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Origin of life


Origin of first cells at terrestrial, anoxic geothermal fields [1]

Little is known about the conditions on the primitive Earth under which the first life forms and subsequently the first full-fledged cells have evolved. Life is most likely older than the oldest known rocks, so there is little chance to obtain clues on the earliest life habitats from the geological record. The best window into the earliest stages of life evolution might be provided by the conservation of the fundamental intracellular chemistry. All cells contain much more potassium, phosphate and transition metals than modern or reconstructed primeval oceans, lakes or rivers. Cells maintain ion gradients using sophisticated, energydependent membrane pumps that are embedded in elaborate ion-tight membranes. The first cells could possess neither membrane pumps nor ion-tight membranes, so the concentrations of small inorganic molecules and ions within protocells and in their environment would equilibrate. Hence, the inorganic ion composition of modern cells is expected to reflect the ion composition of the habitats of protocells.

Here, we attempted to reconstruct the ‘hatcheries’ of the first cells by combining geochemical analysis with a comparison of the inorganic ion requirements of the universal components of modern cells. These ubiquitous, and, by inference, primordial proteins and functional systems show affinity to and functional requirement for potassium, zinc, manganese, and phosphate. Thus, protocells must have evolved in habitats with a high K+/Na+ ratio and relatively high concentrations of transition metals and phosphorous compounds. Geochemical reconstruction shows that the ionic composition conducive to the origin of cells could not have existed in marine settings. In contrast, the inorganic ion composition of cells is compatible with emissions of vapor-dominated zones of inland geothermal systems. The geothermal vapor, which results from boiling of ascending geothermal fluids, can carry metal ions and is particularly enriched in potassium, carbon dioxide, ammonia, borate, as well as organic and phosphorous compounds. Geochemical considerations indicate that, in the absence of oxygen and at high carbon dioxide concentration, which were the salient features of the primordial atmosphere, the chemistry of basins at anoxic geothermal fields would resemble the internal milieu of modern cells and could be the most suitable hatcheries for the protocells. Under this scenario, the first cells are envisaged to have evolved in shallow ponds of condensed, cool geothermal vapor; these pools probably were lined with porous silicate minerals mixed with metal sulfides and enriched in potassium, zinc, and phosphorous compounds.

The major biochemical building blocks are derivatives of those molecules that preferably partition to the vapor phase upon the geothermal separation, namely simple carbonaceous and phosphorous compounds, ammonia, and sulfide. Hence, anoxic geothermal fields could also provide crucial chemical conditions for the emergence of life. As summarized in Table P1, primordial anoxic geothermal fields, as putative cradles of life, share all the advantages of the deep-sea hydrothermal vents that have been previously proposed in the same capacity, including the presence of inorganic compartments, versatile catalysts, and sources of organic matter. However, in contrast to deep-sea vents, terrestrial geothermal fields are conducive to condensation reactions and enable the involvement of solar light as an energy source and a selective factor that would have favored the accumulation of photostable nucleotides. Also in contrast to the fluids of deep-sea vents, the geothermal vapor is enriched in phosphorous and boron compounds that would be essential for the emergence of the first RNA-like oligomers.

Clearly, this model for the origin of cells – and probably of life itself – is consonant, at least conceptually, with Charles Darwin’s famous vision of a primordial ‘little warm pond’ as a cradle of life.

Kamchatka peninsula. Picture by Dr. Anna S. Karyagina

The hypothesis described here [1] implies that cells invaded the oceans at a relatively late, advanced stage of evolution, after elaborate, modern-type membranes capable of efficiently maintaining ion gradients have evolved. Thus, life might have originated in an isolated location and became a planetary phenomenon only after the colonization of the oceans. Further experimental exploration of models that mimic the conditions at terrestrial geothermal fields might shed more light on pre-cellular evolution.

Comparison of geological settings potentially conducive to the early evolution of life

Shallow sea waters Deep-sea hydrothermal vents Geothermal fields over the vapor dominated zones of inland geothermal systems (this work)
Stability/Duration > 109 years < 105 years ≥ 106 years
Steady thermodynamic driving force for continuous supply of organic precursors +

Solar UV photochemistry

+

Serpentinization

++

Solar UV photochemistry, hydrothermal alteration

Continuous supply of phosphorous compounds Unlikely –/+

less than 0.5 μM in hydrothermal fluids

+

Up to 1 mM in geothermal fluids

Opportunity for reagent concentration Modest

(wet/dry cycles in the tidal zones)

Modest

(concentration at mineral surfaces)

High

(concentration at mineral surfaces combined with wet/dry cycles, evaporation, freezing)

Selection force for abiotically formed (poly)nucleotides Solar UV light Solar UV light
Probability of spontaneous condensation reactions, polymerization and replication Modest

(only during wet/dry cycles in the tidal zones)

Low

High

(wet/dry cycles, evaporation, freezing, high amide levels)

Protection of the first replicators from the UV damage Modest

(low in the tidal zones)

High

(no UV light)

High

(protection by UV-absorbing metal sulfides and silica minerals)

Continuous supply of ammonia Unlikely + +
Continuous supply of reduced sulfurous compounds Unlikely + +
Enrichment in transition metals, in particular Zn + +
Enrichment in boron compounds +
K+/Na+ ratio > 1 +

Selection of first RNA-like polymers by UV light

A key event in the origin of life on this planet has been formation of self-replicating RNA-type molecules, which were complex enough to undergo a Darwinian-type evolution (origin of the "RNA world"). However, so far there has been no explanation of how the first RNA-like biopolymers could originate and survive on the primordial Earth.

As condensation of sugar phosphates and nitrogenous bases is thermodynamically unfavorable, these compounds, if ever formed, should have undergone rapid hydrolysis. Thus, formation of oligonucleotide-like structures could have happened only if and when these structures had some selective advantage over simpler compounds. It is well known that nitrogenous bases are powerful quenchers of UV quanta and effectively protect the pentose-phosphate backbones of RNA and DNA from UV cleavage. To check if such a protection could play a role in abiogenic evolution on the primordial Earth (in the absence of the UV-protecting ozone layer), we simulated, by using Monte Carlo approach, the formation of the first oligonucleotides under continuous UV illumination. The simulations confirmed that UV irradiation could have worked as a selective factor leading to a relative enrichment of the system in longer sugar-phosphate polymers carrying nitrogenous bases as UV-protectors. Partial funneling of the UV energy into the condensation reactions could provide a further boost for the oligomerization. These results suggest that accumulation of the first polynucleotides could be explained by their abiogenic selection as the most UV-resistant biopolymers [15].

ATP2

Schematic representation of the modeled reactions. The figure is taken taken from [15].

ATP2

Monte Carlo simulation of a sugar-phosphate polymerization reaction in the presence of nitrogenous bases and under UV-illumination. The figure is taken taken from [15].

Origin of life in the Zinc world

In a search for a plausible origin of life scenario we have tried to consider simultaneously various bioenergetic, physical, and geological constraints. The constrains could be satisfied by an evolutionary scenario that proposes that life on Earth emerged, powered by UV-rich solar radiation, at photosynthetically active porous edifices made of precipitated zinc sulfide (ZnS) similar to those found around modern deep-sea hydrothermal vents. Under the high pressure of the primeval, carbon dioxide-dominated atmosphere ZnS could precipitate at the surface of the first continents, within reach of solar light. It is suggested that the ZnS surfaces (1) used the solar radiation to drive carbon dioxide reduction, yielding the building blocks for the first biopolymers, (2) served as templates for the synthesis of longer biopolymers from simpler building blocks, and (3) prevented the first biopolymers from photo-dissociation, by absorbing from them the excess radiation. In addition, the UV light may have favoured the selective enrichment of photostable, RNA-like polymers.

The suggested "Zn world" scenario identifies the geological conditions under which photosynthesizing ZnS edifices of hydrothermal origin could emerge and persist on primordial Earth, includes a mechanism of the transient storage and utilization of solar light for the production of diverse organic compounds, and identifies the driving forces and selective factors that could have promoted the transition from the first simple, photostable polymers to more complex living organisms [12].

ATP2

Primeval ZnS-mediated photosynthesis in sub-aerial, illuminated settings. The figure is taken taken from [12]

As next, we have tried to validate the Zn world scenario. If life started within photosynthesizing ZnS compartments, it should have been able to evolve under the conditions of elevated levels of Zn2+ ions, byproducts of the ZnS-mediated photosynthesis. Therefore, the Zn world hypothesis leads to a set of testable predictions regarding the specific roles of Zn2+ ions in modern organisms, particularly in RNA and protein structures related to the procession of RNA and the "evolutionarily old" cellular functions. We checked these predictions using publicly available data and obtained evidence suggesting that the development of the primeval life forms up to the stage of the Last Universal Common Ancestor proceeded in zinc-rich settings. Testing of the hypothesis has revealed the possible supportive role of manganese sulfide in the primeval photosynthesis. In addition, we demonstrate the explanatory power of the Zn world concept by elucidating several points that so far remained without acceptable rationalization. In particular, this concept implies a new scenario for the separation of Bacteria and Archaea and the origin of Eukarya.

The ability of the Zn world hypothesis to generate non-trivial veritable predictions and explain previously obscure items gives credence to its key postulate that the development of the first life forms started within zinc-rich formations of hydrothermal origin and was driven by solar UV irradiation. This concept implies that the geochemical conditions conducive to the origin of life may have persisted only as long as the atmospheric CO2 pressure remained above ca. 10 bar. This work envisions the first Earth biotopes as photosynthesizing and habitable areas of porous ZnS and MnS precipitates around primeval hot springs [13].

ATP2

Proposed scenario for the evolution of membranes and membrane enzymes. The figure is taken taken from [10]

The scheme suggests the emergence of first replicating entities within honeycomb-like ZnS precipitates of hydrothermal origin. The evolution of membranes is shown as a transition from primitive, porous membranes that were leaky both to Na+ and H+ (dotted lines), via membranes that were Na+-tight but H+-leaky (dashed lines) to the modern-type membranes that are impermeable to both H+ and Na+ (solid lines). As the common ancestor of the F- and V-ATPases possessed a Na+-binding site (Mulkidjanian et al. 2008b; Mulkidjanian et al. 2009), the LUCA (regardless of whether it was a modern-type cell or a consortium that included replicating, membrane-surrounded entities) either had porous membranes so that the common ancestor of the F- and A/V ATPases operated as a polymer translocase, with Na+ ions performing a structural role, or had membranes that were tight to sodium but permeable to protons; in this case the LUCA could possess sodium energetic [9-13].

References

1. Mulkidjanian, A. Y., A. Y. Bychkov, D. V. Dibrova, M. Y. Galperin, and E. V. Koonin. 2012. Origin of first cells at terrestrial, anoxic geothermal fields. Proc Natl Acad Sci U S A, in press. (freely accessible at http://www.pnas.org/content/early/2012/02/08/1117774109)

2. Book: Origins of Life: The Primal Self-Organisation. Egel, H., D.-H. Lankenau, and A. Y. Mulkidjanian, editors, Springer, Heidelberg. 2011.

3. Mulkidjanian, A. Y., and D.-H. Lankenau. 2011. LUCA - letzter gemeinsamer Vorfahre allen Lebens. In Moleküle aus dem All? K. Al-Shamery, editor. Wiley-VCH-Verlag, Weinheim. 137-188. (Full text, pdf)

4. Mulkidjanian, A. Y., and H. J. Cleaves. 2011. Substrate. In Encyclopedia of Astrobiology. R. Amils, C. Quintanilla, H. J. Cleaves, W. M. Irvine, D. L. Pinti, and V. M., editors. Springer, Heidelberg. 1614.

5. Mulkidjanian, A. Y. 2011. Energetics of the first life. In Origins of Life: The Primal Self-Organisation. H. Egel, D.-H. Lankenau, and A. Y. Mulkidjanian, editors. Springer, Heidelberg. 1-33. (Full text, pdf)

6. Mulkidjanian, A. Y. 2011. Abiotic Photosynthesis. In Encyclopedia of Astrobiology. R. Amils, C. Quintanilla, H. J. Cleaves, W. M. Irvine, D. L. Pinti, and V. M., editors. Springer, Heidelberg. 1-3. (Full text, pdf)

7. Dibrova, D. V., K. S. Makarova, M. Y. Galperin, E. V. Koonin, and A. Y. Mulkidjanian. 2011. Comparative analysis of lipid biosynthesis in Archaea and Bacteria: What was the structure of first membrane lipids? In Proceedings of the International Moscow Conference on Computational Molecular Biology. Moscow State University, Moscow. 92-93. (Proceedings of MCCMB'11)

8. Dibrova, D. V., M. Y. Galperin, and A. Y. Mulkidjanian. 2011. Evolution of membrane bioenergetics. In Proceedings of the International Moscow Conference on Computational Molecular Biology. Moscow State University, Moscow. 241-242. (Proceedings of MCCMB'11)

9. Mulkidjanian, A.Y., M.Y. Galperin. 2010. On the abundance of zinc in the evolutionarily old protein domains (Letter). Proc. Natl. Acad. Sci. U.S.A, in press. (Full text, pdf).

10. Mulkidjanian, A.Y., M.Y. Galperin. 2010. Evolutionary origins of membrane proteins In: Structural Bioinformatics of Membrane Proteins (D. Frishman, Ed.), Springer, Wien, in press (Full text, pdf)

11. Mulkidjanian, A.Y., M.Y. Galperin, E.V. Koonin. 2009. Co-evolution of membranes and membrane proteins, Trends Biochem. Sci. 34, 206-215. (Full text, pdf)

12. Mulkidjanian, A.Y. 2009. On the origin of life in the Zinc World: 1. Photosynthetic, porous edifices built of hydrothermally precipitated zinc sulfide (ZnS) as cradles of life on Earth. Biol. Direct 4:26. (freely accessible at http://www.biology-direct.com/content/4/1/26)

13. Mulkidjanian, A.Y., M.Y. Galperin. 2009. On the origin of life in the Zinc World. 2. Validation of the hypothesis on the photosynthesizing zinc sulfide edifices as cradles of life on Earth Biol. Direct 4:27 (freely accessible at http://www.biology-direct.com/content/4/1/27)

14. Mulkidjanian, A.Y. and M. Y. Galperin. 2007. Physico-chemical and evolutionary constraints for the formation and selection of first biopolymers: Towards the consensus paradigm of the abiogenic origin of life. Chemistry and Biodiversity, 4:2003-2015.

15. Mulkidjanian, A.Y., D.A. Cherepanov, and M.Y. Galperin. 2003. Survival of the fittest before the beginning of life: selection of the first oligonucleotide-like polymers by UV light. BMC. Evol. Biol 3:12 (freely accessible athttp://www.biomedcentral.com/1471-2148/3/12)

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Letzte Änderung: 23.11.2014 Katrin Jahns