The origin of atmospheric oxygen on Earth: The innovation of oxygenic photosynthesis

被引:240
作者
Dismukes, GC [1 ]
Klimov, VV
Baranov, SV
Kozlov, YN
DasGupta, J
Tyryshkin, A
机构
[1] Princeton Univ, Dept Chem, Hoyt Lab, Princeton, NJ 08544 USA
[2] Russian Acad Sci, Inst Basic Biol Problems, Pushchino 142290, Moscow Region, Russia
关键词
bicarbonate; carbon dioxide; cyanobacteria; evolution; manganese;
D O I
10.1073/pnas.061514798
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
The evolution of O-2-producing cyanobacteria that use water as terminal reductant transformed Earth's atmosphere to one suitable for the evolution of aerobic metabolism and complex life. The innovation of water oxidation freed photosynthesis to invade new environments and visibly changed the face of the Earth. We offer a new hypothesis for how this process evolved, which identifies two critical roles for carbon dioxide in the Archean period. First, we present a thermodynamic analysis showing that bicarbonate (formed by dissolution of CO2) is a more efficient alternative substrate than water for O-2 production by oxygenic phototrophs. This analysis clarifies the origin of the long debated "bicarbonate effect" on photosynthetic O-2 production. We propose that bicarbonate was the thermodynamically preferred reductant before water in the evolution of oxygenic photosynthesis. Second, we have examined the speciation of manganese(II) and bicarbonate in water, and find that they form Mn-bicarbonate clusters as the major species under conditions that model the chemistry of the Archean sea. These clusters have been found to be highly efficient precursors for the assembly of the tetramanganese-oxide core of the water-oxidizing enzyme during biogenesis. We show that these clusters can be oxidized at electrochemical potentials that are accessible to anoxygenic phototrophs and thus the most likely building blocks for assembly of the first O-2 evolving photoreaction center, most likely originating from green nonsulfur bacteria before the evolution of cyanobacteria.
引用
收藏
页码:2170 / 2175
页数:6
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