The evolution of Photosystem II: insights into the past and future

Williamson, Adele Kim; Conlan, Brendon; Hillier, Warwick; Wydrzynski, Tom

doi:10.1007/s11120-010-9559-3

Cited by 58 publications

(42 citation statements)

References 126 publications

(143 reference statements)

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“…Given the complex nature of the four-electron water oxidation process, the development from anoxygenic to oxygenic photosynthesis has been proposed to be enabled by a catalytic intermediate containing a Mn cofactor (30)(31)(32)(33)(34)(35)(36)(37). A complex mechanism has been developed in cyanobacteria and plants to recover from the damage that occurs due to the presence of the highly oxidizing primary donor (38).…”

Section: Resultsmentioning

confidence: 99%

Light-driven oxygen production from superoxide by Mn-binding bacterial reaction centers

Allen

Olson

Oyala

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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One of the outstanding questions concerning the early Earth is how ancient phototrophs made the evolutionary transition from anoxygenic to oxygenic photosynthesis, which resulted in a substantial increase in the amount of oxygen in the atmosphere. We have previously demonstrated that reaction centers from anoxygenic photosynthetic bacteria can be modified to bind a redoxactive Mn cofactor, thus gaining a key functional feature of photosystem II, which contains the site for water oxidation in cyanobacteria, algae, and plants [Thielges M, et al. (2005) Biochemistry 44:7389-7394]. In this paper, the Mn-binding reaction centers are shown to have a light-driven enzymatic function; namely, the ability to convert superoxide into molecular oxygen. This activity has a relatively high efficiency with a k cat of approximately 1 s −1 that is significantly larger than typically observed for designed enzymes, and a K m of 35-40 μM that is comparable to the value of 50 μM for Mn-superoxide dismutase, which catalyzes a similar reaction. Unlike wild-type reaction centers, the highly oxidizing reaction centers are not stable in the light unless they have a bound Mn. The stability and enzymatic ability of this type of Mn-binding reaction centers would have provided primitive phototrophs with an environmental advantage before the evolution of organisms with a more complex Mn 4 Ca cluster needed to perform the multielectron reactions required to oxidize water. I n photosynthesis, the primary conversion of light energy into chemical energy is performed by the evolutionarily related pigment-protein complexes, reaction centers in purple and green bacteria and photosystems I and II in cyanobacteria, algae, and plants (1, 2). In the purple bacterium Rhodobacter sphaeroides, the reaction center is composed of two core protein subunits, identified as the L and M subunits, which each have five transmembrane helices and are related by an approximate twofold symmetry axis. These protein subunits surround the cofactors, which are arranged in two branches with the same twofold symmetry axis. In addition, reaction centers have a third subunit, identified as the H subunit, which has a single transmembrane helix and a large extramembrane domain. Light excitation of the primary electron donor P, a bacteriochlorophyll dimer, is followed by electron transfer steps predominately along one branch of cofactors to Q A , the primary quinone, and then to Q B , the secondary quinone, forming the charge-separated state P þ· Q B −· . In the cell, the oxidized bacteriochlorophyll dimer is reduced by a water-soluble cytochrome c 2 allowing a second electron transfer to Q B in a proton-coupled process. The electrons and protons associated with the oxidized cytochrome c 2 and reduced quinone (quinol) are coupled to the cytochrome bc 1 complex resulting in a net proton transfer across the cell membrane that is used to create energy-rich compounds. Photosystem II has a significant structural homology to this type of reaction center, with a core of two protein subu...

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Section: Resultsmentioning

confidence: 99%

Light-driven oxygen production from superoxide by Mn-binding bacterial reaction centers

Allen

Olson

Oyala

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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“…water oxidation | X-ray absorption spectroscopy | Great Oxidation Event | pyrite T he rise of atmospheric oxygen ∼2.4 Ga (1, 2) is the most marked environmental change in Earth history, and this transition ultimately stems from a major biological innovationthe evolution of oxygenic photosynthesis (3,4). Several biochemical attributes were invented to facilitate this metabolism, including a core photosystem pigment with a higher redox potential than other photosynthetic reaction centers (to enable the oxidation of water) and coupled photosystems.…”

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confidence: 99%

“…Furthermore, this process is not recapitulated during formation of the WOC today, which only requires soluble Mn(II) and light (15). During modern assembly of the WOC, no O 2 is evolved, but rather electrons are donated from divalent Mn to the photosystem to arrive at the basal oxidation state (S 0 ) of the water-oxidizing Mn(III) 3 Mn(IV) cluster (4,7). This mechanism of photoassembly offers a potential clue to the evolution of the WOC.…”

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confidence: 99%

Manganese-oxidizing photosynthesis before the rise of cyanobacteria

Johnson

Webb

Thomas

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

199

137

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The emergence of oxygen-producing (oxygenic) photosynthesis fundamentally transformed our planet; however, the processes that led to the evolution of biological water splitting have remained largely unknown. To illuminate this history, we examined the behavior of the ancient Mn cycle using newly obtained scientific drill cores through an early Paleoproterozoic succession (2.415 Ga) preserved in South Africa. These strata contain substantial Mn enrichments (up to ∼17 wt %) well before those associated with the rise of oxygen such as the ∼2.2 Ga Kalahari Mn deposit. Using microscale X-ray spectroscopic techniques coupled to optical and electron microscopy and carbon isotope ratios, we demonstrate that the Mn is hosted exclusively in carbonate mineral phases derived from reduction of Mn oxides during diagenesis of primary sediments. Additional observations of independent proxies for O 2 -multiple S isotopes (measured by isotope-ratio mass spectrometry and secondary ion mass spectrometry) and redoxsensitive detrital grains-reveal that the original Mn-oxide phases were not produced by reactions with O 2 , which points to a different high-potential oxidant. These results show that the oxidative branch of the Mn cycle predates the rise of oxygen, and provide strong support for the hypothesis that the water-oxidizing complex of photosystem II evolved from a former transitional photosystem capable of single-electron oxidation reactions of Mn.water oxidation | X-ray absorption spectroscopy | Great Oxidation Event | pyrite

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“…It is clear, however, that the manganese/calcium oxide cluster on the luminal side of photosystem II, and the four light driven electron transfer reactions leading to the production of each O 2 molecule is unique in biology. The structure and evolution of PSII, is discussed by Hiller and his group (Williamson et al 2010), and the timing of the appearance of cyanobacteria in the fossil record is discussed by Schopf (2010). The latter examines the data for both morphological fossils (or ''cellular'' fossils) as well as molecular fossils and isotopic measurements.…”

Section: Biological Contingenciesmentioning

confidence: 99%

The biological and geological contingencies for the rise of oxygen on Earth

Falkowski

2010

Photosynth Res

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The evolution of Photosystem II: insights into the past and future

Cited by 58 publications

References 126 publications

Light-driven oxygen production from superoxide by Mn-binding bacterial reaction centers

Light-driven oxygen production from superoxide by Mn-binding bacterial reaction centers

Manganese-oxidizing photosynthesis before the rise of cyanobacteria

The biological and geological contingencies for the rise of oxygen on Earth

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