Oparin-2014 The problem of the origin of life Moscow, September 22 -26, 2014 Role of hydrogen and metals in the formation and evolution metabolic systems Mikhail Fedonkin Geological Institute, Russian Academy of Sciences, Moscow
Alexander Ivanovich Oparin, 1894 -1980, biochemist, author of theory of the origin of life: Oparin, A. I. The Origin of Life. Moscow: Moscow Worker publisher, 1924. According to Oparin the early Earth had a strongly reducing atmosphere, containing hydrogen, water vapor, methane, and ammonia. These elements and simple compounds were the raw materials for complex organic molecules subjected to natural selection and evolution.
Georges Cuvier, 1769 - 1832
Tornado, Cuvier’s metaphor for life: priority of energy flow
Morowitz, 1992 Nonequilibrium, - the flow of matter or energy, can be the source of order and complexity (Prigogine and Stengers, 2003)
Origin of life: physical approach priority In the contrast to the chemical approach focused on the origin of “building blocks” of the living cell (RNA, DNA, proteins etc. ), the physical approach concentrates on the origin of energy flow common for all living organisms: proton gradients and electron transfer. Central place should belong to hydrogen and metals!
Wackett et al. , 2004
1877 -1932 В начале был единый Океан, Дымившийся на раскаленном ложе. И в этом жарком лоне завязался Неразрешимый узел жизни: плоть, Пронзенная дыханьем и биеньем. Планета стыла. Жизни разгорались. Наш пращур, что из охлажденных вод Свой рыбий остов выволок на землю, В себе унес весь древний Океан С дыханием приливов и отливов, С первичной теплотой и солью вод — Живую кровь, струящуюся в жилах. In the beginning there was a single ocean, That was smoking on the heated bed. And in this hot lap ensued Insoluble knot of life: the flesh, Pierced by breath and beat. The planet cooled. Lives flared. Our ancestor that of chilled water His fish skeleton dragged to the ground, In itself carried all the ancient ocean With the breath of the tides, With the primary heat and salt of water Live blood flowing in his veins.
Concentration of metals in human plasma and in sea water (nm/l) Fe Zn Cu Mo Cr V Mn Ni 22300 / 0, 5 -20 17200 / 80 16500 / 10 10000 / 100 55 / 4 200 / 40 110 / 0, 7 44 / 5
Phytoplankton vs sea water chemistry Fe – 87 000 Zn – 65 000 Al – 25 000 N – 19 000 P – 15 000 Cu – 17 000 Mn – 9 400 Cd – 910 S – 1. 7 Mg – 0. 69 Na – 0. 14 Ratio of the concentration of elements in phytoplankton to concentration of elements in sea water reflects the degree of biological need and, on the other hand, the degree of depletion of the particular elements from the seawater Bowen (1966)
Biologically relevant metals § Na, K, Ca, Mg, Mn, Zn, Cu, Fe, V, Cr, Co, Ni, Mo, W Metals in the living cell serve as – electron-transfer agents – oxygen carriers – cellular messengers – structural components of proteins – nucleophiles – catalysts
Some specific metal ion catalysis Frausto da Silva & Williams, 1997
Transition metals as catalysts § over 30% of known enzymes contain metal ions as a cofactor of an active site § metal activators increase the rate of reactions catalysed by enzymes up 1012 times! § removal of the metals from protein molecule leads to decrease or loss of its catalytic properties.
Could the metals ions or their simple compounds be the first catalysers that, due to fast reactions segregated life, first dynamically and then structurally, from the mineral realm?
At catalytic centres, metals increase acidity, electrophilicity and/or nucleophilicity of reacting species, promote heterolysis, or receive and donate electrons. The protein’s primary and secondary metalcoordination spheres tune the properties of the metal to optimize reactivity and influence metal selection. Donor ligands (S, O or N) can impart bias in favour of the correct metal.
Crystal structure of the nitrogenase Mo-Fe protein. Are the proteins the later addition to the primary inorganic catalysts?
The elements used as cofactors by enzymes are shown in blue. The height of each column represents the proportion of all enzymes with known structures using the respective metal. A single enzyme uses cadmium (Waldron et al. , 2009).
The proportion of proteins using the indicated metals that occur in each of the six Enzyme classes: oxidoreductases (EC 1), blue; transferases (EC 2), yellow; Hydrolases (EC 3), purple; lyases (EC 4), pink; isomerases (EC 5), green; Ligases (EC 6), grey. EC, Enzyme Commission. After Waldron et al. , 2009
The abundances of Fe-, Zn-, Mn-, and Co. B 12 -binding structural domains in the proteomes of Archaea (black), Bacteria (red), and Eukarya (blue). Dupont et al. , 2009
Cu Bacteria Occurrence of Cu users and nonusers among bacteria differing in their dependence on oxygen (Ridge et al. , 2008).
Cu Archaea Occurrence of Cu users and nonusers among archaea differing in their dependence on oxygen (Ridge et al. , 2008).
§ Taxonomic and ecological distribution of the metals as activators of enzymes may be a subject for geohistorical and evolutionary interpretation.
Hydrogen role in the energetic metabolism § Hydrogen, the most abundant chemical element in the Universe, well could be the primary fuel for early life. § Biological role of hydrogen is related not only to the domination of H 2 O in the mass of the living cell. § The soft hydrogen bonds provide stability and versatility of the macromolecules. § Many recent microorganisms use H 2 as a source of energy.
Hydrogen role in the energetic metabolism § Various microbial enzymes perform the H+ transfer. § The H+ gradients are used in the process of ATP generation. § Negative ion of hydrogen H- is known as an energy currency of the cell (an equivalent of two electrons). § H 2 as a key intermediate product of anaerobic metabolism makes a universal trophic (energetic) connection between the microorganisms that live on different substrates – a key ecosystem factor.
Biological role of hydrogen § Many microorganisms use H 2 as an electron donor in both catabolic and anabolic redox processes. § H 2 plays an important role as an intermediary metabolite during microbial transformation of organic matter. § H 2 is produced as a catabolic end product by a variety of anaerobic bacteria or as a byproduct of the nitrogenase reaction by nitrogen-fixing bacteria.
Biological role of hydrogen § Anaerobically, hydrogen oxidation is coupled to CO 2 reduction by methanogens and acidogens, and to sulfate reduction by sulfidogenic bacteria. § Aerobically, the hydrogen bacteria use hydrogen gas for both energy conservation and autotrophic CO 2 fixation. § Phototrophic bacteria can either produce or consume molecular hydrogen.
Biological role of hydrogen § Hydrogen as a source of energy and free electrons is easy to take up by various chemosynthesizing organisms. § The near universality of hydrogen metabolism among microorganisms and high similarity between all the Ni-Fe hydrogenase operons suggests that the microbial ability to metabolize hydrogen is of great importance and ancient origin (Casalot, 2003).
Hydrogen metabolism in Bacteria
Proportions of the H 2 oxidizing methanogenic Archaea (99%) and Bacteria in groundwater from Lidy Hot Spring (Beaverhead Mts, Idaho). Depth 200 m, temperature 58. 5 °C, anoxic, very low dissolved Corg and high concentration of H 2 (Chapelle et al. , 2002).
Spear et al. , 2006
Stetter, 1996 O 2 Hyperthermophyles H 2
EUBACTERIA ARCHAEOBACTERIA EUKARYOTES Fundamental difference between prokaryotic and eukaryotic physiology from the standpoint of energy metabolism may indicate chemoautotrophic origin of life. Large part of the reactions in the prokaryotes involves hydrogen and its volatile compounds that must be the primary feature. Redox reactions involving inorganic donors and acceptors after Amend & Shock, 2001, Doeller et al. 2001 (see refs. in Martin & Russell, 2002)
catalysts The prime role of hydrogen and its close interactions with other established biogeochemical cycles (Williams & Ramsden 2007)
The role of hydrogen and the connection that it forms between the geological world and the biological world (Nealson, 2005)
The deep hydrogen-driven biosphere hypothesis (Karsten, Pedersen, 2000)
Early Earth (> 4 Ga) § Radiogenic heat was over 10 times higher than at present § Contribution of close Moon into the mechanical heating of the Earth interior was high § Intensive volcanism § Full recycling of the earth crust § Low relief § Global shallow ocean
1 -10 bars CO 2 ocean 400 C springs CO 2 ocean Mantle convection cells at 4. 4 Ga Russell & Hall 2006 GSA Mem 192, 1 -32
Early Earth (> 4 Ga) § § § § Low luminosity of Sun (30% below present) Dense green-house atmosphere High temperature of the planet surface Rapid formation of the metal core of the planet (during the first 100 Ma) Magnetic field was established early as well Reducing atmosphere Anoxia, no protective ozone screen
Iron sulfide bubbles around alkaline vents in the Hadean ocean. Fe-Ni sulfides catalyzed synthesis of simple organic molecules that formed more complex peptides. The peptides have coated the inside surfaces of the bubbles, the first step towards cellular autonomy. Russell, 2006 Hydrothermal mounds were key to life’s origin. Alkaline fluids from such vents carried hydrogen, sulfide and ammonia. Water was enriched with the heavy metals (Fe, Ni etc. ).
From the physical point of view the onset of life by the hydrothermal systems or in the hot ocean seems to be a plausible hypothesis because of the factors such as: - electron-rich environment - electrochemical gradients - abundance of metal ions - molecular hydrogen and its volatile compounds
Sources of hydrogen on early Earth § Kadik A. A. & Litvin Yu. A. (2007): … the first stages of the core growth took place under reduced conditions imposed by the pristine terrestrial materials and was accompanied by the emission of CH 4, H 2, NH 3 and minor H 2 O into the atmosphere. § According to Galimov (1985, 2004) the great bulk (95%) of the metal core was formed during the first 100 Ma after the accretion of the planet.
Sources of hydrogen on early Earth § the degassing of the mantle that released the neutral or slightly acidic fluids saturated with H 2, CH 4, H 2 S, and CO 2; § the serpentinization, reaction of the rocks, rich with olivine and pyroxene, with water. § photolysis of water by UV light § radiolysis, radiation-induced dissociation of H 2 O (background radiation on early Earth could be much higher than at present, mostly due to the decay of the short-lived isotopes.
Serpentinization — the reaction of olivine- and pyroxene-rich rocks with water at temperature 200 -400°С — produces magnetite, hydroxide, and serpentine minerals, and liberates molecular hydrogen, a source of energy and electrons that can be readily utilized by a broad array of chemosynthetic organisms. Schulte et al. , 2006
Schulte et al. , 2006 Serpentinization: olivine and pyroxene are altered into serpentine minerals: Fe 2 Si. O 4 + 5 Mg 2 Si. O 4 + 9 H 2 O 3 Mg 3 Si 2 O 5(OH)4 + Mg(OH)2 + 2 Fe(OH)2. (1) fayalite + forsterite + water serpentine + brucite + iron hydroxide where fayalite and forsterite are the olivine solidsolution end-members, and Mg 2 Si. O 4 + Mg. Si. O 3 + 2 H 2 O Mg 3 Si 2 O 5(OH)4 (2) forsterite + pyroxene + water serpentine The reduced iron from the fayalite component of olivine (Reaction 1) may then be Oxidized to magnetite through the reduction of water to molecular hydrogen through the reaction 3 Fe(OH)2 Fe 3 O 4 + 2 H 2 O + H 2 iron hydroxide magnetite + water + hydrogen (3)
Sources of hydrogen on early Earth § Calculations by Tian F. et al. (2005) demonstrate that hydrogen could make up to 30% of ancient atmosphere. § The concentration of H 2 in the prebiotic atmosphere was 3 -4 orders of magnitude higher than at present (Hoehler, 2005).
Sources of hydrogen on early Earth § Concentration of hydrogen could be even greater among the dissolved gases in the fluids going through the rocks and sediments due to slow migration of the fluids. § Abundance of hydrogen gave an easy access to the protons and electrons, the very motor of the cellular energy machine.
Hydrogenases These enzymes catalyze the simplest of chemical reactions: the reversible reductive formation of hydrogen from protons and electrons: 2 H+ + 2 e- H 2
Ragsdale, 2004 The water-gas shift reaction, an organometallic reaction sequence that is catalysed by Fe-Ni dehydrogenase, may also be one of the oldest on Earth.
The structure of Cp. I hydrogenase from Clostridium pasteurianum with its naturally embedded metallo-clusters. Arrows show the pathways for the electrons, hydrogen ions, and the hydrogen product to and from the active H-cluster.
Iron hydrogenases: Prosthetic group features http: //metallo. scripps. edu/PROMISE/MAIN. html
Nickel-iron hydrogenases Prosthetic groups in large subunits Prosthetic groups in small subunits
Similarity of the molecular structures: a - mineral greigite (Fe 5 Ni. S 8), b -thiocubane unite of the ferredoxine protein, c - the cuboidal complex in the active site of the enzyme acetyl-Co. A synthasa/carbon monoxide dehydrogenase (shown simplified), and d - A-cluster of the latter. Atoms: Fe – red, Ni – green, S – yellow, C – grey, N – blue. R – links through sulfur to the reminder of the protein. After Russell, 2006
Metals in The Early Oceans Abundant: Fe 2+, Ni 2+, Mn 2+, Mo 6+, V 4+, W 6+ etc. (Frausto da Silva& Williams, 1997) HOWEVER: The chemical and physical parameters of biosphere irreversibly departed from the initial conditions. MAJOR CHANGES: Global temperature decline, oxygenation, and decreasing availability of hydrogen and some metals.
Geochemical evolution of magmatism between 3. 5 and 2. 7 Ga: At the early stage of their development, tholeiitic magmas were considerably enriched in chalcophile and siderophile elements Fe, Mg, Cr, Ni, Co, V, Cu, and Zn. At the next stage, calc-alkaline volcanics of greenstone belts and syntectonic TTG granitoids were enriched in lithophile elements Rb, Cs, Ba, Th, U, Pb, Nb, La, Sr, Be and others (Samsonov, Larionova, 2006). Lead isotope compositions of tungsten-bearing minerals occurrences worldwide indicate that tungsten (W) of crustal mineralization was mainly supplied by the mantle between 3. 0 and 2. 4 Ga (Chiaradia, 2003).
Ni Konhauser et al. , 2009 A decline of dissolved Ni concentrations in sea water through time reduced the bioproduction of methane and affected other kinds of hydrogen metabolism
Atmosphere history (Kasting, Pavlov, 2001) Availability change for some elements in the ocean due to its oxygenation (Williams, Frausto da Silva, 1996)
Range of MIF of sulphur over time. The great oxidation event occurred ~2. 45 billion years ago. The pink bar shows the range of variability in Δ 33 S that is due to mass-dependent effects, indicating only small variations during the past 2. 32 billion years (Kump, 2008).
Glass et al. , 2009
Solubility of some metal hydroxides and metal sulfides in modern ocean (Di Toro et al. , 2001)
Mn Fe Kirschvink J. L. , 2004. Largest ore deposits of Mn and Fe in Early Proterozoic was causes by active oxygenation of ocean water due to the photosynthesis of cyanobacteria and increasing circulation of cooling waters.
Iron formation: the sedimentary product of a complex interplay among mantle, tectonic, oceanic, and biospheric processes Bekker et al. , 2010
The age distribution of relative volumes of juvenile continental crust (Condie, 2005), and of crystallization ages for over 7000 detrital zircons (Campbell and Allen, 2008). The peaks in the zircon crystallization ages are similar to the ages of supercontinents. The crust generation rate curve illustrates a model in which the volume of new crust generated decreases with decreasing age. Hawkesworth et al. , 2010
Two major systems of nutrirent supply in the ocean ecosystem § First, mid-oceanic ridge where circulating seawater transports nutrients from MORB (mid oceanic ridge basalt) crust § Second, the Earth's surface erosion that is 12 probably 10 times more powerful than the first nutrient supply system (Maruyama et al. , 2013)
A)Temporal trends in Mo concentrations in anoxic organic rich black shales. B) Temporal trends in Mo/TOC ratios in anoxic black shales (Wallis, 2006; Och, 2011).
A) A compilation of Vanadium concentrations in black shales B) V/TOC ratios greatly increase across the Precambrian–Cambrian boundary whereby the highest values (exceeding 1000) are exclusively from black shales sampled in South China (Och, Shields-Zhou, 2012)
Mn The chemistry of manganese ores through time: a signal of increasing diversity of Earth-surface environments (Maynard, 2010)
METAL COFACTORS OF ENZYMES Hypothetical sequence of the incorporation of the metals into the enzymatic evolution in the early history of the biosphere (Fedonkin, 2003, 2005). Oxygenation of the environments dramatically reduced availability of some metals (such as W, V, Ni, Fe), while others (such as Mo, Cu, Zn) became more readily available. Replacement of the unavailable metals with those available seems to be a major way in early evolution of enzymes. Geological Time
H 2 -related evolution § All sources of hydrogen declined in time. § The subsequent evolution of life was in a great extent driven by the competition for access to hydrogen. § Decline of the primary sources of hydrogen made life to switch for the hydrogen compounds such as H 2 S, CH 4, NH 3, and at last, H 2 O in the oxygenic photosynthesis.
H 2 -related evolution > 4 Ga ago The length of the thick arrows indicates the amount of energy released. Time 2. 7 Ga ago ? (Lane, 2006)
H 2 -related evolution § By-products of the biochemical reactions related to the hydrogen uptake could be the factor of historical change in the atmosphere chemistry, in particular, the rising content of nitrogen and oxygen.
The biogeochemical cycles of macroelements (C, N, P and Si) are modulated by trace metals (J. T. Cullen et al. , 1995)
Biological consequences Decreasing availability of hydrogen and some metals as well as the oxygenation of the habitats in the Archean-Proterozoic oceans were the major driving forces for evolution of the metabolic pathways and biological complexity of the cell.
Biological consequences § Compartmentalization of internal environment in the cell (membranes, vesicles, organelles) that keeps the Archean biochemistry intact § Mechanisms of scavenging, concentration and storage of the metals internally § Integration of the complementary metabolic types in the cell
Biological consequences § Symbiosis of the prokaryotic cells mutually dependent on each others' waste products gave the rise of the eukaryotes § Increasing rates of the biological recycling of nutrients in the ecosystem § Shift towards the heterotrophy because of need to acquire nutrients in chemically impoverished environment
Modern approach to the symbiogenesis problem follows the principles of ecosystem ecology and syntrophy: Symbiogenetic origin of the eukaryotic cell was a long process of a functional optimization and structural miniaturization of the primary prokaryotic ecosystems in response to the irreversible change of the environmental parameters.
O 2 utilizing gene birth over time (David and Alm, 2010).
David and Alm, 2010
Acknowledgements: Program of the Presidium of the Russian Academy of Sciences (‘‘Problem of the Origin of the Earth’s Biosphere and Its Evolution’’), Russian Foundation for Basic Research Thank you for your attention!
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