Bacterial Na+- or H+-coupled ATP Synthases Operating at Low Electrochemical Potential

doi:10.1016/S0065-2911(04)49004-3

Advances in Microbial Physiology

Volume 49, 2004, Pages 175-218

https://doi.org/10.1016/S0065-2911(04)49004-3 Get rights and content

Abstract

In certain strictly anaerobic bacteria, the energy for growth is derived entirely from a decarboxylation reaction. A prominent example is Propionigenium modestum, which converts the free energy of the decarboxylation of (S)-methylmalonyl-CoA to propionyl-CoA (ΔG°=−20.6 kJ/mol) into an electrochemical Na⁺ ion gradient across the membrane. This energy source is used as a driving force for ATP synthesis by a Na⁺-translocating F₁F₀ ATP synthase. According to bioenergetic considerations, approximately four decarboxylation events are necessary to support the synthesis of one ATP. This unique feature of using Na⁺ instead of H⁺ as the coupling ion has made this ATP synthase the paradigm to study the ion pathway across the membrane and its relationship to rotational catalysis. The membrane potential (Δψ) is the key driving force to convert ion translocation through the F₀ motor components into torque. The resulting rotation elicits conformational changes at the catalytic sites of the peripheral F₁ domain which are instrumental for ATP synthesis. Alkaliphilic bacteria also face the challenge of synthesizing ATP at a low electrochemical potential, but for entirely different reasons. Here, the low potential is not the result of insufficient energy input from substrate degradation, but of an inverse pH gradient. This is a consequence of the high environmental pH where these bacteria grow and the necessity to keep the intracellular pH in the neutral range. In spite of this unfavorable bioenergetic condition, ATP synthesis in alkaliphilic bacteria is coupled to the proton motive force (ΔμH⁺) and not to the much higher sodium motive force (ΔμNa⁺). A peculiar feature of the ATP synthases of alkaliphiles is the specific inhibition of their ATP hydrolysis activity. This inhibition appears to be an essential strategy for survival at high external pH: if the enzyme were to operate as an ATPase, protons would be pumped outwards to counteract the low ΔμH⁺, thus wasting valuable ATP and compromising acidification of the cytoplasm at alkaline pH.

Section snippets

INTRODUCTION

Bacteria are remarkably versatile organisms degrading a wide variety of organic substrates under diverse environmental conditions. Anaerobic bacteria, in general, gain much less energy from substrate degradation compared to their aerobic counterparts, and in some species the degradation of more than one substrate molecule is required to fulfill energetic requirements for the synthesis of one ATP. A prominent example is Propionigenium modestum, which grows from the fermentation of succinate to

ATP SYNTHESIS IN ANAEROBIC BACTERIA AT LOW ELECTROCHEMICAL POTENTIAL

Many anaerobic bacteria perform a chemiosmotic ATP synthesis mechanism like their aerobic counterparts. In special cases when the energy from substrate degradation is not sufficient to support the synthesis of stoichiometric amounts of ATP, the chemiosmotic ATP synthesis mechanism is obligatory. The free energy derived from the degradation of several substrate molecules is stored in the electrochemical ion gradient over the membrane which thus becomes sufficient to drive the synthesis of ATP. A

ALKALIPHILIC BACTERIA GROWING AT LOW ΔμH⁺

Like anaerobic bacteria, alkaliphilic bacteria are also faced with the challenge of synthesizing ATP at low ΔμH⁺. Alkaliphilic bacteria grow over the pH range 7.5–11.5 and can be divided into two groups: obligate alkaliphiles that grow between pH 9.0 and pH 11.5 (e.g. Bacillus alcalophilus, Bacillus firmus RAB) and facultative alkaliphiles that grow between pH values of pH 7.5 and 11.2 (e.g. Bacillus pseudofirmus OF4 and Bacillus halodurans C-125) (Krulwich and Guffanti, 1989). Recently, a

Acknowledgements

Work in GMC’s laboratory was supported by a Marsden grant from the Royal Society of New Zealand, work in PD’s laboratory was supported by the Swiss National Science Foundation and Research Commission of ETH Zürich.

References (150)

W. Buckel
Sodium ion-translocating decarboxylases
Biochim. Biophys. Acta
(2001)
E. Cabezón et al.
Dimerization of bovine F₁-ATPase by binding the inhibitor protein, IF₁
J. Biol. Chem.
(2000)
E. Cabezón et al.
Modulation of the oligomerization state of the bovine F₁-ATPase inhibitor protein, IF₁, by pH
J. Biol. Chem.
(2000)
B.D. Cain et al.
Proton translocation by the F₁F₀ ATPase of Escherichia coli. Mutagenic analysis of the a subunit
J. Biol. Chem.
(1989)
R.A. Capaldi et al.
Mechanism of the F₁F₀-type ATP synthase, a biological rotary motor
Trends Biochem. Sci.
(2002)
D.J. Cipriano et al.
Genetic fusions of globular proteins to the ϵ subunit of the Escherichia coli ATP synthase: Implications for in vivo rotational catalysis and ϵ subunit function
J. Biol. Chem.
(2002)
P. Dimroth
The ATPases of Propionigenium modestum and Bacillus alcalophilus. Strategies for ATP synthesis under low energy conditions
Biochim. Biophys. Acta
(1992)
P. Dimroth
Primary sodium ion translocating enzymes
Biochim. Biophys. Acta
(1997)
P. Dimroth et al.
Coupling mechanism of the oxaloacetate decarboxylase Na⁺ pump
Biochim. Biophys. Acta
(2001)
R.H. Fillingame et al.
Coupling proton movements to c-ring rotation in F₁F₀ ATP synthase: aqueous access channels and helix rotations at the a–c interface
Biochim. Biophys. Acta
(2002)

R.H. Fillingame et al.

Structural interpretations of F₀ rotary function in the Escherichia coli F₁F₀ ATP synthase

Biochim. Biophys. Acta

(2000)

A.C. Gemperli et al.

The respiratory complex I (NDH I) from Klebsiella pneumoniae, a sodium pump

J. Biol. Chem.

(2002)

R. Gilmour et al.

Purification and characterization of the succinate dehydrogenase complex and CO-reactive b-type cytochromes from the facultative alkaliphile Bacillus firmus OF4

Biochim. Biophys. Acta

(1996)

G. Gottschalk et al.

The Na⁺ translocating methyltransferase complex from methanogenic archea

Biochim. Biophys. Acta

(2001)

A.A. Guffanti et al.

Failure of an alkalophilic bacterium to synthesize ATP in response to a valinomycin-induced potassium diffusion potential at high pH

Arch. Biochem. Biophys.

(1985)

A.A. Guffanti et al.

A transmembrane electrical potential generated by respiration is not equivalent to a diffusion potential of the same magnitude for ATP synthesis by Bacillus firmus RAB

J. Biol. Chem.

(1984)

A.A. Guffanti et al.

Features of apparent non-chemiosmotic energization of oxidative phosphorylation by alkaliphilic Bacillus firmus OF4

J. Biol. Chem.

(1992)

P.E. Hartzog et al.

Second-site suppressor mutations at glycine 218 and histidine 245 in the α subunit of F₁F₀ ATP synthase in Escherichia coli

J. Biol. Chem.

(1994)

L.P. Hatch et al.

The essential arginine residue at position 210 in the a subunit of the Escherichia coli ATP synthase can be transferred to position 252 with partial retention of activity

J. Biol. Chem.

(1995)

M. Hayashi et al.

Recent progress in the Na⁺-translocating NADH-quinone reductase from the marine Vibrio alginolyticus

Biochim. Biophys. Acta

(2001)

D.B. Hicks et al.

Purification and reconstitution of the F₁F₀-ATP synthase from alkaliphilic Bacillus firmus OF4. Evidence that the enzyme translocates H⁺ but not Na⁺

J. Biol. Chem.

(1990)

D.B. Hicks et al.

The respiratory chain of alkaliphilic bacteria

Biochim. Biophys. Acta

(1995)

Y. Imae et al.

Sodium-driven flagellar motors of alkalophilic Bacillus

Methods Enzymol.

(1986)

D.M. Ivey et al.

Molecular cloning and sequencing of a gene from alkaliphilic Bacillus firmus OF4 that functionally complements an Escherichia coli strain carrying a deletion in the nhaA Na⁺/H⁺ antiporter gene

J. Biol. Chem.

(1991)

D.M. Ivey et al.

Two unrelated alkaliphilic Bacillus species possess identical deviations in sequence from those of other prokaryotes in regions of F₀ proposed to be involved in proton translocation through the ATP synthase

Res. Microbiol.

(1992)

P.J. Jackson et al.

The mitochondrial ATP synthase inhibitor protein binds near the C-terminus of the F₁ beta-subunit

FEBS Lett.

(1988)

W. Junge et al.

ATP synthase: An electrochemical transducer with rotatory mechanics

Trends Biochem. Sci.

(1997)

G. Kaim et al.

ATP synthesis by the F₁F₀ ATP synthase of Escherichia coli is obligatorily dependent on the electric potential

FEBS Lett.

(1998)

G. Kaim et al.

Coupled rotation within single F₀F₁ enzyme complexes during ATP synthesis or hydrolysis

FEBS Lett.

(2002)

C. Kluge et al.

Specific protection by Na⁺ or Li⁺ of the F₁F₀-ATPase of Propionigenium modestum from the reaction with dicyclohexylcarbodiimide

J. Biol. Chem.

(1993)

N. Koyama et al.

Na⁺-dependent uptake of amino acids by an alkalophilic Bacillus

FEBS Lett.

(1976)

T.A. Krulwich et al.

Presence of a nonmetabolizable solute that is translocated with Na⁺ enhances Na⁺-dependent pH homeostasis in an alkalophilic Bacillus

J. Biol. Chem.

(1985)

T.A. Krulwich et al.

Energetics of alkaliphilic Bacillus species: physiology and molecules

Adv. Microb. Physiol.

(1998)

T.A. Krulwich et al.

The Na⁺- dependence of alkaliphily in Bacillus

Biochim. Biophys. Acta

(2001)

R.N. Lightowlers et al.

The proton pore in Escherichia coli F₀F₁-ATPase: A requirement of arginine at position 210 of the a-subunit

Biochim. Biophys. Acta

(1987)

T. Meier et al.

The central plug in the reconstituted undecameric c cylinder of a bacterial ATP synthase consists of phospholipids

FEBS Lett.

(2001)

D.J. Müller et al.

ATP synthase: constrained stoichiometry of the transmembrane rotor

FEBS Lett.

(2001)

V. Müller et al.

The Na⁺ cycle in Acetobacterium woodii: identification and characterization of a Na⁺ translocating F₁F₀-ATPase with a mixed oligomer of 8 and 16 kDa proteolipids

Biochim. Biophys. Acta

(2001)

J.P. Abrahams et al.

The structure of bovine F₁-ATPase complexed with the peptide antibiotic efrapeptin

Proc. Natl. Acad. Sci. USA

(1996)

J.P. Abrahams et al.

Structure at 2.8 Å resolution of F₁-ATPase from bovine heart mitochondria

Nature

(1994)

R. Birkenhäger et al.

The F₀ complex of the Escherichia coli ATP synthase. Investigation by electron spectroscopic imaging and immunoelectron microscopy

Eur. J. Biochem.

(1995)

M. Bott

Anaerobic citrate metabolism and its regulation in enterobacteria

Arch. Microbiol.

(1997)

M. Bott et al.

Regulation of anaerobic citrate metabolism in Klebsiella pneumoniae

Mol. Microbiol.

(1995)

M. Bott et al.

Methylmalonyl-CoA decarboxylase from Propionigenium modestum: cloning and sequencing of the structural genes and purification of the enzyme complex

Eur. J. Biochem.

(1997)

W. Buckel et al.

Purification, characterization and reconstitution of glutaconyl-CoA decarboxylase, a biotin-dependent sodium pump from anaerobic bacteria

Eur. J. Biochem.

(1983)

E. Cabezón et al.

The structure of bovine IF₁, the regulatory subunit of mitochondrial F-ATPase

EMBO J.

(2001)

G.M. Cook et al.

Purification and biochemical characterization of the F₁F₀-ATP synthase from thermoalkaliphilic Bacillus sp. strain TA2.A1

J. Bacteriol.

(2003)

M. Di Berardino et al.

Aspartate 203 of the oxaloacetate decarboxylase β-subunit catalyses both the chemical and vectorial reaction of the Na⁺ pump

EMBO J.

(1996)

P. Dimroth

The generation of an electrochemical gradient of sodium ions upon decarboxylation of oxaloacetate by the membrane-bound and Na⁺-activated oxaloacetate decarboxylase from Klebsiella aerogenes

Eur. J. Biochem.

(1982)

P. Dimroth

Sodium ion transport decarboxylases and other aspects of sodium ion cycling in bacteria

Microbiol. Rev.

(1987)

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Bacterial Na+- or H+-coupled ATP Synthases Operating at Low Electrochemical Potential

Abstract

Section snippets

INTRODUCTION

ATP SYNTHESIS IN ANAEROBIC BACTERIA AT LOW ELECTROCHEMICAL POTENTIAL

ALKALIPHILIC BACTERIA GROWING AT LOW ΔμH+

Acknowledgements

Biochim. Biophys. Acta

J. Biol. Chem.

J. Biol. Chem.

J. Biol. Chem.

Trends Biochem. Sci.

J. Biol. Chem.

Biochim. Biophys. Acta

Biochim. Biophys. Acta

Biochim. Biophys. Acta

Biochim. Biophys. Acta

Biochim. Biophys. Acta

J. Biol. Chem.

Biochim. Biophys. Acta

Biochim. Biophys. Acta

Arch. Biochem. Biophys.

J. Biol. Chem.

J. Biol. Chem.

J. Biol. Chem.

J. Biol. Chem.

Biochim. Biophys. Acta

J. Biol. Chem.

Biochim. Biophys. Acta

Methods Enzymol.

J. Biol. Chem.

Res. Microbiol.

FEBS Lett.

Trends Biochem. Sci.

FEBS Lett.

FEBS Lett.

J. Biol. Chem.

FEBS Lett.

J. Biol. Chem.

Adv. Microb. Physiol.

Biochim. Biophys. Acta

Biochim. Biophys. Acta

FEBS Lett.

FEBS Lett.

Biochim. Biophys. Acta

The structure of bovine F1-ATPase complexed with the peptide antibiotic efrapeptin

Proc. Natl. Acad. Sci. USA

Structure at 2.8 Å resolution of F1-ATPase from bovine heart mitochondria

Nature

The F0 complex of the Escherichia coli ATP synthase. Investigation by electron spectroscopic imaging and immunoelectron microscopy

Eur. J. Biochem.

Anaerobic citrate metabolism and its regulation in enterobacteria

Arch. Microbiol.

Regulation of anaerobic citrate metabolism in Klebsiella pneumoniae

Mol. Microbiol.

Methylmalonyl-CoA decarboxylase from Propionigenium modestum: cloning and sequencing of the structural genes and purification of the enzyme complex

Eur. J. Biochem.

Purification, characterization and reconstitution of glutaconyl-CoA decarboxylase, a biotin-dependent sodium pump from anaerobic bacteria

Eur. J. Biochem.

The structure of bovine IF1, the regulatory subunit of mitochondrial F-ATPase

EMBO J.

Purification and biochemical characterization of the F1F0-ATP synthase from thermoalkaliphilic Bacillus sp. strain TA2.A1

J. Bacteriol.

Aspartate 203 of the oxaloacetate decarboxylase β-subunit catalyses both the chemical and vectorial reaction of the Na+ pump

EMBO J.

The generation of an electrochemical gradient of sodium ions upon decarboxylation of oxaloacetate by the membrane-bound and Na+-activated oxaloacetate decarboxylase from Klebsiella aerogenes

Eur. J. Biochem.

Sodium ion transport decarboxylases and other aspects of sodium ion cycling in bacteria

Microbiol. Rev.

Bacterial Na⁺- or H⁺-coupled ATP Synthases Operating at Low Electrochemical Potential

ALKALIPHILIC BACTERIA GROWING AT LOW ΔμH⁺

The structure of bovine F₁-ATPase complexed with the peptide antibiotic efrapeptin

Structure at 2.8 Å resolution of F₁-ATPase from bovine heart mitochondria

The F₀ complex of the Escherichia coli ATP synthase. Investigation by electron spectroscopic imaging and immunoelectron microscopy

The structure of bovine IF₁, the regulatory subunit of mitochondrial F-ATPase

Purification and biochemical characterization of the F₁F₀-ATP synthase from thermoalkaliphilic Bacillus sp. strain TA2.A1

Aspartate 203 of the oxaloacetate decarboxylase β-subunit catalyses both the chemical and vectorial reaction of the Na⁺ pump

The generation of an electrochemical gradient of sodium ions upon decarboxylation of oxaloacetate by the membrane-bound and Na⁺-activated oxaloacetate decarboxylase from Klebsiella aerogenes