinds of energy, including that of light quanta, X-rays, electrons (as in displays), α-particles (ZnS was introduced as the first inorganic scintillator by Sir William Crookes in 1903), into (electro)chemical energy of separated electric charges (reviewed in ref. 10).
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1117774109/-/DCSupplemental.
Freely available online through the PNAS open access option.
