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PHYSIOLOGY AND METABOLISM

Involvement of the cynABDS Operon and the CO2-Concentrating Mechanism in the Light-Dependent Transport and Metabolism of Cyanate by Cyanobacteria

George S. Espie, Farid Jalali, Tommy Tong, Natalie J. Zacal, Anthony K.-C. So
George S. Espie
Department of Biology, University of Toronto at Mississauga, Mississauga, Ontario L5L 1C6, Canada
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  • For correspondence: espie@utm.utoronto.ca
Farid Jalali
Department of Biology, University of Toronto at Mississauga, Mississauga, Ontario L5L 1C6, Canada
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Tommy Tong
Department of Biology, University of Toronto at Mississauga, Mississauga, Ontario L5L 1C6, Canada
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Natalie J. Zacal
Department of Biology, University of Toronto at Mississauga, Mississauga, Ontario L5L 1C6, Canada
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Anthony K.-C. So
Department of Biology, University of Toronto at Mississauga, Mississauga, Ontario L5L 1C6, Canada
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DOI: 10.1128/JB.01328-06
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  • FIG. 1.
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    FIG. 1.

    Time course (180 s) of NCO− uptake in the light for Synechococcus sp. strain UTEX 625 standing culture cells provided with 1 mM KO14CN, as determined by method A. Shown are total uptake (○), the acid-stable products of C-fixation (•), and the acid-labile intracellular pool of NCO− + Ci (▪). Data are the average of three replicates ±10.4% (maximum). Also shown (dashed line) is the calculated intracellular pool of NCO− corrected for intracellular Ci.

  • FIG. 2.
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    FIG. 2.

    Typical time course (25 min) of NCO− uptake and utilization by S. elongatus PCC7942 wild type (WT) and the cynA mutant (::cynA). Cells grown in standing culture with low Ci concentrations were provided with 1 mM KO14CN in the light. Uptake and accumulation of 14C was determined as described in method B. (A) Simultaneous measurements of cyanate-dependent CO2 fixation (•) and O2 evolution (○) for the wild type and the cynA mutant. (B) Intracellular accumulation of acid-labile NCO− + Ci (▪) for the wild type and the cynA mutant (::cynA).

  • FIG. 3.
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    FIG. 3.

    Effect of KOCN on HCO3 − and CO2 transport in Synechococcus sp. strain UTEX 625 cells grown in standing culture. The initial rate (20 s) of HCO3 − transport was measured (method C) at substrate concentrations of 50 μM (•) and 250 μM (○) in pH 8 buffer to determine the effect of increasing [KOCN] on Na+-independent HCO3 − transport in the presence of 100 μM NaCl (A) or Na+-dependent HCO3 − transport in the presence 30 mM NaCl (B). (C) The initial rate (10 s) of CO2 transport (▪) was measured at 10 μM in the presence of 100 μM NaCl (method D). Also shown is the effect of KOCN on CO2 transport in cells grown under high-Ci conditions(⋄). The data are the average of six determinations ± standard deviations.

  • FIG. 4.
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    FIG. 4.

    KOCN-dependent CO2 efflux by cells grown under high-CO2 conditions. Illuminated wild-type (WT) S. elongatus PCC7942 cells were provided with 1 mM KO13CN, and the efflux of 13CO2 was followed by MS over time in the absence or presence of 25 mM NaNO3 or NaNO2. Bovine CA was added to the suspension to illustrate that CO2 was the Ci species arising in the cell suspensions. Also shown are the CO2 fluxes arising from the cynA and cynS mutants and from Synechocystis sp. strain PCC6803 grown in high-CO2 concentrations.

  • FIG. 5.
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    FIG. 5.

    Measurements of KOCN-dependent O2 evolution (A) and Chl a fluorescence quenching (B) in S. elongatus PCC7942 wild-type (WT) cells and the cynA and cynS mutants. Cells grown under low-Ci conditions were allowed to deplete the medium of Ci in the light. Cells were then provided with 1 mM KOCN, and O2 evolution and Chl a fluorescence quenching were measured simultaneously over time. Once a steady state was achieved, Ci-dependent O2 evolution and Chl a fluorescence quenching were also measured following the addition of 25 μM Ci to the cell suspensions. Also shown in panel A is the response of Synechocystis sp. strain PCC6803 to the addition of 1 mM KOCN.

  • FIG. 6.
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    FIG. 6.

    Effect of KOCN on CO2 transport. S. elongatus PCC7942 cynA mutant cells grown under low-Ci conditions were placed in the reaction chamber attached to the MS and allowed to equilibrate (25 mM BTP-HCl buffer, pH 8, at 30°C) in the light (300 μmol of photons m−2 s−1) in the presence of KOCN. CO2 transport was initiated by adding 3.5 μM CO2 to the reaction vessel, and its concentration was followed over time. The difference between the curves obtained in the light (A, 0 mM KOCN, maximum uptake) and the dark (F, no uptake) was taken as a measure of CO2 transport. The effect of 1, 3, 5, or 10 mM KOCN (B, C, D, and E) on CO2 transport are also shown.

  • FIG. 7.
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    FIG. 7.

    Involvement of the cyanobacterial CCM in cyanate metabolism. (A) Time course of KOCN-dependent 12CO2 efflux in the light (solid lines) and dark (dashed lines). S. elongatus strain PCC7942 ΔchpX ΔchpY cells grown on 5% CO2 were suspended in 100 mM EPPS (N-[2-hydroxyethyl]piperazine-N′-[3-propanesulfonic acid]) buffer, pH 8, and incubated in the light or dark for 5 min in the reaction cuvette, in the absence and presence of 10 mM NaH13CO3 (13Ci). The experiment was started by the addition of 1 mM KOCN, and 12CO2 efflux was measured over time by MS. (B) Dependence of 12Ci efflux rate on 13Ci concentration. The average rate of 12Ci efflux, at a constant cell density (7.5 μg of Chl a ml−1), was calculated from 12CO2 efflux measurements over an 8-min interval as a function of 13Ci concentration for ΔchpX ΔchpY (chpXY) cells in the light (•) and dark (○) provided with 1 mM KOCN. Also shown (dashed line and ▴) is the dependence on 13Ci concentration of 12CO2 efflux in S. elongatus PCC7942 wild-type (WT) cells grown under low-Ci conditions.

  • FIG. 8.
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    FIG. 8.

    Unrooted phylogenetic tree illustrating the relationship between CynA proteins identified from bacterial sources and NrtA and CmpA from cyanobacteria. Cyanobacterial species are as follows: S. elongatus PCC7942, Synechococcus sp. strain PCC6301, Synechocystis sp. strain PCC6803, Thermosynechococcus elongatus BP-1, Cyanothece sp. strain PCC8801, Nostoc sp. strain PCC7120, Anabaena variabilis ATCC 29413, Gloeobacter violaceus PCC7421, Synechococcus sp. strain WH8102, and P. marinus CCMP1986. Other organisms are Rhodopseudomonas palustris strains CGA009, BisA53, and HaA2; Xanthobacter autotrophicus Py2; Bradyrhizobium japonicum USDA 110; Bradyrhizobium sp. strain BTAi1; Roseovarius sp. strain R217; Alkalilimnicola ehrlichei MLHE-1; Polaromonas sp. strain JS666; Rubrivivax gelatinosus PM1; Rhodoferax ferrireducens T118; Methylobacillus flagellatus KT; and Pseudomonas aeruginosa PA2192. Organisms are represented on the figure generally by the strain designation or culture collection number.

Tables

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  • TABLE 1.

    Characterization of NCO− uptake and metabolism in Synechococcus sp. strain UTEX 625

    Experimental conditionsaN14CO− uptake (% of control)14C fixation (% of control)
    Light (control)100100
    Dark6.32.4
    Light + 25 μM DCMU7.92.2
    Light + 15 mM glycolaldhyde59.15.6
    Light + 15 mM oxalate8899.7
    Light + 1 mM ethoxyzolamide3932.3
    • ↵ a NCO− uptake and C fixation were measured by the silicone fluid filtering centrifugation technique using method A. Cells grown in standing culture were incubated with 1 mM KO14CN for 2 min in BTP/HCl buffer, pH 8.0, containing 25 mM NaCl at 30°C and illuminated at 300 μmol m−2 s−1. Data are the average of 5 experiments in triplicate ±6.5%.

  • TABLE 2.

    Effect of [12Ci] on N14 CO− transport by Synechococcus sp. strain UTEX 625 grown in standing culturea

    Experimental condition (with 1 mM KO14CN)% of control value at 20 s % of control value at 2 min
    N14CO− uptakePool14C fixationN14CO− uptakePool14C fixation
    0 mM KHCO3 100100b 100c 100100d 100e
    2 mM KHCO3 48.2 ± 9.345.4 ± 16.247.5 ± 21.638.4 ± 15.241.0 ± 12.924.9 ± 10.6
    5 mM KHCO3 49.4 ± 7.346.4 ± 19.342.9 ± 12.239.6 ± 14.641.5 ± 18.730.4 ± 19.7
    • ↵ a Values were determined using method C in BTP-HCl buffer, pH 8, containing 25 mM NaCl. Light was supplied at 300 μmol of photons m−2 s−1. Data are the average of seven experiments ± standard deviations.

    • ↵ b Control value, 6.0 ± 2.0 mM.

    • ↵ c Control value, 0.06 μmol of C mg−1 Chl.

    • ↵ d Control value, 11.0 ± 7.0 mM.

    • ↵ e Control value, 0.23 μmol of C mg−1 Chl.

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Involvement of the cynABDS Operon and the CO2-Concentrating Mechanism in the Light-Dependent Transport and Metabolism of Cyanate by Cyanobacteria
George S. Espie, Farid Jalali, Tommy Tong, Natalie J. Zacal, Anthony K.-C. So
Journal of Bacteriology Jan 2007, 189 (3) 1013-1024; DOI: 10.1128/JB.01328-06

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Involvement of the cynABDS Operon and the CO2-Concentrating Mechanism in the Light-Dependent Transport and Metabolism of Cyanate by Cyanobacteria
George S. Espie, Farid Jalali, Tommy Tong, Natalie J. Zacal, Anthony K.-C. So
Journal of Bacteriology Jan 2007, 189 (3) 1013-1024; DOI: 10.1128/JB.01328-06
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KEYWORDS

carbon dioxide
Cyanates
cyanobacteria
operon

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