The role of Rubisco kinetics and pyrenoid morphology in shaping the CCM of haptophyte microalgae

Heureux, Ana; Young, Jodi N.; Whitney, Spencer M.; Eason-Hubbard, Maeve R; Lee, Renee B. Y.; Sharwood, Robert E.; Rickaby, Rosalind E. M.

doi:10.1093/jxb/erx179

Cited by 60 publications

(51 citation statements)

References 86 publications

(185 reference statements)

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“…For instance, in the oceans where the pH is between 7.8 and 8.4, only approximately 1% of the total dissolved inorganic carbon (DIC) is present in the form of CO 2 , bicarbonate being the most abundant inorganic carbon compound [25][26][27]. Moreover, at equilibrium with the atmosphere, the concentration of CO 2 is around 15 µM, which is lower than the typical values of half saturation constant ( C K 0.5 ) of the CO 2 -fixing enzyme ribulose 1,5-bisphosphate carboxylase oxygenase (Rubisco; C K 0.5 = 100-180 µM in cyanobacteria [28], 23-65 µM in diatoms [29], and 15-24 µM in haptophytes [30]). In addition, Rubisco-mediated carboxylation competes with the oxygenation of ribulose 1,5-bisphosphate (RuBP), which reduces carbon fixation and promotes photorespiration [31].…”

Section: The Need For Co 2 -Concentrating Mechanisms In Microalgaementioning

confidence: 88%

Insights on the Functions and Ecophysiological Relevance of the Diverse Carbonic Anhydrases in Microalgae

Jensen

Maberly

Gontero

2020

IJMS

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Carbonic anhydrases (CAs) exist in all kingdoms of life. They are metalloenzymes, often containing zinc, that catalyze the interconversion of bicarbonate and carbon dioxide—a ubiquitous reaction involved in a variety of cellular processes. So far, eight classes of apparently evolutionary unrelated CAs that are present in a large diversity of living organisms have been described. In this review, we focus on the diversity of CAs and their roles in photosynthetic microalgae. We describe their essential role in carbon dioxide-concentrating mechanisms and photosynthesis, their regulation, as well as their less studied roles in non-photosynthetic processes. We also discuss the presence in some microalgae, especially diatoms, of cambialistic CAs (i.e., CAs that can replace Zn by Co, Cd, or Fe) and, more recently, a CA that uses Mn as a metal cofactor, with potential ecological relevance in aquatic environments where trace metal concentrations are low. There has been a recent explosion of knowledge about this well-known enzyme with exciting future opportunities to answer outstanding questions using a range of different approaches.

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Section: The Need For Co 2 -Concentrating Mechanisms In Microalgaementioning

confidence: 88%

Insights on the Functions and Ecophysiological Relevance of the Diverse Carbonic Anhydrases in Microalgae

Jensen

Maberly

Gontero

2020

IJMS

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“…In any case, increasing the CO 2 concentration inside the cell relaxes the need for a highly substrate‐specific Rubisco. Organisms with a CCM usually express a Rubisco that trades off an increased

k_{cat}^{c}

for a decreased S c/o (Badger et al , ; Sharwood et al , ; Heureux et al , ; Sharwood, ). Non‐CCM ways to reduce Rubisco oxygenation include increasing S c/o by lowering the leaf temperature, which can be achieved by decreasing the absorbance of solar radiation or increasing transpiration (Sage, ).…”

Section: How Have Plants Dealt With Photorespiration Evolutionarily?mentioning

confidence: 99%

Photorespiration in the context of Rubisco biochemistry, CO₂ diffusion and metabolism

2020

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Summary Photorespiratory metabolism is essential for plants to maintain functional photosynthesis in an oxygen‐containing environment. Because the oxygenation reaction of Rubisco is followed by the loss of previously fixed carbon, photorespiration is often considered a wasteful process and considerable efforts are aimed at minimizing the negative impact of photorespiration on the plant’s carbon uptake. However, the photorespiratory pathway has also many positive aspects, as it is well integrated within other metabolic processes, such as nitrogen assimilation and C1 metabolism, and it is important for maintaining the redox balance of the plant. The overall effect of photorespiratory carbon loss on the net CO2 fixation of the plant is also strongly influenced by the physiology of the leaf related to CO2 diffusion. This review outlines the distinction between Rubisco oxygenation and photorespiratory CO2 release as a basis to evaluate the costs and benefits of photorespiration.

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“…During this time, substantial progress has been made in understanding the structure of the active site and the complete reaction mechanism catalyzed by RuBisCO (Andersson, 2008). Although most of the studies on RuBisCO structural properties and its reaction mechanism have been focused on a few model species, and large-scale explorations of RuBisCO catalytic traits have been frequently restricted to angiosperm species (Galm es et al, 2005;Kubien et al, 2008;Hermida-Carrera et al, 2016;Orr et al, 2016;Sharwood et al, 2016a), recent research studies have shed light on the variability of biochemical and molecular RuBisCO traits in previously underreported groups (Satagopan et al, 2014;Galm es et al, 2014aGalm es et al, , 2015Galm es et al, , 2016Wilson et al, 2016;Young et al, 2016;Heureux et al, 2017;Valeg ard et al, 2018;Iñiguez et al, 2018). The increase in the availability of RuBisCO measurements on phylogenetically distant groups have enabled a more profound analysis of RuBisCO fine tuning through evolution (Liu et al, 2017;Young and Hopkinson, 2017;Cummins et al, 2018;Tcherkez et al, 2018).…”

Section: Introductionmentioning

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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The role of Rubisco kinetics and pyrenoid morphology in shaping the CCM of haptophyte microalgae

Abstract: Variations in the pyrenoid morphology, Rubisco content, and kinetics among haptophyte algae provide insight into their carbon-concentrating mechanisms.

Cited by 60 publications

References 86 publications

Insights on the Functions and Ecophysiological Relevance of the Diverse Carbonic Anhydrases in Microalgae

Insights on the Functions and Ecophysiological Relevance of the Diverse Carbonic Anhydrases in Microalgae

Photorespiration in the context of Rubisco biochemistry, CO₂ diffusion and metabolism

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

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The role of Rubisco kinetics and pyrenoid morphology in shaping the CCM of haptophyte microalgae

Abstract: Variations in the pyrenoid morphology, Rubisco content, and kinetics among haptophyte algae provide insight into their carbon-concentrating mechanisms.

Cited by 60 publications

References 86 publications

Insights on the Functions and Ecophysiological Relevance of the Diverse Carbonic Anhydrases in Microalgae

Insights on the Functions and Ecophysiological Relevance of the Diverse Carbonic Anhydrases in Microalgae

Photorespiration in the context of Rubisco biochemistry, CO2 diffusion and metabolism

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

Contact Info

Product

Resources

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Photorespiration in the context of Rubisco biochemistry, CO₂ diffusion and metabolism

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