Looking for life elsewhere: Photosynthesis and astrobiology

Photosynthesis produces signs of life we can see from space: the absorbance spectrum of surface photosynthetic pigments and, with oxygenic photosynthesis, atmospheric oxygen. Since the first discovery of a planet in another solar system in 1989, there has been an explosion in the detection of exoplanets (over 1849 as of 7 November 2014) and we are getting ever closer to finding that Goldilocks planet that might harbour life. With telescope observations of these planets, oxygenic photosynthesis has been considered our most robust target ‘biosignature’ that would not appear on a lifeless planet. Since anoxygenic photosynthetic organisms do not produce unambiguously biogenic gases, there is interest in their pigments serving as spectral indicators of life. But will they look the same as on Earth, can we distinguish them from the abiotic, and what will dominate on another planet? Examples from Earth provide us with the potential to extrapolate some rules for photosynthesis to predict its signature on another planet, but there are yet things we must answer about life here to improve our confidence. In particular, given the combination of the available stellar spectrum and molecular constraints on photon energy use, can we predict the pigment spectral features that will dominate, which reductant will match, and what biogenic gases would result? We take clues from the diversity of anoxygenic photosynthetic metabolisms and three very recent examples of oxygenic photosynthesis utilizing other reaction centre (RC) chlorophylls in addition to chlorophyll a (Chl a).

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Reflections on the Nature and Function of the Photosystem II Reaction Centre

Functional Plant Biology ◽

10.1071/pp9950161 ◽

1995 ◽

Vol 22 (2) ◽

pp. 161 ◽

Cited By ~ 6

Author(s):

M Seibert

Keyword(s):

Photosystem Ii ◽

Atmospheric Carbon Dioxide ◽

Chemical Potential ◽

Atmospheric Oxygen ◽

Primary Electron ◽

Reaction Centre ◽

Primary Electron Donor ◽

Primary Charge Separation ◽

Photosynthetic Organisms ◽

And Function

The reaction centre of photosystem II (PSII) converts light energy into chemical potential used by higher photosynthetic organisms to produce atmospheric oxygen. Water is the source of the oxygen and also the reductant required to fix atmospheric carbon dioxide. The purpose of this paper is to identify the physical location of the reaction centre complex in the thylakoid membrane, quantitate the core chlorophyll pigment stoichiometry in the isolated complex, discuss the primary charge-separation process, and examine current information on the nature of the primary electron donor of PSII.

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Oxygenic photosynthesis: history, status and perspective

Quarterly Reviews of Biophysics ◽

10.1017/s0033583518000112 ◽

2019 ◽

Vol 52 ◽

Cited By ~ 19

Author(s):

Wolfgang Junge

Keyword(s):

Water Oxidation ◽

Acoustic Waves ◽

Homo Sapiens ◽

Atmospheric Oxygen ◽

Average Power ◽

Oxygenic Photosynthesis ◽

Reaction Centre ◽

Total Energy Consumption ◽

X Ray ◽

Average Power Consumption

AbstractCyanobacteria and plants carry out oxygenic photosynthesis. They use water to generate the atmospheric oxygen we breathe and carbon dioxide to produce the biomass serving as food, feed, fibre and fuel. This paper scans the emergence of structural and mechanistic understanding of oxygen evolution over the past 50 years. It reviews speculative concepts and the stepped insight provided by novel experimental and theoretical techniques. Driven by sunlight photosystem II oxidizes the catalyst of water oxidation, a hetero-metallic Mn4CaO5(H2O)4 cluster. Mn3Ca are arranged in cubanoid and one Mn dangles out. By accumulation of four oxidizing equivalents before initiating dioxygen formation it matches the four-electron chemistry from water to dioxygen to the one-electron chemistry of the photo-sensitizer. Potentially harmful intermediates are thereby occluded in space and time. Kinetic signatures of the catalytic cluster and its partners in the photo-reaction centre have been resolved, in the frequency domain ranging from acoustic waves via infra-red to X-ray radiation, and in the time domain from nano- to milli-seconds. X-ray structures to a resolution of 1.9 Å are available. Even time resolved X-ray structures have been obtained by clocking the reaction cycle by flashes of light and diffraction with femtosecond X-ray pulses. The terminal reaction cascade from two molecules of water to dioxygen involves the transfer of four electrons, two protons, one dioxygen and one water. A rigorous mechanistic analysis is challenging because of the kinetic enslaving at millisecond duration of six partial reactions (4e−, 1H+, 1O2). For the time being a peroxide-intermediate in the reaction cascade to dioxygen has been in focus, both experimentally and by quantum chemistry. Homo sapiens has relied on burning the products of oxygenic photosynthesis, recent and fossil. Mankind's total energy consumption amounts to almost one-fourth of the global photosynthetic productivity. If the average power consumption equalled one of those nations with the highest consumption per capita it was four times greater and matched the total productivity. It is obvious that biomass should be harvested for food, feed, fibre and platform chemicals rather than for fuel.

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Early Archean origin of heterodimeric Photosystem I

10.1101/225888 ◽

2017 ◽

Author(s):

Tanai Cardona

Keyword(s):

Gene Duplication ◽

Photosystem I ◽

Water Oxidation ◽

Duplication Event ◽

Oxygenic Photosynthesis ◽

Recent Common Ancestor ◽

Type I ◽

Reaction Centre ◽

Gene Duplication Event ◽

Most Recent Common Ancestor

AbstractWhen 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.

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Insights into the evolution of oxygenic photosynthesis from a phylogenetically novel, low-light cyanobacterium

10.1101/334458 ◽

2018 ◽

Author(s):

Christen L. Grettenberger ◽

Dawn Y. Sumner ◽

Kate Wall ◽

C. Titus Brown ◽

Jonathan Eisen ◽

...

Keyword(s):

Atmospheric Oxygen ◽

Evolutionary Model ◽

Reaction Centers ◽

Oxygenic Photosynthesis ◽

Oxygen Production ◽

Crown Group ◽

Low Light ◽

Extrinsic Proteins ◽

Structural Parts ◽

Life On Earth

AbstractAtmospheric oxygen level rose dramatically around 2.4 billion years ago due to oxygenic photosynthesis by the Cyanobacteria. The oxidation of surface environments permanently changed the future of life on Earth, yet the evolutionary processes leading to oxygen production are poorly constrained. Partial records of these evolutionary steps are preserved in the genomes of organisms phylogenetically placed between non-photosynthetic Melainabacteria, crown-group Cyanobacteria, and Gloeobacter, representing the earliest-branching Cyanobacteria capable of oxygenic photosynthesis. Here, we describe nearly complete, metagenome assembled genomes of an uncultured organism phylogenetically placed between the Melainabacteria and crown-group Cyanobacteria, for which we propose the name Candidatus Aurora vandensis {au.rora Latin noun dawn and vand.ensis, originating from Vanda}.The metagenome assembled genome of A. vandensis contains homologs of most genes necessary for oxygenic photosynthesis including key reaction center proteins. Many extrinsic proteins associated with the photosystems in other species are, however, missing or poorly conserved. The assembled genome also lacks homologs of genes associated with the pigments phycocyanoerethrin, phycoeretherin and several structural parts of the phycobilisome. Based on the content of the genome, we propose an evolutionary model for increasing efficiency of oxygenic photosynthesis through the evolution of extrinsic proteins to stabilize photosystem II and I reaction centers and improve photon capture. This model suggests that the evolution of oxygenic photosynthesis may have significantly preceded oxidation of Earth’s atmosphere due to low net oxygen production by early Cyanobacteria.

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Global biosphere primary productivity over the last 800,000 years reconstructed from the triple-isotope composition of dioxygen trapped in polar ice cores

10.5194/egusphere-egu21-12552 ◽

2021 ◽

Author(s):

Ji-Woong Yang ◽

Amaëlle Landais ◽

Margaux Brandon ◽

Thomas Blunier ◽

Frédéric Prié ◽

...

Keyword(s):

Primary Productivity ◽

Isotope Composition ◽

Atmospheric Oxygen ◽

Ice Cores ◽

Oxygenic Photosynthesis ◽

Time Interval ◽

Polar Ice ◽

Future Evolution ◽

Glacial Stage ◽

Glacial Periods

The primary production, or oxygenic photosynthesis of the global biosphere, is one of the main source and sink of atmospheric oxygen (O2) and carbon dioxide (CO2), respectively. There has been a growing number of evidence that global gross primary productivity (GPP) varies in response to climate change. It is therefore important to understand the climate- and/or environment controls of the global biosphere primary productivity for better predicting the future evolution of biosphere carbon uptake. The triple-isotope composition of O2 (&#916;17O of O2) trapped in polar ice cores allows us to trace the past changes of global biosphere primary productivity as far back as 800,000 years before present (800 ka). Previously available &#916;17O of O2 records over the last ca. 450 ka show relatively low and high global biosphere productivity over the last five glacial and interglacial intervals respectively, with a unique pattern over Termination V (TV) - Marine Isotopic Stage (MIS) 11, as biosphere productivity at the end of TV is ~ 20 % higher than the four younger ones (Blunier et al., 2012; Brandon et al., 2020). However, questions remain on (1) whether the concomitant changes of global biosphere productivity and CO2 were the pervasive feature of glacial periods over the last 800 ka, and (2) whether the global biosphere productivity during the &#8220;lukewarm&#8221; interglacials before the Mid-Brunhes Event (MBE) were lower than those after the MBE. Here, we present an extended composite record of &#916;17O of O2 covering the last 800 ka, based on new &#916;17O of O2 results from the EPICA Dome C and reconstruct the evolution of global biosphere productivity over that time interval using the independent box models of Landais et al. (2007) and Blunier et al. (2012). We find that the glacial productivity minima occurred nearly synchronously with the glacial CO2 minima at mid-glacial stage; interestingly millennia before the sea level reaches their minima. Following the mid-glacial minima, we also show slight productivity increases at the full-glacial stages, before deglacial productivity rises. Comparison of reconstructed interglacial productivity demonstrates a slightly higher productivity over the post-MBE (MISs 1, 5, 7, 9, and 11) than pre-MBE ones (MISs 13, 15, 17, and 19). However, the mean difference between post- and pre-MBE interglacials largely depends on the box model used for productivity reconstruction.

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Structural basis for blue-green light harvesting and energy dissipation in diatoms

Science ◽

10.1126/science.aav0365 ◽

2019 ◽

Vol 363 (6427) ◽

pp. eaav0365 ◽

Cited By ~ 49

Author(s):

Wenda Wang ◽

Long-Jiang Yu ◽

Caizhe Xu ◽

Takashi Tomizaki ◽

Songhao Zhao ◽

...

Keyword(s):

Energy Transfer ◽

Phaeodactylum Tricornutum ◽

Light Harvesting ◽

Green Light ◽

Marine Diatom ◽

Structural Basis ◽

Aquatic Environments ◽

Efficient Energy Transfer ◽

Chl A ◽

Photosynthetic Organisms

Diatoms are abundant photosynthetic organisms in aquatic environments and contribute 40% of its primary productivity. An important factor that contributes to the success of diatoms is their fucoxanthin chlorophyll a/c-binding proteins (FCPs), which have exceptional light-harvesting and photoprotection capabilities. Here, we report the crystal structure of an FCP from the marine diatom Phaeodactylum tricornutum, which reveals the binding of seven chlorophylls (Chls) a, two Chls c, seven fucoxanthins (Fxs), and probably one diadinoxanthin within the protein scaffold. Efficient energy transfer pathways can be found between Chl a and c, and each Fx is surrounded by Chls, enabling the energy transfer and quenching via Fx highly efficient. The structure provides a basis for elucidating the mechanisms of blue-green light harvesting, energy transfer, and dissipation in diatoms.

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Lysine Propionylation is a Widespread Post-Translational Modification Involved in Regulation of Photosynthesis and Metabolism in Cyanobacteria

International Journal of Molecular Sciences ◽

10.3390/ijms20194792 ◽

2019 ◽

Vol 20 (19) ◽

pp. 4792 ◽

Cited By ~ 1

Author(s):

Mingkun Yang ◽

Hui Huang ◽

Feng Ge

Keyword(s):

Large Fraction ◽

Bioinformatic Analysis ◽

High Light ◽

Site Directed Mutagenesis ◽

Oxygenic Photosynthesis ◽

Post Translational Modification ◽

Functional Studies ◽

Photosynthetic Organisms ◽

Model Combining ◽

And Function

Lysine propionylation is a reversible and widely distributed post-translational modification that is known to play a regulatory role in both eukaryotes and prokaryotes. However, the extent and function of lysine propionylation in photosynthetic organisms remains unclear. Cyanobacteria are the most ancient group of Gram-negative bacteria capable of oxygenic photosynthesis, and are of great importance to global carbon and nitrogen cycles. Here, we carried out a systematic study of lysine propionylaiton in cyanobacteria where we used Synechocystis sp. PCC 6803 (Synechocystis) as a model. Combining high-affinity anti-propionyllysine pan antibodies with high-accuracy mass spectrometry (MS) analysis, we identified 111 unique lysine propionylation sites on 69 proteins in Synechocystis. Further bioinformatic analysis showed that a large fraction of the propionylated proteins were involved in photosynthesis and metabolism. The functional significance of lysine propionylation on the enzymatic activity of fructose-1,6-bisphosphatase (FbpI) was studied by site-directed mutagenesis and biochemical studies. Further functional studies revealed that the propionylation level of subunit II of photosystem I (PsaD) was obviously increased after high light (HL) treatment, suggesting that propionylation may be involved in high light adaption in Synechocystis. Thus, our findings provide novel insights into the range of functions regulated by propionylation and reveal that reversible propionylation is a functional modification with the potential to regulate photosynthesis and carbon metabolism in Synechocystis, as well as in other photosynthetic organisms.

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Cryo-EM Structure of a Tetrameric Photosystem I from Chroococcidiopsis TS-821, a Thermophilic, Non-heterocyst-forming Cyanobacteria

10.21203/rs.3.rs-81702/v1 ◽

2020 ◽

Author(s):

Dmitry Semchonok ◽

Jyotirmoy Mondal ◽

Connor Cooper ◽

Katrina Schlum ◽

Meng Li ◽

...

Keyword(s):

Excitation Energy ◽

Photosystem I ◽

Bioinformatics Analysis ◽

Oxygenic Photosynthesis ◽

Monomeric Form ◽

Oligomeric State ◽

Unicellular Cyanobacterium ◽

Photosynthetic Organisms ◽

Conserved Regions ◽

Evolutionary Step

Abstract Photosystem I (PSI) is one of two the photosystems involved in oxygenic photosynthesis. PSI of cyanobacteria exists in monomeric, trimeric, and tetrameric forms, which is in contrast to the strictly monomeric form of PSI in plants and algae. The tetrameric organization raises questions about its structural, physiological, and evolutional significance. Here we report the ~3.9 Å resolution cryo-EM structure of tetrameric PSI from the thermophilic, unicellular cyanobacterium Chroococcidiopsis sp. TS-821. The structure resolves all 44 subunits and 448 cofactor molecules. We conclude that the tetramer is arranged via two different interfaces resulting from a dimer-of-dimers organization. The localization of chlorophyll molecules permits an excitation energy pathway within and between adjacent monomers. Bioinformatics analysis reveals conserved regions in PsaL subunit that correlate with the oligomeric state. Tetrameric PSI may function as a key evolutionary step between the trimeric and monomeric forms of PSI organization in photosynthetic organisms.

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Revisiting the early evolution of Cyanobacteria with a new thylakoid-less and deeply diverged isolate from a hornwort

10.1101/2021.02.18.431691 ◽

2021 ◽

Author(s):

Nasim Rahmatpour ◽

Duncan A. Hauser ◽

Jessica M. Nelson ◽

Pa Yu Chen ◽

Juan Carlos Villarreal A. ◽

...

Keyword(s):

Clock Genes ◽

Atmospheric Oxygen ◽

Carotenoid Biosynthesis ◽

Oxygenic Photosynthesis ◽

Phylogenetic Position ◽

Closely Related Species ◽

Gene Sets ◽

Wide Range ◽

Circadian Clock Genes ◽

Carotenoid Biosynthesis Pathway

SummaryCyanobacteria have played pivotal roles in Earth’s geological history especially during the rise of atmospheric oxygen. However, our ability to infer the early transitions in Cyanobacteria evolution has been limited by their extremely lopsided tree of life—the vast majority of extant diversity belongs to Phycobacteria (or “crown Cyanobacteria”), while its sister lineage, Gloeobacteria, is depauperate and contains only two closely related species of Gloeobacter and a metagenome-assembled genome. Here we describe a new culturable member of Gloeobacteria, Anthocerobacter panamensis, isolated from a tropical hornwort. Anthocerobacter diverged from Gloeobacter over 1.4 billion years ago and has low 16S identities with environmental samples. Our ultrastructural, physiological, and genomic analyses revealed that this species possesses a unique combination of traits that are exclusively shared with either Gloeobacteria or Phycobacteria. For example, similar to Gloeobacter, it lacks thylakoids and circadian clock genes, but the carotenoid biosynthesis pathway is typical of Phycobacteria. Furthermore, Anthocerobacter has one of the most reduced gene sets for photosystems and phycobilisomes among Cyanobacteria. Despite this, Anthocerobacter is capable of oxygenic photosynthesis under a wide range of light intensities, albeit with much less efficiency. Given its key phylogenetic position, distinct trait combination, and availability as a culture, Anthocerobacter opens a new window to further illuminate the dawn of oxygenic photosynthesis.

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Photosynthesis: basics, history and modelling

Annals of Botany ◽

10.1093/aob/mcz171 ◽

2019 ◽

Vol 126 (4) ◽

pp. 511-537 ◽

Cited By ~ 8

Author(s):

Alexandrina Stirbet ◽

Dušan Lazár ◽

Ya Guo ◽

Govindjee Govindjee

Keyword(s):

Chlorophyll A ◽

Water Oxidation ◽

Carbon Fixation ◽

Agricultural Land ◽

Atp Synthesis ◽

Oxygenic Photosynthesis ◽

State Transitions ◽

Photochemical Quenching ◽

Exciting Light ◽

Reaction Centre

Abstract Background With limited agricultural land and increasing human population, it is essential to enhance overall photosynthesis and thus productivity. Oxygenic photosynthesis begins with light absorption, followed by excitation energy transfer to the reaction centres, primary photochemistry, electron and proton transport, NADPH and ATP synthesis, and then CO2 fixation (Calvin–Benson cycle, as well as Hatch–Slack cycle). Here we cover some of the discoveries related to this process, such as the existence of two light reactions and two photosystems connected by an electron transport ‘chain’ (the Z-scheme), chemiosmotic hypothesis for ATP synthesis, water oxidation clock for oxygen evolution, steps for carbon fixation, and finally the diverse mechanisms of regulatory processes, such as ‘state transitions’ and ‘non-photochemical quenching’ of the excited state of chlorophyll a. Scope In this review, we emphasize that mathematical modelling is a highly valuable tool in understanding and making predictions regarding photosynthesis. Different mathematical models have been used to examine current theories on diverse photosynthetic processes; these have been validated through simulation(s) of available experimental data, such as chlorophyll a fluorescence induction, measured with fluorometers using continuous (or modulated) exciting light, and absorbance changes at 820 nm (ΔA820) related to redox changes in P700, the reaction centre of photosystem I. Conclusions We highlight here the important role of modelling in deciphering and untangling complex photosynthesis processes taking place simultaneously, as well as in predicting possible ways to obtain higher biomass and productivity in plants, algae and cyanobacteria.

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