Manganese-oxidizing photosynthesis before the rise of cyanobacteria

Johnson, J. E.; Webb, Samuel M.; Thomas, Katherine; Ono, Shuhei; Kirschvink, Joseph L.; Fischer, Woodward W.

doi:10.1073/pnas.1305530110

Cited by 214 publications

(158 citation statements)

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“…and that may have been precursors to biological water oxidation catalysts (14). The evidence we provide for δ-MnO 2 photoreduction in the absence of organic electron donors establishes this pathway as an important component of the Mn cycle.…”

Section: Environmental Implicationsmentioning

confidence: 53%

“…Experimental studies on the photochemical cycling of Mn have incorporated natural organic ligands that can enhance metal reduction via multiple pathways (5,8,9). These studies have identified aqueous Mn(II) as a reaction end product but have not investigated the fate of Mn(III) in the dissolution process, even though Mn(III) is a necessary intermediate in the reduction of Mn(IV) to Mn(II) (10) and an important component of environmental systems (11).The photochemistry of Mn also enables solar energy harvesting (12) and water oxidation catalysis in synthetic and biological systems (3,13,14). Mn-based cluster compounds (15, 16) and disordered birnessite nanoparticles (2) can exhibit analogous reactivity to the water-oxidizing center of photosystem II.…”

mentioning

confidence: 99%

“…The photochemistry of Mn also enables solar energy harvesting (12) and water oxidation catalysis in synthetic and biological systems (3,13,14). Mn-based cluster compounds (15, 16) and disordered birnessite nanoparticles (2) can exhibit analogous reactivity to the water-oxidizing center of photosystem II.…”

mentioning

confidence: 99%

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Rate and mechanism of the photoreduction of birnessite (MnO ₂ ) nanosheets

Marafatto

Strader

Gonzalez-Holguera

et al. 2015

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

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The photoreductive dissolution of Mn(IV) oxide minerals in sunlit aquatic environments couples the Mn cycle to the oxidation of organic matter and fate of trace elements associated with Mn oxides, but the intrinsic rate and mechanism of mineral dissolution in the absence of organic electron donors is unknown. We investigated the photoreduction of δ-MnO 2 nanosheets at pH 6.5 with Na or Ca as the interlayer cation under 400-nm light irradiation and quantified the yield and timescales of Mn(III) production. Our study of transient intermediate states using time-resolved optical and X-ray absorption spectroscopy showed key roles for chemically distinct Mn(III) species. The reaction pathway involves (i) formation of Jahn-Teller distorted Mn(III) sites in the octahedral sheet within 0.6 ps of photoexcitation; (ii) Mn(III) migration into the interlayer within 600 ps; and (iii) increased nanosheet stacking. We propose that irreversible Mn reduction is coupled to hole-scavenging by surface water molecules or hydroxyl groups, with associated radical formation. This work demonstrates the importance of direct MnO 2 photoreduction in environmental processes and provides a framework to test new hypotheses regarding the role of organic molecules and metal species in photochemical reactions with Mn oxide phases. The timescales for the production and evolution of Mn(III) species and a catalytic role for interlayer Ca 2+ identified here from spectroscopic measurements can also guide the design of efficient Mn-based catalysts for water oxidation.manganese oxide | photoreduction | band-gap excitation | pump-probe spectroscopy | water oxidation M anganese is a key element in environmental processes, catalytic materials, and biological systems due to its rich redox chemistry and ability to form species with a high oxidizing potential. Photochemical processes can enhance significantly the cycling of Mn between the +4, +3, and +2 valence states (1-3). Photoreduction of Mn(IV) is the first step in the reductive dissolution of birnessite minerals in the euphotic zone of marine and lacustrine environments (4-6). This process couples the biogeochemical cycle of Mn to the redox cycling of carbon and trace metals associated with Mn oxide phases. In addition, the greater role of Mn(IV) photoreduction relative to microbial Mn(II) oxidation leads to the predominance of dissolved over particulate Mn in the photic zone of natural waters (1). Thermodynamic calculations predict that direct photoexcitation of Mn oxides in water by visible light will lead to net metal reduction over a wide range of environmentally relevant pH values (7). However, experimental evidence of direct photoexcitation of MnO 2 and subsequent photoreduction of Mn(IV) in the absence of organic electron donors is currently lacking. Experimental studies on the photochemical cycling of Mn have incorporated natural organic ligands that can enhance metal reduction via multiple pathways (5,8,9). These studies have identified aqueous Mn(II) as a reaction end product but have not inve...

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Section: Environmental Implicationsmentioning

confidence: 53%

mentioning

confidence: 99%

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Rate and mechanism of the photoreduction of birnessite (MnO ₂ ) nanosheets

Marafatto

Strader

Gonzalez-Holguera

et al. 2015

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

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“…Therefore, it is possible that these mutational enrichment periods correspond to the adaptation of key oxygen‐sensitive components of Rubisco prior to the GOE (Anbar et al., 2007; Planavsky, Reinhard, et al., 2014). This would further indicate that calibrating the Rubisco tree to the appearance of cyanobacterial fossils or the GOE itself must be undertaken with care, given the possibility that stem group oxygenic photosynthetic organisms could have existed long before the appearance of recognizable Cyanobacteria in the fossil record (Blankenship & Hartman, 1998; Cardona, 2016; Fischer, Hemp, & Johnson, 2016; Johnson et al., 2013). Phenotypic characterization of expressed and purified ancestral forms of Rubisco may provide a biochemical and physiological basis for correlating the specific site mutations between the Anc.…”

Section: Discussionmentioning

confidence: 99%

Constraining the timing of the Great Oxidation Event within the Rubisco phylogenetic tree

et al. 2017

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Ribulose 1,5‐bisphosphate (RuBP) carboxylase/oxygenase (RuBisCO, or Rubisco) catalyzes a key reaction by which inorganic carbon is converted into organic carbon in the metabolism of many aerobic and anaerobic organisms. Across the broader Rubisco protein family, homologs exhibit diverse biochemical characteristics and metabolic functions, but the evolutionary origins of this diversity are unclear. Evidence of the timing of Rubisco family emergence and diversification of its different forms has been obscured by a meager paleontological record of early Earth biota, their subcellular physiology and metabolic components. Here, we use computational models to reconstruct a Rubisco family phylogenetic tree, ancestral amino acid sequences at branching points on the tree, and protein structures for several key ancestors. Analysis of historic substitutions with respect to their structural locations shows that there were distinct periods of amino acid substitution enrichment above background levels near and within its oxygen‐sensitive active site and subunit interfaces over the divergence between Form III (associated with anoxia) and Form I (associated with oxia) groups in its evolutionary history. One possible interpretation is that these periods of substitutional enrichment are coincident with oxidative stress exerted by the rise of oxygenic photosynthesis in the Precambrian era. Our interpretation implies that the periods of Rubisco substitutional enrichment inferred near the transition from anaerobic Form III to aerobic Form I ancestral sequences predate the acquisition of Rubisco by fully derived cyanobacterial (i.e., dual photosystem‐bearing, oxygen‐evolving) clades. The partitioning of extant lineages at high clade levels within our Rubisco phylogeny indicates that horizontal transfer of Rubisco is a relatively infrequent event. Therefore, it is possible that the mutational enrichment periods between the Form III and Form I common ancestral sequences correspond to the adaptation of key oxygen‐sensitive components of Rubisco prior to, or coincident with, the Great Oxidation Event.

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“…The final step would have been the transition from oxidizing environmental Mn II (possibly with the help of uv) one at a time as a substrate, to oxidizing a portable Mn III reserve in the cluster of the water splitting apparatus at the periplasmic side of PSII [69]. Recently, geochemical evidence was reported that is in agreement with both that scenario [70] and the model of Dismukes and colleagues [65,71], which also suggested a role for environmental Mn II while also pointing out a role for high CO 2 in the origin of water splitting. The Mn-oxidizing abilities of RCII from Rhodobacter [72] are also compatible with the models deriving water splitting complex from environmental Mn II .…”

Section: Plastid Origin and The Origin Of Oxygenic Photosynthesismentioning

confidence: 60%

Plastid origin: who, when and why?

Roettger

Zimorski

et al. 2014

Acta Soc Bot Pol

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Plastid origin: 110 years since MereschkowskyPlastids are eukaryotic metabolic compartments responsible for photosynthesis [1] and a variety of metabolic functions including the biosynthesis of amino acids [2], nucleotides [3], lipids [4], and cofactors [5]. The importance of plastids to photosynthetic lineages of eukaryotes cannot be overstated. In 1905, Mereschkowsky proposed a fully articulated version of endosymbiotic theory positing that plastids originated from cyanobacteria that came to reside as symbionts in eukaryotic cells [6,7]. The theory did not make its way into mainstream biological thinking until it was revived in a synthesis by Margulis [8,9] that also incorporated Wallin's [10] -and Paul Portier's (published in French, cited in Sapp [11]) -ideas about endosymbiotic theory for mitochondrial origin, yet adorned by Margulis' own suggestion of a spirochaete origin of flagella. The spirochaete story never took hold, leaving endosymbiotic theory with three main players: the plastid, the mitochondrion, and its host, which is now understood to be an archaeon [12]. Well into the 1970s, resistance to the concept of endosymbiosis for the origin of plastids (and mitochondria) was stiff [13][14][15].With the availability of protein and DNA sequences, of which Mereschkowsky knew nothing, strong evidence had accumulated by the early 1980s that plastids originated through endosymbiosis from cyanobacteria, rather than autogenously [16]. However, there have been recurrent suggestions, starting with Mereschkowsky [6] and tracing into the 1970's [17], that there were several independent origins of plastids from cyanobacteria. Today it is widely, but not universally [18,19], accepted that plastids had a single origin. The strongest evidence for that view is that the protein import machinery, a good marker for endosymbiotic events [20], in the three lineages of Archaeplastida -eukaryotes with primary plastids [21] -consists of homologous host-originated components [22][23][24], which would not be the case had plastids in those lineages arisen from independent cyanobacterial symbioses.Genomics has enriched our understanding of plastid origin. We now know that the plastid genome has undergone extreme reduction while leaving its imprints in the nuclear genome through endosymbiotic gene transfer [25,26] and that plastids have spread across eukaryotes through symbiosis and become secondary and tertiary plastids [27]. Genomic data also supports the case for a single plastid origin. Despite some concerns about incomplete sampling and phylogenetic artifacts [18], recent analyses from different groups, incorporating improved phylogenetic algorithms and sampling of cyanobacteria, provide two lines of evidence, in addition to * Corresponding author. Email: bill@hhu.deHandling Editor: Andrzej Bodył INVITED REVIEW Acta Soc Bot Pol 83(4): 281-289 DOI: 10.5586/asbp.2014.045 Received: 2014-11-20 Accepted: 2014-12-04 Published electronically: 2014 Plastid origin: who, when and why?Chuan Ku, Mayo Roettger, Verena Zimorski, Shijulal...

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Manganese-oxidizing photosynthesis before the rise of cyanobacteria

Cited by 214 publications

References 59 publications

Rate and mechanism of the photoreduction of birnessite (MnO ₂ ) nanosheets

Rate and mechanism of the photoreduction of birnessite (MnO ₂ ) nanosheets

Constraining the timing of the Great Oxidation Event within the Rubisco phylogenetic tree

Plastid origin: who, when and why?

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Manganese-oxidizing photosynthesis before the rise of cyanobacteria

Cited by 214 publications

References 59 publications

Rate and mechanism of the photoreduction of birnessite (MnO 2 ) nanosheets

Rate and mechanism of the photoreduction of birnessite (MnO 2 ) nanosheets

Constraining the timing of the Great Oxidation Event within the Rubisco phylogenetic tree

Plastid origin: who, when and why?

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Rate and mechanism of the photoreduction of birnessite (MnO ₂ ) nanosheets

Rate and mechanism of the photoreduction of birnessite (MnO ₂ ) nanosheets