37 results found
Photosystem II is the water-oxidizing and O2 -evolving enzyme of photosynthesis. How and when this remarkable enzyme arose are fundamental questions in the history of life that have remained difficult to answer. Here, recent advances in our understanding of the origin andevolution of photosystem II are reviewed and discussed in detail. The evolution of photosystem II indicates that water oxidation originated early in the history of life, long before the diversification of cyanobacteria and other major groups of prokaryotes, challenging and transforming current paradigms on the evolution of photosynthesis. We show that photosystem II has remained virtually unchanged for well over three billion years, and yet the nonstop duplication process of the D1 subunit of photosystem II, which controls photochemistry and catalysis, has enabled the enzyme to become adaptable to variable environmental conditions, and even to innovate enzymatic functions beyond water oxidation. It is suggested that this evolvability can be exploited to develop novel light-powered enzymes with the capacity to carry out complex multi-step oxidative transformations for sustainable biocatalysis.
Gisriel CJ, Cardona Londono T, Bryant DA, et al., 2022, Molecular evolution of far-red light-acclimated photosystem II, Microorganisms, Vol: 10, Pages: 1-19, ISSN: 2076-2607
Cyanobacteria are major contributors to global carbon fixation and primarily use visible light (400−700 nm) to drive oxygenic photosynthesis. When shifted into environments where visible light is attenuated, a small, but highly diverse and widespread number of cyanobacteria can express modified pigments and paralogous versions of photosystem subunits and phycobiliproteins that confer far-red light (FRL) absorbance (700−800 nm), a process termed far-red light photoacclimation, or FaRLiP. During FaRLiP, alternate photosystem II (PSII) subunits enable the complex to bind chlorophylls d and f, which absorb at lower energy than chlorophyll a but still support water oxidation. How the FaRLiP response arose remains poorly studied. Here, we report ancestral sequence reconstruction and structure-based molecular evolutionary studies of the FRL-specific subunits of FRL-PSII. We show that the duplications leading to the origin of two PsbA (D1) paralogs required to make chlorophyll f and to bind chlorophyll d in water-splitting FRL-PSII are likely the first to have occurred prior to the diversification of extant cyanobacteria. These duplications were followed by those leading to alternative PsbC (CP43) and PsbD (D2) subunits, occurring early during the diversification of cyanobacteria, and culminating with those leading to PsbB (CP47) and PsbH paralogs coincident with the radiation of the major groups. We show that the origin of FRL-PSII required the accumulation of a relatively small number of amino acid changes and that the ancestral FRL-PSII likely contained a chlorophyll d molecule in the electron transfer chain, two chlorophyll f molecules in the antenna subunits at equivalent positions, and three chlorophyll a molecules whose site energies were altered. The results suggest a minimal model for engineering far-red light absorbance into plant PSII for biotechnological applications.
Antonaru LA, Cardona T, Larkum AWD, et al., 2022, Global distribution of a chlorophyll <i>f</i> cyanobacterial marker (vol 14, pg 2275, 2020), ISME JOURNAL, Vol: 16, Pages: 1680-1680, ISSN: 1751-7362
<jats:p>What if oxygenic photosynthesis is a primordial process with roots at the origin of life? What would the impact of this change in perspective be on our understanding of the early Earth and of the emergence and diversification of life? In here, I will examine some of the historical context of the study of the evolution of photosynthesis, which led to the consolidation of the current notion that the origin of anoxygenic photosynthesis occurred before the origin of oxygenic photosynthesis. I will show with a few examples how the mainstream view on the evolution of photosynthesis traces back to Oparin&rsquo;s &lsquo;primordial soup&rsquo; scenario for the origin of life, fuelled by the century-old perception that oxygenic photosynthesis is a plant rather than a bacterial trait. However, it has become more evident than ever before that the mainstream view is not supported by the evolution of the photosystems. In other words, the origin of biological water oxidation appears to be the seed from where photosynthesis sprout. Somewhat troubling and contrary to all predictions that derive from the mainstream view, photosystem II&mdash;the water-splitting and oxygen-evolving enzyme&mdash;shows features that are better explained if photochemical reaction centres originated during the establishment of oxygenic photosynthesis. An urgent revision of the evolution of photosynthesis procured to be free from biases of interpretations and presuppositions is strongly encouraged from all angles of the Life and Earth Sciences.</jats:p>
Saw JH, Cardona T, Montejano G, 2021, Complete genome sequencing of a novel gloeobacter species from a waterfall cave in Mexico., Genome Biology and Evolution, Vol: 13, Pages: 1-8, ISSN: 1759-6653
Only two complete genomes of the cyanobacterial genus Gloeobacter from two very different regions of the world currently exist. Here, we present the complete genome sequence of a third member of the genus isolated from a waterfall cave in Mexico. Analysis of the average nucleotide identities (ANIs) between published Gloeobacter genomes revealed that the complete genome of this new member is only 92.7% similar to Gloeobacter violaceus and therefore we determined it to be a new species. We propose to name this new species Gloeobacter morelensis after the location in Mexico where it was isolated. The complete genome consists of one circular chromosome (4,921,229 bp), one linear plasmid (172,328 bp), and one circular plasmid (8,839 bp). Its genome is the largest of all completely sequenced genomes of Gloeobacter species. Pangenomic comparisons revealed that G. morelensis encodes 759 genes not shared with other Gloeobacter species. Despite being more closely related to G. violaceus, it features an extremely divergent psbA gene encoding an atypical D1 core subunit of Photosystem II previously only found within the genome of Gloeobacter kilaueensis. In addition, we detected evidence of concerted evolution of psbA genes encoding identical D1 in all three Gloeobacter genomes, a characteristic that seems widespread in cyanobacteria and may therefore be traced back to their last common ancestor.
Gisriel C, Azai C, Cardona Londono T, 2021, Recent advances in the structural diversity of reaction centers, Photosynthesis Research, Vol: 149, Pages: 329-343, ISSN: 0166-8595
Photosynthetic reaction centers (RC) catalyze the conversion of light to chemical energy that supports life on Earth, but they exhibit substantial diversity among different phyla. This is exemplified in a recent structure of the RC from an anoxygenic green sulfur bacterium (GsbRC) which has characteristics that may challenge the canonical view of RC classification. The GsbRC structure is analyzed and compared with other RCs, and the observations reveal important but unstudied research directions that are vital for disentangling RC evolution and diversity. Namely, (1) common themes of electron donation implicate a Ca2+ site whose role is unknown; (2) a previously unidentified lipid molecule with unclear functional significance is involved in the axial ligation of a cofactor in the electron transfer chain; (3) the GsbRC features surprising structural similarities with the distantly-related photosystem II; and (4) a structural basis for energy quenching in the GsbRC can be gleaned that exemplifies the importance of how exposure to oxygen has shaped the evolution of RCs. The analysis highlights these novel avenues of research that are critical for revealing evolutionary relationships that underpin the great diversity observed in extant RCs.
Oliver T, Sanchez-Baracaldo P, Larkum AW, et al., 2021, Time-resolved comparative molecular evolution of oxygenic photosynthesis, BBA: Bioenergetics, Vol: 1862, Pages: 1-20, ISSN: 0005-2728
Oxygenic photosynthesis starts with the oxidation of water to O2, a light-driven reaction catalysed by photosystem II. Cyanobacteria are the only prokaryotes capable of water oxidation and therefore, it is assumed that the origin of oxygenic photosynthesis is a late innovation relative to the origin of life and bioenergetics. However, when exactly water oxidation originated remains an unanswered question. Here we use phylogenetic analysis to study a gene duplication event that is unique to photosystem II: the duplication that led to the evolution of the core antenna subunits CP43 and CP47. We compare the changes in the rates of evolution of this duplication with those of some of the oldest well-described events in the history of life: namely, the duplication leading to the Alpha and Beta subunits of the catalytic head of ATP synthase, and the divergence of archaeal and bacterial RNA polymerases and ribosomes. We also compare it with more recent events such as the duplication of Cyanobacteria-specific FtsH metalloprotease subunits and the radiation leading to Margulisbacteria, Sericytochromatia, Vampirovibrionia, and other clades containing anoxygenic phototrophs. We demonstrate that the ancestral core duplication of photosystem II exhibits patterns in the rates of protein evolution through geological time that are nearly identical to those of the ATP synthase, RNA polymerase, or the ribosome. Furthermore, we use ancestral sequence reconstruction in combination with comparative structural biology of photosystem subunits, to provide additional evidence supporting the premise that water oxidation had originated before the ancestral core duplications. Our work suggests that photosynthetic water oxidation originated closer to the origin of life and bioenergetics than can be documented based on phylogenetic or phylogenomic species trees alone.
Laura A A, Cardona Londono T, Larkum AWD, et al., 2020, Global distribution of a chlorophyll f cyanobacterial marker, The ISME Journal: multidisciplinary journal of microbial ecology, Vol: 14, Pages: 2275-2287, ISSN: 1751-7362
Some cyanobacteria use light outside the visible spectrum for oxygenic photosynthesis. The far-red light (FRL) region is made accessible through a complex acclimation process that involves the formation of new phycobilisomes and photosystems containing chlorophyll f. Diverse cyanobacteria ranging from unicellular to branched-filamentous forms show this response. These organisms have been isolated from shaded environments such as microbial mats, soil, rock, and stromatolites. However, the full spread of chlorophyll f-containing species in nature is still unknown. Currently, discovering new chlorophyll f cyanobacteria involves lengthy incubation times under selective far-red light. We have used a marker gene to detect chlorophyll f organisms in environmental samples and metagenomic data. This marker, apcE2, encodes a phycobilisome linker associated with FRL-photosynthesis. By focusing on a far-red motif within the sequence, degenerate PCR and BLAST searches can effectively discriminate against the normal chlorophyll a-associated apcE. Even short recovered sequences carry enough information for phylogenetic placement. Markers of chlorophyll f photosynthesis were found in metagenomic datasets from diverse environments around the globe, including cyanobacterial symbionts, hypersaline lakes, corals, and the Arctic/Antarctic regions. This additional information enabled higher phylogenetic resolution supporting the hypothesis that vertical descent, as opposed to horizontal gene transfer, is largely responsible for this phenotype’s distribution.
Oliver T, Sánchez-Baracaldo P, Larkum AW, et al., 2020, Time-resolved comparative molecular evolution of oxygenic photosynthesis
<jats:title>Abstract</jats:title><jats:p>Oxygenic photosynthesis starts with the oxidation of water to O<jats:sub>2</jats:sub>, a light-driven reaction catalysed by photosystem II. Cyanobacteria are the only prokaryotes capable of water oxidation and therefore, it is assumed that relative to the origin of life and bioenergetics, the origin of oxygenic photosynthesis is a late innovation. However, when exactly water oxidation originated remains an unanswered question. Here we use relaxed molecular clocks to compare one of the two ancestral core duplications that are unique to water-oxidizing photosystem II, that leading to CP43 and CP47, with some of the oldest well-described events in the history of life. Namely, the duplication leading to the Alpha and Beta subunits of the catalytic head of ATP synthase, and the divergence of archaeal and bacterial RNA polymerases and ribosomes. We also compare it with more recent events such as the duplication of cyanobacteria-specific FtsH metalloprotease subunits, of CP43 variants used in a variety of photoacclimation responses, and the speciation events leading to Margulisbacteria, Sericytochromatia, Vampirovibrionia, and other clades containing anoxygenic phototrophs. We demonstrate that the ancestral core duplication of photosystem II exhibits patterns in the rates of protein evolution through geological time that are nearly identical to those of the ATP synthase, RNA polymerase, or the ribosome. Furthermore, we use ancestral sequence reconstruction in combination with comparative structural biology of photosystem subunits, to provide additional evidence supporting the premise that water oxidation had originated before the ancestral core duplications. Our work suggests that photosynthetic water oxidation originated closer to the origin of life and bioenergetics than can be documented based on species trees alone.</jats:p>
Sánchez-Baracaldo P, Cardona Londono T, 2020, On the origin of oxygenic photosynthesis and Cyanobacteria, New Phytologist, Vol: 225, Pages: 1440-1446, ISSN: 0028-646X
Oxygenic phototrophs have played a fundamental role in Earth's history by enabling the rise of atmospheric oxygen (O2) and paving the way for animal evolution. Understanding the origin of oxygenic photosynthesis and Cyanobacteria are key when piecing together the events around Earth's oxygenation. It is likely that photosynthesis evolved within bacterial lineages that are not extant, so it can be challenging when studying the early history of photosynthesis. Recent genomic and molecular evolution studies have transformed our understanding about the evolution of photosynthetic reaction centres and the evolution of Cyanobacteria. The evidence reviewed here highlights some of the most recent advances on the origin of photosynthesis both at the genomic and gene family level.
Cardona Londono T, Rutherford AW, 2019, Evolution of photochemical reaction centres: more twists?, Trends in Plant Science, Vol: 24, Pages: 1008-1021, ISSN: 1878-4372
One of the earliest events in the molecular evolution of photosynthesis is the structural and functional specialisation of Type I (ferredoxin-reducing) and Type II (quinone-reducing) reaction centres. In this opinion article we point out that the homodimeric Type I reaction centre of Heliobacteria has a calcium-binding site with striking structural similarities to the Mn4CaO5 cluster of Photosystem II. These similarities indicate that most of the structural elements required to evolve water oxidation chemistry were present in the earliest reaction centres. We suggest that the divergence of Type I and Type II reaction centres was made possible by a drastic structural shift linked to a change in redox properties that coincided with or facilitated the origin of photosynthetic water oxidation.
Cardona Londono T, 2019, Thinking twice about the evolution of photosynthesis, Open Biology, Vol: 9, ISSN: 2046-2441
Sam Granick opened his seminal 1957 paper titled ‘Speculations on the origins and evolution of photosynthesis’ with the assertion that there is a constant urge in human beings to seek beginnings (I concur). This urge has led to an incessant stream of speculative ideas and debates on the evolution of photosynthesis that started in the first half of the twentieth century and shows no signs of abating. Some of these speculative ideas have become commonplace, are taken as fact, but find little support. Here, I review and scrutinize three widely accepted ideas that underpin the current study of the evolution of photosynthesis: first, that the photochemical reaction centres used in anoxygenic photosynthesis are more primitive than those in oxygenic photosynthesis; second, that the probability of acquiring photosynthesis via horizontal gene transfer is greater than the probability of losing photosynthesis; and third, and most important, that the origin of anoxygenic photosynthesis pre-dates the origin of oxygenic photosynthesis. I shall attempt to demonstrate that these three ideas are often grounded in incorrect assumptions built on more assumptions with no experimental or observational support. I hope that this brief review will not only serve as a cautionary tale but also that it will open new avenues of research aimed at disentangling the complex evolution of photosynthesis and its impact on the early history of life and the planet.
Photosystem II is a photochemical reaction center that catalyzes the light‐driven oxidation of water to molecular oxygen. Water oxidation is the distinctive photochemical reaction that permitted the evolution of oxygenic photosynthesis and the eventual rise of eukaryotes. At what point during the history of life an ancestral photosystem evolved the capacity to oxidize water still remains unknown. Here, we study the evolution of the core reaction center proteins of Photosystem II using sequence and structural comparisons in combination with Bayesian relaxed molecular clocks. Our results indicate that a homodimeric photosystem with sufficient oxidizing power to split water had already appeared in the early Archean about a billion years before the most recent common ancestor of all described Cyanobacteria capable of oxygenic photosynthesis, and well before the diversification of some of the known groups of anoxygenic photosynthetic bacteria. Based on a structural and functional rationale, we hypothesize that this early Archean photosystem was capable of water oxidation to oxygen and had already evolved protection mechanisms against the formation of reactive oxygen species. This would place primordial forms of oxygenic photosynthesis at a very early stage in the evolutionary history of life.
Nuernberg DJ, Morton J, Santabarbara S, et al., 2018, Photochemistry beyond the red limit in chlorophyll f-containing photosystems, Science, Vol: 360, Pages: 1210-1213, ISSN: 0036-8075
Photosystems I and II convert solar energy into the chemical energy that powers life. Chlorophyll a photochemistry, using red light (680 to 700 nm), is near universal and is considered to define the energy “red limit” of oxygenic photosynthesis. We present biophysical studies on the photosystems from a cyanobacterium grown in far-red light (750 nm). The few long-wavelength chlorophylls present are well resolved from each other and from the majority pigment, chlorophyll a. Charge separation in photosystem I and II uses chlorophyll f at 745 nm and chlorophyll f (or d) at 727 nm, respectively. Each photosystem has a few even longer-wavelength chlorophylls f that collect light and pass excitation energy uphill to the photochemically active pigments. These photosystems function beyond the red limit using far-red pigments in only a few key positions.
Cardona T, Shao S, Nixon PJ, 2018, Enhancing photosynthesis in plants: the light reactions, Essays in Biochemistry, Vol: 62, Pages: 85-94, ISSN: 0071-1365
In this review, we highlight recent research and current ideas on how to improve the efficiency of the light reactions of photosynthesis in crops. We note that the efficiency of photosynthesis is a balance between how much energy is used for growth and the energy wasted or spent protecting the photosynthetic machinery from photodamage. There are reasons to be optimistic about enhancing photosynthetic efficiency, but many appealing ideas are still on the drawing board. It is envisioned that the crops of the future will be extensively genetically modified to tailor them to specific natural or artificial environmental conditions.
Cardona Londono T, 2018, Early Archean origin of heterodimeric Photosystem I, Heliyon, Vol: 4, ISSN: 2405-8440
When and how oxygenic photosynthesis originated remains controversial. Wide uncertainties exist for the earliest detection of biogenic oxygen in the geochemical record or the origin of water oxidation in ancestral lineages of the phylum Cyanobacteria. A unique trait of oxygenic photosynthesis is that the process uses a Type I reaction centre with a heterodimeric core, also known as Photosystem I, made of two distinct but homologous subunits, PsaA and PsaB. In contrast, all other known Type I reaction centres in anoxygenic phototrophs have a homodimeric core. A compelling hypothesis for the evolution of a heterodimeric Type I reaction centre is that the gene duplication that allowed the divergence of PsaA and PsaB was an adaptation to incorporate photoprotective mechanisms against the formation of reactive oxygen species, therefore occurring after the origin of water oxidation to oxygen. Here I show, using sequence comparisons and Bayesian relaxed molecular clocks that this gene duplication event may have occurred in the early Archean more than 3.4 billion years ago, long before the most recent common ancestor of crown group Cyanobacteria and the Great Oxidation Event. If the origin of water oxidation predated this gene duplication event, then that would place primordial forms of oxygenic photosynthesis at a very early stage in the evolutionary history of life.
Shao S, Cardona T, Nixon PJ, 2018, Early emergence of the FtsH proteases involved in Photosystem II repair, Photosynthetica, Vol: 56, Pages: 163-177, ISSN: 0300-3604
Efficient degradation of damaged D1 during the repair of PSII is carried out by a set of dedicated FtsH proteases in the thylakoid membrane. Here we investigated whether the evolution of FtsH could hold clues to the origin of oxygenic photosynthesis. A phylogenetic analysis of over 6000 FtsH protease sequences revealed that there are three major groups of FtsH proteases originating from gene duplication events in the last common ancestor of bacteria, and that the FtsH proteases involved in PSII repair make a distinct clade branching out before the divergence of FtsH proteases found in all groups of anoxygenic phototrophic bacteria. Furthermore, we showed that the phylogenetic tree of FtsH proteases in phototrophic bacteria is similar to that for Type I and Type II reaction centre proteins. We conclude that the phylogeny of FtsH proteases is consistent with an early origin of water oxidation chemistry.
Cardona T, 2017, Early Archean origin of heterodimeric Photosystem I
<jats:title>Abstract</jats:title><jats:p>When and how oxygenic photosynthesis originated remains controversial. Wide uncertainties exist for the earliest detection of biogenic oxygen in the geochemical record or the origin of water oxidation in ancestral lineages of the phylum Cyanobacteria. A unique trait of oxygenic photosynthesis is that the process uses a Type I reaction centre with a heterodimeric core, also known as Photosystem I, made of two distinct but homologous subunits, PsaA and PsaB. In contrast, all other known Type I reaction centres in anoxygenic phototrophs have a homodimeric core. A compelling hypothesis for the evolution of a heterodimeric Type I reaction centre is that the gene duplication that allowed the divergence of PsaA and PsaB was an adaptation to incorporate photoprotective mechanisms against the formation of reactive oxygen species, therefore occurring after the origin of water oxidation to oxygen. Here I show, using sequence comparisons and Bayesian relaxed molecular clocks that this gene duplication event may have occurred in the early Archean more than 3.4 billion years ago, long before the most recent common ancestor of crown group Cyanobacteria and the Great Oxidation Event. If the origin of water oxidation predated this gene duplication event, then that would place primordial forms of oxygenic photosynthesis at a very early stage in the evolutionary history of life.</jats:p>
Cardona Londono T, Ann Magnuson, 2017, Isolation of Intact Thylakoid Membranes from Heterocysts of Filamentous, Nitrogen-Fixing Cyanobacteria, Plant Membrane Proteomics, Editors: Mock HP, Matros A, Witzel K, Publisher: Humana Press, New York, NY, Pages: 137-145, ISBN: 978-1-4939-7411-5
The isolation of thylakoid membranes, including intact membrane protein complexes, from heterocysts of filamentous cyanobacteria such as Nostoc punctiforme, is described. Protocols for BN-PAGE/SDS-PAGE 2-D electrophoresis are not included. However, the chapter ends with advisory notes on sample preparation for blue-native PAGE of thylakoid membrane proteins, which can then be used together with any standard protocol.
Cardona Londono T, 2017, Photosystem II is a chimera of reaction centers, Journal of Molecular Evolution, Vol: 84, Pages: 149-151, ISSN: 1432-1432
A complete scenario for the evolution of photosynthesis must account for the origin and diversification of photochemical reaction centers. Two lively debated questions are how the distinct types of reaction centers evolved and how cyanobacteria acquired two distinct reaction centers—Photosystem I and Photosystem II—in the path towards the origin of light-driven water oxidation, or in other words, towards the evolution of oxygenic photosynthesis (Hohmann-Marriott and Blankenship 2011; Fischer et al. 2016). Here I show how the chimeric structure of Photosystem II provides unambiguous answer to these questions.
<jats:title>Abstract</jats:title><jats:p>Photosystem II is a photochemical reaction center that catalyzes the light-driven oxidation of water to molecular oxygen. Water oxidation is the distinctive photochemical reaction that permitted the evolution of oxygenic photosynthesis and the eventual rise of Eukaryotes. At what point during the history of life an ancestral photosystem evolved the capacity to oxidize water still remains unknown. Here we study the evolution of the core reaction center proteins of Photosystem II using sequence and structural comparisons in combination with Bayesian relaxed molecular clocks. Our results indicate that a homodimeric photosystem with sufficient oxidizing power to split water had already appeared in the early Archean about a billion years before the most recent common ancestor of all described Cyanobacteria capable of oxygenic photosynthesis, and well before the diversification of some of the known groups of anoxygenic photosynthetic bacteria. Based on a structural and functional rationale we hypothesize that this early Archean photosystem was capable of water oxidation and had already evolved some level of protection against the formation of reactive oxygen species, which would place primordial forms of oxygenic photosynthesis at a very early stage in the evolutionary history of life.</jats:p>
Cardona Londono T, 2017, Evolution of photosynthesis, eLS
Cardona Londono T, 2016, Origin of bacteriochlorophyll a and the early diversification of photosynthesis, PLOS One, Vol: 11, ISSN: 1932-6203
Photosynthesis originated in the domain Bacteria billions of years ago; however, the identity of the last common ancestor to all phototrophic bacteria remains undetermined and speculative. Here I present the evolution of BchF or 3-vinyl-bacteriochlorophyll hydratase, an enzyme exclusively found in bacteria capable of synthetizing bacteriochlorophyll a. I show that BchF exists in two forms originating from an early divergence, one found in the phylum Chlorobi, including its paralogue BchV, and a second form that was ancestral to the enzyme found in the remaining anoxygenic phototrophic bacteria. The phylogeny of BchF is consistent with bacteriochlorophyll a evolving in an ancestral phototrophic bacterium that lived before the radiation event that gave rise to the phylum Chloroflexi, Chlorobi, Acidobacteria, Proteobacteria, and Gemmatimonadetes, but only after the divergence of Type I and Type II reaction centers. Consequently, it is suggested that the lack of phototrophy in many groups of extant bacteria is a derived trait.
Magnuson A, Cardona T, 2016, Thylakoid membrane function in heterocysts, BIOCHIMICA ET BIOPHYSICA ACTA-BIOENERGETICS, Vol: 1857, Pages: 309-319, ISSN: 0005-2728
Cardona Londono T, 2016, Reconstructing the origin of oxygenic photosynthesis: do assembly and photoactivation recapitulate evolution?, Frontiers in Plant Science, Vol: 7, ISSN: 1664-462X
Due to the great abundance of genomes and protein structures that today span a broad diversity of organisms, now more than ever before, it is possible to reconstruct the molecular evolution of protein complexes at an incredible level of detail. Here, I recount the story of oxygenic photosynthesis or how an ancestral reaction center was transformed into a sophisticated photochemical machine capable of water oxidation. First, I review the evolution of all reaction center proteins in order to highlight that Photosystem II and Photosystem I, today only found in the phylum Cyanobacteria, branched out very early in the history of photosynthesis. Therefore, it is very unlikely that they were acquired via horizontal gene transfer from any of the described phyla of anoxygenic phototrophic bacteria. Second, I present a new evolutionary scenario for the origin of the CP43 and CP47 antenna of Photosystem II. I suggest that the antenna proteins originated from the remodeling of an entire Type I reaction center protein and not from the partial gene duplication of a Type I reaction center gene. Third, I highlight how Photosystem II and Photosystem I reaction center proteins interact with small peripheral subunits in remarkably similar patterns and hypothesize that some of this complexity may be traced back to the most ancestral reaction center. Fourth, I outline the sequence of events that led to the origin of the Mn4CaO5 cluster and show that the most ancestral Type II reaction center had some of the basic structural components that would become essential in the coordination of the water-oxidizing complex. Finally, I collect all these ideas, starting at the origin of the first reaction center proteins and ending with the emergence of the water-oxidizing cluster, to hypothesize that the complex and well-organized process of assembly and photoactivation of Photosystem II recapitulate evolutionary transitions in the path to oxygenic photosynthesis.
Cardona T, Murray JW, Rutherford AW, 2015, Origin and Evolution of Water Oxidation before the Last Common Ancestor of the Cyanobacteria., Mol Biol Evol, Vol: 32, Pages: 1310-1328
Photosystem II, the water oxidizing enzyme, altered the course of evolution by filling the atmosphere with oxygen. Here, we reconstruct the origin and evolution of water oxidation at an unprecedented level of detail by studying the phylogeny of all D1 subunits, the main protein coordinating the water oxidizing cluster (Mn4CaO5) of Photosystem II. We show that D1 exists in several forms making well-defined clades, some of which could have evolved before the origin of water oxidation and presenting many atypical characteristics. The most ancient form is found in the genome of Gloeobacter kilaueensis JS-1 and this has a C-terminus with a higher sequence identity to D2 than to any other D1. Two other groups of early evolving D1 correspond to those expressed under prolonged far-red illumination and in darkness. These atypical D1 forms are characterized by a dramatically different Mn4CaO5 binding site and a Photosystem II containing such a site may assemble an unconventional metal cluster. The first D1 forms with a full set of ligands to the Mn4CaO5 cluster are grouped with D1 proteins expressed only under low oxygen concentrations and the latest evolving form is the dominant type of D1 found in all cyanobacteria and plastids. In addition, we show that the plastid ancestor had a D1 more similar to those in early branching Synechococcus. We suggest each one of these forms of D1 originated from transitional forms at different stages toward the innovation and optimization of water oxidation before the last common ancestor of all known cyanobacteria.
Cardona T, 2014, A fresh look at the evolution and diversification of photochemical reaction centers, Photosynthesis Research, ISSN: 1573-5079
Kato M, Cardona T, Rutherford AW, et al., 2013, Covalent Immobilization of Oriented Photosystem II on a Nanostructured Electrode for Solar Water Oxidation, JOURNAL OF THE AMERICAN CHEMICAL SOCIETY, Vol: 135, Pages: 10610-10613, ISSN: 0002-7863
Kato M, Cardona T, Rutherford AW, et al., 2012, Photoelectrochemical Water Oxidation with Photosystem II Integrated in a Mesoporous; Indium Tin Oxide Electrode, JOURNAL OF THE AMERICAN CHEMICAL SOCIETY, Vol: 134, Pages: 8332-8335, ISSN: 0002-7863
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