The trouble with oxygen: The ecophysiology of extant phototrophs and implications for the evolution of oxygenic photosynthesis

Hamilton, Trinity L.

doi:10.1016/j.freeradbiomed.2019.05.003

Cited by 43 publications

(23 citation statements)

References 220 publications

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“…After the appearance of oxygenic photosynthesis, RuBisCO had to face substantial [O 2 ] for the first time, and oxygenation of RuBP that produced 2‐phosphoglycolate led to the evolution of the photorespiration pathway. Indeed, fine tuning of oxygenic photosynthesis, photorespiration, and evolving mechanisms for detoxifying reactive oxygen species (ROS) has been proposed to have occurred in an anaerobic photosynthesizing cyanobacterial ancestor before the GOE (Hamilton, ). This process of co‐evolution would have been aided by the prevailing reducing conditions until the organism was able to detoxify 2‐phosphoglycolate and ROS.…”

Section: The Diversification Of Photosynthetic Organisms and The Origmentioning

confidence: 99%

Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO₂ concentrating mechanisms

et al. 2020

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Summary RuBisCO‐catalyzed CO2 fixation is the main source of organic carbon in the biosphere. This enzyme is present in all domains of life in different forms (III, II, and I) and its origin goes back to 3500 Mya, when the atmosphere was anoxygenic. However, the RuBisCO active site also catalyzes oxygenation of ribulose 1,5‐bisphosphate, therefore, the development of oxygenic photosynthesis and the subsequent oxygen‐rich atmosphere promoted the appearance of CO2 concentrating mechanisms (CCMs) and/or the evolution of a more CO2‐specific RuBisCO enzyme. The wide variability in RuBisCO kinetic traits of extant organisms reveals a history of adaptation to the prevailing CO2/O2 concentrations and the thermal environment throughout evolution. Notable differences in the kinetic parameters are found among the different forms of RuBisCO, but the differences are also associated with the presence and type of CCMs within each form, indicative of co‐evolution of RuBisCO and CCMs. Trade‐offs between RuBisCO kinetic traits vary among the RuBisCO forms and also among phylogenetic groups within the same form. These results suggest that different biochemical and structural constraints have operated on each type of RuBisCO during evolution, probably reflecting different environmental selective pressures. In a similar way, variations in carbon isotopic fractionation of the enzyme point to significant differences in its relationship to the CO2 specificity among different RuBisCO forms. A deeper knowledge of the natural variability of RuBisCO catalytic traits and the chemical mechanism of RuBisCO carboxylation and oxygenation reactions raises the possibility of finding unrevealed landscapes in RuBisCO evolution.

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Section: The Diversification Of Photosynthetic Organisms and The Origmentioning

confidence: 99%

Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO₂ concentrating mechanisms

et al. 2020

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“…The functional link between the B-family HCO and phototrophy in these organisms is not well understood, but may relate to the adaptation of B-family HCOs to relatively low oxygen concentrations (Han et al 2011) and the oxygen sensitivity of proteins involved in anoxygenic phototrophy (e.g. Hamilton 2019) tying anoxygenic photoheterotrophy in these organisms to low-oxygen environments. Interestingly, phylogenetic relationships of B-family HCO proteins are incongruent with organismal relationships and with relationships among phototrophy proteins (Figure 3, Figure 4).…”

Section: Resultsmentioning

confidence: 99%

Complex history of aerobic respiration and phototrophy in the Chloroflexota class Anaerolineae revealed by high-quality draft genome ofCa. Roseilinea mizusawaensis AA3_104

Ward

Hau-Li

Kakegawa

et al. 2020

Preprint

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The candidate genus Roseilinea is a novel lineage in the Chloroflexota (formerly Chloroflexi or green nonsulfur bacteria) phylum known so far only from very incomplete metagenome-assembled genomes and preliminary enrichments. Roseilinea is notable for appearing capable of anoxygenic photoheterotrophy despite being only distantly related to well-known phototrophic Chloroflexota in the Chloroflexia class such as Chloroflexus and Roseiflexus. Here, we present a high quality metagenome-assembled genome of a member of Roseilinea, greatly improving our understanding of the metabolic capacity and taxonomic assignment of this genus. These data allow us to confidently describe the genetic basis for photoheterotrophy in these organisms as well as propose a candidate family for these organisms, Ca. Roseilineaceae, within the Anaerolineae class of Chloroflexota.

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“…Its initial evolution was very likely coupled to the appearance of the dual‐photosystem bearing, oxygen‐evolving cyanobacteria − the 'oxyphotobacteria' – and their divergence from non‐phototrophic cyanobacteria sometime between 3.2 and 2.5 billion years ago, as illustrated in Figure (for review, see Schirrmeister et al , ; Soo et al , ). These ancestral phototrophic cyanobacteria were the first organisms to be challenged by high to super‐saturating daytime oxygen tensions in locally oxygen‐rich environments, with such conditions being particularly prominent in microbial mats (for review, see Dick et al , ; Hamilton, ). These conditions triggered new metabolic processes and innovations, including massively increased rates of 2PG synthesis and its subsequent degradation by an ancient photorespiratory pathway.…”

Section: The Past and Future Of Photorespirationmentioning

confidence: 99%

Wasteful, essential, evolutionary stepping stone? The multiple personalities of the photorespiratory pathway

Fernie

Bauwe

2020

The Plant Journal

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The photorespiratory pathway, in short photorespiration, is a metabolic repair system that enables the CO 2 fixation enzyme Rubisco to sustainably operate in the presence of oxygen, that is, during oxygenic photosynthesis of plants and cyanobacteria. Photorespiration is necessary because an auto-inhibitory metabolite, 2-phosphoglycolate (2PG), is produced when Rubisco binds oxygen instead of CO 2 as a substrate and must be removed, to avoid collapse of metabolism, and recycled as efficiently as possible. The basic principle of recycling 2PG very likely evolved several billion years ago in connection with the evolution of oxyphotobacteria. It comprises the multi-step combination of two molecules of 2PG to form 3-phosphoglycerate. The biochemistry of this process dictates that one out of four 2PG carbons is lost as CO 2 , which is a long-standing plant breeders' concern because it represents by far the largest fraction of respiratory processes that reduce gross-photosynthesis of major crops down to about 50% and less, lowering potential yields. In addition to the ATP needed for recycling of the 2PG carbon, extra energy is needed for the refixation of liberated equal amounts of ammonia. It is thought that the energy costs of photorespiration have an additional negative impact on crop yields in at least some environments. This paper discusses recent advances concerning the origin and evolution of photorespiration, and gives an overview of contemporary and envisioned strategies to engineer the biochemistry of, or even avoid, photorespiration.

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The trouble with oxygen: The ecophysiology of extant phototrophs and implications for the evolution of oxygenic photosynthesis

Cited by 43 publications

References 220 publications

Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO₂ concentrating mechanisms

Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO₂ concentrating mechanisms

Complex history of aerobic respiration and phototrophy in the Chloroflexota class Anaerolineae revealed by high-quality draft genome ofCa. Roseilinea mizusawaensis AA3_104

Wasteful, essential, evolutionary stepping stone? The multiple personalities of the photorespiratory pathway

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The trouble with oxygen: The ecophysiology of extant phototrophs and implications for the evolution of oxygenic photosynthesis

Cited by 43 publications

References 220 publications

Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO2 concentrating mechanisms

Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO2 concentrating mechanisms

Complex history of aerobic respiration and phototrophy in the Chloroflexota class Anaerolineae revealed by high-quality draft genome ofCa. Roseilinea mizusawaensis AA3_104

Wasteful, essential, evolutionary stepping stone? The multiple personalities of the photorespiratory pathway

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Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO₂ concentrating mechanisms

Evolutionary trends in RuBisCO kinetics and their co‐evolution with CO₂ concentrating mechanisms