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

Abstract

Background: The 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.

Results: 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.

Conclusion: 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. Further work will be needed to provide details on the life within these communities and to elucidate the primordial (bio)chemical reactions.

Reviewers: This article was reviewed by Arcady Mushegian, Eugene Koonin, and Patrick Forterre. For the full reviews, please go to the Reviewers' reports section.

Figure 1

Energy diagrams for FeS, ZnS, and MnS as potential donors of photo-excited electrons (left column) and for the biologically relevant electron acceptors (right column). The Highest Occupied Molecular Orbital (HOMO) level in the valence bands of each semiconductor is shown by a darker color than the respective Lowest Unoccupied Molecular Orbital (LUMO) level in the conduction band. The picture is based on data from references [72,99,122,262,264].

Figure 2

A schematic representation of interweaved haloes made of porous ZnS/MnS (shown as aggregates of grey spheres) around the sub-aerial, hydrothermal hot springs. These networks are proposed to have served as the Earth's first biotopes (see the text and the accompanying article [97]). The picture uses data from refs. [66,105,115,117,260,261].

Figure 3

A comparison of energy diagrams for a photosynthesizing ZnS nanoparticle (left panel, the picture is taken from the accompanying article [97] and is based on references [98,103,122]) and a bacterial photochemical reaction center (right panel, a primitive, sulfide-oxidizing reaction center complex of green sulfur bacteria [276,277] is shown schematically as an example).