Rubisco proton production can drive the elevation of CO2 within condensates and carboxysomes

Membraneless organelles containing the enzyme ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) are a common feature of organisms utilizing CO2 concentrating mechanisms to enhance photosynthetic carbon acquisition. In cyanobacteria and proteobacteria, the Rubisco condensate is encapsulated in a proteinaceous shell, collectively termed a carboxysome, while some algae and hornworts have evolved Rubisco condensates known as pyrenoids. In both cases, CO2 fixation is enhanced compared with the free enzyme. Previous mathematical models have attributed the improved function of carboxysomes to the generation of elevated CO2 within the organelle via a colocalized carbonic anhydrase (CA) and inwardly diffusing HCO3−, which have accumulated in the cytoplasm via dedicated transporters. Here, we present a concept in which we consider the net of two protons produced in every Rubisco carboxylase reaction. We evaluate this in a reaction–diffusion compartment model to investigate functional advantages these protons may provide Rubisco condensates and carboxysomes, prior to the evolution of HCO3− accumulation. Our model highlights that diffusional resistance to reaction species within a condensate allows Rubisco-derived protons to drive the conversion of HCO3− to CO2 via colocalized CA, enhancing both condensate [CO2] and Rubisco rate. Protonation of Rubisco substrate (RuBP) and product (phosphoglycerate) plays an important role in modulating internal pH and CO2 generation. Application of the model to putative evolutionary ancestors, prior to contemporary cellular HCO3− accumulation, revealed photosynthetic enhancements along a logical sequence of advancements, via Rubisco condensation, to fully formed carboxysomes. Our model suggests that evolution of Rubisco condensation could be favored under low CO2 and low light environments.

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Rubisco proton production can drive the elevation of CO2 within condensates and carboxysomes

10.1101/2020.07.08.125609 ◽

2020 ◽

Cited By ~ 1

Author(s):

Benedict M. Long ◽

Britta Förster ◽

Sacha B. Pulsford ◽

G. Dean Price ◽

Murray R. Badger

Keyword(s):

Reaction Diffusion ◽

Compartment Model ◽

Low Light ◽

Bisphosphate Carboxylase ◽

Proton Production ◽

Logical Sequence ◽

Photosynthetic Carbon ◽

Internal Ph ◽

Novel Concept ◽

Improved Function

ABSTRACTMembraneless organelles containing the enzyme Ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) are a common feature of organisms utilizing CO2 concentrating mechanisms (CCMs) to enhance photosynthetic carbon acquisition. In cyanobacteria and proteobacteria, the Rubisco condensate is encapsulated in a proteinaceous shell, collectively termed a carboxysome, while some algae and hornworts have evolved Rubisco condensates known as pyrenoids. In both cases, CO2 fixation is enhanced compared with the free enzyme. Previous mathematical models have attributed the improved function of carboxysomes to the generation of elevated CO2 within the organelle via a co-localized carbonic anhydrase (CA), and inwardly diffusing HCO3- which has accumulated in the cytoplasm via dedicated transporters. Here we present a novel concept in which we consider the net of two protons produced in every Rubisco carboxylase reaction. We evaluate this in a reaction-diffusion, compartment model to investigate functional advantages these protons may provide Rubisco condensates and carboxysomes, prior to the evolution of HCO3- accumulation. Our model highlights that diffusional resistance to reaction species within a condensate allows Rubisco-derived protons to drive the conversion of HCO3- to CO2 via co-localized CA, enhancing both condensate [CO2] and Rubisco rate. Protonation of Rubisco substrate (RuBP) and product (PGA) plays an important role in modulating internal pH and CO2 generation. Application of the model to putative evolutionary ancestors, prior to contemporary cellular HCO3- accumulation, revealed photosynthetic enhancements along a logical sequence of advancements, via Rubisco condensation, to fully-formed carboxysomes. Our model suggests that evolution of Rubisco condensation could be favored under low CO2 and low light environments.

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Expression patterns of two carbonic anhydrase genes, Na+/K+-ATPase and V-type H+-ATPase, in the freshwater crayfish, Cherax quadricarinatus, exposed to low pH and high pH

Australian Journal of Zoology ◽

10.1071/zo16048 ◽

2017 ◽

Vol 65 (1) ◽

pp. 50 ◽

Cited By ~ 3

Author(s):

Muhammad Yousuf Ali ◽

Ana Pavasovic ◽

Peter B. Mather ◽

Peter J. Prentis

Keyword(s):

Carbonic Anhydrase ◽

Expression Patterns ◽

Maximum Level ◽

Low Ph ◽

Freshwater Crayfish ◽

Α Subunit ◽

Cherax Quadricarinatus ◽

High Ph ◽

Internal Ph ◽

Ph Conditions

Carbonic anhydrase (CA), Na+/K+-ATPase (NKA) and Vacuolar-type H+-ATPase (HAT) play vital roles in osmoregulation and pH balance in decapod crustaceans. As variable pH levels have a significant impact on the physiology of crustaceans, it is crucial to understand the mechanisms by which an animal maintains its internal pH. We examined expression patterns of cytoplasmic (CAc) and membrane-associated form (CAg) of CA, NKA α subunit and HAT subunit a in gills of freshwater crayfish, Cherax quadricarinatus, at three pH levels – 6.2, 7.2 (control) and 8.2 – over 24 h. Expression levels of CAc were significantly increased at low pH and decreased at high pH conditions 24 h after transfer. Expression increased at low pH after 12 h, and reached its maximum level by 24 h. CAg showed a significant increase in expression at 6 h after transfer at low pH. Expression of NKA significantly increased at 6 h after transfer to pH 6.2 and remained elevated for up to 24 h. Expression for HAT and NKA showed similar patterns, where expression significantly increased 6 h after transfer to low pH and remained significantly elevated throughout the experiment. Overall, CAc, CAg, NKA and HAT gene expression is induced at low pH conditions in freshwater crayfish.

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Distinctive Responses of Ribulose-1,5-Bisphosphate Carboxylase and Carbonic Anhydrase in Wheat Leaves to Nitrogen Nutrition and their Possible Relationships to CO2-Transfer Resistance

PLANT PHYSIOLOGY ◽

10.1104/pp.100.4.1737 ◽

1992 ◽

Vol 100 (4) ◽

pp. 1737-1743 ◽

Cited By ~ 135

Author(s):

Amane Makino ◽

Hiroshi Sakashita ◽

Jun Hidema ◽

Tadahiko Mae ◽

Kunihiko Ojima ◽

...

Keyword(s):

Carbonic Anhydrase ◽

Nitrogen Nutrition ◽

Transfer Resistance ◽

Bisphosphate Carboxylase ◽

Wheat Leaves

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A two-dimensional compartment model for the reaction-diffusion system of acetylcholine in the synaptic cleft at the neuromuscular junction

Biosystems ◽

10.1016/s0303-2647(96)01659-0 ◽

1997 ◽

Vol 41 (1) ◽

pp. 17-27 ◽

Cited By ~ 8

Author(s):

Takashi Naka ◽

Kosuke Shiba ◽

Naoto Sakamoto

Keyword(s):

Neuromuscular Junction ◽

Reaction Diffusion ◽

Compartment Model ◽

Synaptic Cleft ◽

Reaction Diffusion System ◽

Diffusion System ◽

Two Dimensional

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Impacts of UV radiation on growth and photosynthetic carbon acquisition in Gracilaria lemaneiformis (Rhodophyta) under phosphorus-limited and replete conditions

Functional Plant Biology ◽

10.1071/fp09092 ◽

2009 ◽

Vol 36 (12) ◽

pp. 1057 ◽

Cited By ~ 25

Author(s):

Zhiguang Xu ◽

Kunshan Gao

Keyword(s):

Growth Rate ◽

Carbonic Anhydrase ◽

Photosynthetic Efficiency ◽

Inorganic Carbon ◽

Inorganic Phosphorus ◽

Gracilaria Lemaneiformis ◽

Solar Ultraviolet Radiation ◽

Relative Growth ◽

Photosynthetic Carbon ◽

Solar Ultraviolet

Solar ultraviolet radiation (UVR, 280–400 nm) is known to negatively affect macroalgal growth and photosynthesis, while phosphorus availability may affect their sensitivity to UVR. Here, we show that UV-A enhanced the growth rate of the red macroalga, Gracilaria lemaneiformis Bory de Saint-Vincent under inorganic phosphorus (Pi)-replete but reduced it under Pi-limited conditions. Maximal net photosynthetic rates were significantly reduced by both UV-A and UV-B, but the apparent photosynthetic efficiency was enhanced in the presence of UV-A. The UV-induced inhibition was exacerbated under Pi-limited conditions. The activity of total carbonic anhydrase was enhanced and the photosynthetic affinity for exogenous inorganic carbon (Ci) was raised for thalli grown in the presence of UVR under both Pi-replete and Pi-limited conditions. The relative growth rate was closely related to Ci acquisition capability (Vmax/KDIC), which was enhanced by UVR exposure under Pi-replete but not significantly affected under Pi-limited conditions.

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Effect of CO2 Concentration on Carbonic Anhydrase and Ribulose-1,5-Bisphosphate Carboxylase/Oxygenase Expression in Pea

PLANT PHYSIOLOGY ◽

10.1104/pp.112.2.569 ◽

1996 ◽

Vol 112 (2) ◽

pp. 569-574 ◽

Cited By ~ 51

Author(s):

N. Majeau ◽

J. R. Coleman

Keyword(s):

Carbonic Anhydrase ◽

Co2 Concentration ◽

Bisphosphate Carboxylase

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THE ACQUISITION OF INORGANIC CARBON IN MARINE MACROPHYTES

Israel Journal of Plant Sciences ◽

10.1080/07929978.1998.10676714 ◽

1998 ◽

Vol 46 (2) ◽

pp. 83-87 ◽

Cited By ~ 2

Author(s):

Sven Beer

Keyword(s):

Carbonic Anhydrase ◽

Aquatic Plants ◽

Inorganic Carbon ◽

External Medium ◽

Uptake Mechanism ◽

Tropical Regions ◽

Marine Macrophytes ◽

Photosynthetic Carbon ◽

Diffusion Rates ◽

Carbon Transport

The low diffusion rates of solutes in water call for a separation of photosynthetic carbon acquirement in aquatic plants into carbon transport and the subsequent photosynthetic reduction of CO2. This paper will focus on the transport of inorganic carbon from the external medium to the site of fixation in marine macrophytes. In accord with the much higher concentration of HCO3− than of CO2 in seawater, most marine macrophytes can utilize the ionic carbon form for their photosynthetic needs. The two known ways of HCO, utilization are (a) via extracellular, carbonic anhydrase catalyzed dehydration of HCO3− to form CO2, which then diffuses into the photosynthesizing cells, and (b) by direct uptake via a transporter. While the first way may be sufficient to support low rates of photosynthesis in temperate regions, it is viewed as futile under situations where high temperatures and irradiances would cause a high pH to form close to the uptake site of carbon and where, consequently, the CO2/HCO3− ratio would be very low. Therefore, it may well be that the direct HCO3− uptake mechanism described for Ulva from more tropical regions confers an adaptational advantage under conditions conducive to higher photosynthetic rates.

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In situ Immunofluorescent Labelling of Ribulose-1,5-Bisphosphate Carboxylase in Leaves of C3 and C4 Plants

Functional Plant Biology ◽

10.1071/pp9770523 ◽

1977 ◽

Vol 4 (4) ◽

pp. 523 ◽

Cited By ~ 64

Author(s):

PW Hattersley ◽

L Watson ◽

CB Osmond

Keyword(s):

Leaf Anatomy ◽

Bisphosphate Carboxylase ◽

Carbon Reduction ◽

C4 Species ◽

Photosynthetic Carbon ◽

Photosynthetic Carbon Metabolism ◽

Plant Families ◽

Indirect Technique ◽

Cam Species ◽

Species Specific

Antibodies raised to wheat and spinach ribulose-1,5-bisphosphate carboxylase (RuP2Case) have been used to locate the enzyme in hand-cut leaf blade transections of 40 C3 and C4 species, and one crassulacean acid metabolism (CAM) plant by immunofluorescence (using the indirect technique). The sample includes species from seven plant families, both monocotyledons and dicotyledons. In C3 and CAM species, specific fluorescence is associated with chloroplasts of all leaf chlorenchymatous cells when labelled with anti-RuP2 Case, while in species with 'classical' C4 leaf anatomy RuP2 Case is located almost exclusively in 'bundle sheath' ['Kranz' or 'photosynthetic carbon reduction' (PCR)] cell chloroplasts. Ten C4 species exhibit various types of 'non-classical' C4 leaf anatomy (Alloteropsis, Aristida, Arundinella, Cyperus, Fimbristylis, Triodia and Salsola types) and, for all but one of these types, immunofluorescent labelling of RuP2 Case provides the first direct experimental evidence of a cellular compartmentation of photosynthetic carbon metabolism and of the location of PCR compartments. Leaves of two Atriplex C3/C4 hybrid individuals and of Panicum milioides, a putative C3/C4 intermediate, exhibited a C3 antibody labelling response.

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Ultraviolet radiation stimulated activity of extracellular carbonic anhydrase in the marine diatom Skeletonema costatum

Functional Plant Biology ◽

10.1071/fp08172 ◽

2009 ◽

Vol 36 (2) ◽

pp. 137 ◽

Cited By ~ 27

Author(s):

Hongyan Wu ◽

Kunshan Gao

Keyword(s):

Carbonic Anhydrase ◽

Ultraviolet Radiation ◽

Uv Radiation ◽

Carbon Fixation ◽

Skeletonema Costatum ◽

Marine Phytoplankton ◽

Marine Diatom ◽

Redox Activity ◽

Photosynthetic Carbon Fixation ◽

Photosynthetic Carbon

Previous studies have shown that reduced levels of solar UV radiation (280–400 nm) can enhance photosynthetic carbon fixation of marine phytoplankton, but the mechanisms are not known. The supply of CO2 for photosynthesis is facilitated by extracellular (periplasmic) carbonic anhydrase (CAe) in most marine phytoplankton species. The present study showed that the CAe activity of Skeletonema costatum (Greville) Cleve was stimulated when treated with UV-A (320–395 nm) or UV-A + UV-B (295–320 nm) in addition to visible radiation. The presence of UV-A and UV-B enhanced the activity by 28% and 24%, respectively, at a low irradiance (PAR 161, UV-A 28, UV-B 0.9 W m−2) and by 21% and 19%, respectively, at a high irradiance (PAR 328, UV-A 58, UV-B 1.9 W m−2) level after exposure for 1 h. Ultraviolet radiation stimulated CAe activity contributed up to 6% of the photosynthetic carbon fixation as a result of the enhanced supply of CO2, as revealed using the CAe inhibitor (acetazolamide). As a result, there was less inhibition of photosynthetic carbon fixation compared with the apparent quantum yield of PSII. The UV radiation stimulated CAe activity coincided with the enhanced redox activity at the plasma membrane in the presence of UV-A and/or UV-B. The present study showed that UV radiation can enhance CAe activity, which plays an important role in counteracting UV inhibition of photosynthesis.

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