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.

Armen Y Mulkidjanian,Michael Y Galperin

doi:10.1186/1745-6150-4-27

Abstract

BackgroundThe accompanying article (A.Y. Mulkidjanian, Biology Direct 4:26) puts forward a detailed hypothesis on the role of zinc sulfide (ZnS) in the origin of life on Earth. The hypothesis suggests that life emerged within compartmentalized, photosynthesizing ZnS formations of hydrothermal origin (the Zn world), assembled in sub-aerial settings on the surface of the primeval Earth.ResultsIf 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.ConclusionThe 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. Further work will be needed to provide details on the life within these communities and to elucidate the primordial (bio)chemical reactions.ReviewersThis article was reviewed by Arcady Mushegian, Eugene Koonin, and Patrick Forterre. For the full reviews, please go to the Reviewers' reports section.

Highlights

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
The Zn world hypothesis is based on the three key premises, namely (i) the experimentally demonstrated ability of zinc sulfide (ZnS) crystals and nanoparticles to photoreduce CO2 with a high quantum yield [96,99,100,101,102,103,110], (ii) the need of metal-rich hydrothermal settings for the emergence of first organisms [45,47,62,63,65,66,67,111,112,113,114] and the frequent coating of such settings by ZnS [104,115117], and (iii) the unique photostablity of polynucleotides that could imply their emergence in the presence of UV light as a selective factor [33,78,118,119,120,121]
This figure shows that if we focus on the photosynthesis by ZnS nanoparticles, even the sizes of the abiogenic and biogenic photochemical devices match each other

Summary

Introduction

The hypothesis suggests that life emerged within compartmentalized, photosynthesizing ZnS formations of hydrothermal origin (the Zn world), assembled in sub-aerial settings on the surface of the primeval Earth. The "replication first" paradigm implies that formation of the first replicating entities preceded the origin of metabolism. This concept has grown from the so-called heterotrophic theory of abiogenesis that can be traced to Oparin, who had suggested that formation of complex proteinaceous complexes could proceed spontaneously under the conditions of reducing primordial atmosphere [11,12]. Oligonucleotides of up to 30–50 units could be obtained in abiogenic systems from chemically activated monomers (e.g. nucleoside 5'-phosphorimidazolides [36]) when either polynucleotide chains [36,37,38] or mineral surfaces [39,40,41,42,43,44] were used as polymerization templates

Results

Discussion

Conclusion