Links between hydrothermal environments, pyrophosphate, na(+), and early evolution

Abstract

The discovery that photosynthetic bacterial membrane-bound inorganic pyrophosphatase (PPase) catalyzed light-induced phosphorylation of orthophosphate (Pi) to pyrophosphate (PPi) and the capability of PPi to drive energy requiring dark reactions supported PPi as a possible early alternative to ATP. Like the proton-pumping ATPase, the corresponding membrane-bound PPase also is a H(+)-pump, and like the Na(+)-pumping ATPase, it can be a Na(+)-pump, both in archaeal and bacterial membranes. We suggest that PPi and Na(+) transport preceded ATP and H(+) transport in association with geochemistry of the Earth at the time of the origin and early evolution of life. Life may have started in connection with early plate tectonic processes coupled to alkaline hydrothermal activity. A hydrothermal environment in which Na(+) is abundant exists in sediment-starved subduction zones, like the Mariana forearc in the W Pacific Ocean. It is considered to mimic the Archean Earth. The forearc pore fluids have a pH up to 12.6, a Na(+)-concentration of 0.7 mol/kg seawater. PPi could have been formed during early subduction of oceanic lithosphere by dehydration of protonated orthophosphates. A key to PPi formation in these geological environments is a low local activity of water.

Fig. 1

Cartoon showing a cross section of oceanic lithosphere, extending from the spreading center to the subduction zone. Off-axis hydrothermal flow in the oceanic lithosphere causes partial oxidation of Fe(II) to Fe(III) and reduction of water to molecular hydrogen. Some Fe(II) and Ni(II) is reduced to native metals. CO₂ is reduced to CO and CH₄, while NO₃^- and NO₂^- may be reduced to NH₄⁺ and adsorbed on secondary minerals like smectite and zeolites. During early subduction the descending plate is heated and dehydrated. Adsorbed CO and CH₄ may react with NH₄⁺ and form HCN. The released fluid carrying HCN rises from an environment of relatively low pH into hydrated mantle rock of high pH. At the high pH HCN monomers may form oligomers as well as amino acids, purine bases, nucleosides and nucleotides due to phosphorylation by pyrophosphate (from Holm and Neubeck 2009)

Fig. 2

A novel evolutionary scheme for cation pumping through membranes