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Biochemical Society Transactions (2012) Volume 40, part 6
Mineral respiration under extreme acidic
conditions: from a supramolecular organization
to a molecular adaptation in Acidithiobacillus
ferrooxidans
Magali Roger*, Cindy Castelle†, Marianne Guiral*, Pascale Infossi*, Elisabeth Lojou*, Marie-Thérèse Giudici-Orticoni*
and Marianne Ilbert*1
*Unité de Bioénergétique et Ingénierie des Protéines, Institut de Microbiologie de la Méditerranée – CNRS, Aix-Marseille University, 31 Chemin Joseph
Aiguier, 13402 Marseille Cedex 20, France and †Earth Sciences Division, Lawrence Berkeley National Laboratory, 1 Cyclotron Road, Berkeley, CA 94720, U.S.A.
Abstract
Acidithiobacillus ferrooxidans is an acidophilic chemolithoautotrophic Gram-negative bacterium that can
derive energy from the oxidation of ferrous iron at pH 2 using oxygen as electron acceptor. The study
of this bacterium has economic and fundamental biological interest because of its use in the industrial
extraction of copper and uranium from ores. For this reason, its respiratory chain has been analysed in detail
in recent years. Studies have shown the presence of a functional supercomplex that spans the outer and
the inner membranes and allows a direct electron transfer from the extracellular Fe2 + ions to the inner
membrane cytochrome c oxidase. Iron induces the expression of two operons encoding proteins implicated
in this complex as well as in the regeneration of the reducing power. Most of these are metalloproteins
that have been characterized biochemically, structurally and biophysically. For some of them, the molecular
basis of their adaptation to the periplasmic acidic environment has been described. Modifications in the
metal surroundings have been highlighted for cytochrome c and rusticyanin, whereas, for the cytochrome c
oxidase, an additional partner that maintains its stability and activity has been demonstrated recently.
Introduction
Micro-organisms are found in various ecosystems as they
are adapted to their surroundings, in some of which life
is sometimes hardly considered possible. Studying these
organisms is challenging for researchers on account of
the difficulty of reproducing their natural environments
in the laboratory. Discovery of new concepts is the driving
force that motivates researchers in this field beyond the
difficulties linked to the unfriendly environments. In one of
these environments, which combines acid and iron which are
known as stress factors for ‘classic’ organisms, iron-oxidizing
organisms have been discovered that drive their energy using
ferrous iron (Fe2 + ) as electron donor. In the present minireview, we first describe how life is possible in the presence
of acid and iron, and we focus on one of these peculiar
organisms, Acidithiobacillus ferrooxidans. This bacterium
represents one of the most studied model organisms
to understand life in acidic environments, adaptation to
toxic metals and use of minerals containing iron as an
energy source. As early as 1982, Ingledew [1] described
A. ferrooxidans as “one of Nature’s most unusual bioenergetic
phenomena” owing to several challenges that it has to face.
Key words: Acidithiobacillus ferrooxidans, acidophile, iron, pyrite, respiratory pathway,
supercomplex.
Abbreviation used: PMF, protonmotive force.
To whom correspondence should be addressed (email [email protected]).
1
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Authors Journal compilation Various models of its electron transport pathways have
been proposed and reviewed [2–6]. In the present paper, we
summarize recent work on the iron oxidation pathway. We
emphasize some critical points concerning (i) the organization
of this pathway [7], and (ii) the adaptation to the low pH of
periplasmic proteins involved in it.
Iron and acid: a challenge for living
organisms
Acidophile organisms, the most suited for iron
oxidation
Iron oxidizers have first to deal with the chemistry of
iron. Spontaneous chemical oxidation of iron can be rapid
at neutral pH under aerobic conditions, and oxidized iron
precipitates rapidly as ferric hydroxides. Consequently,
aerobic neutrophilic organisms able to oxidize iron (such as
Mariprofundus ferrooxydans) are rare and are usually present
under micro-oxic conditions to allow them to compete with
the spontaneous oxidation of Fe2 + . In acidic environments,
however, Fe2 + is rather stable and available even in the
presence of atmospheric oxygen. In these environments,
several micro-organisms using Fe2 + as an energy source have
been isolated (such as the bacterium A. ferrooxidans or the
archaeon Ferroplasma acidarmanus).
Biochem. Soc. Trans. (2012) 40, 1324–1329; doi:10.1042/BST20120141
Electron Transfer at the Microbe–Mineral Interface
High redox potential of the Fe2 + /Fe3 + couple:
a low energetic substrate
Owing to the high redox potential of the Fe2 + /Fe3 + couple
( + 0.77 V at pH 2), iron can be used as electron donor only
in presence of an electron acceptor of higher redox potential,
such as the O2 /H2 O couple ( + 1.12 V at pH 2). On the
basis of these values and the small amount of energy thus
available from the oxidative reaction of Fe2 + , Ingledew [1]
commented that “growth on Fe2 + represents one of the
narrowest thermodynamic limits for which growth is known
to occur” and he proposed that 22.4 molecules of Fe2 + are
required for the fixation of one molecule of CO2 .
The electron acceptor for iron is not only the O2 /H2 O
couple, but also Photosystem I ( + 0.45 V) and the
NO3 − /NO2 − couple ( + 0.43 V). They can be used under
anoxic and neutrophilic conditions because the redox
potential of iron decreases to approximately 0.385 V [4,8].
Rhodobacter capsulatus (a phototroph) and Dechloromonas
agitata (a nitrate reducer) are examples of known neutrophilic
iron oxidizers. Even though the study of these organisms is
in its infancy, they are of great interest, as they could help to
decipher the evolution of iron oxidation. It was proposed that
anoxygenic nitrate-dependent Fe2 + oxidation might have
evolved in the primordial deep-sea water [9].
How to survive in acidic environments
Extremely acidic environments are also very challenging for
life, to the point that acidophilic organisms have maintained
their cytoplasm at neutral pH to prevent acid protein
destabilization. Several strategies have been developed by
acidophiles to maintain an internal pH of the cell close to
neutrality [10] creating a natural PMF (protonmotive force)
across the membrane, which is used, for example, by ATP
synthase to produce ATP. Protons that have entered the cell
have to be exported. Among other processes, active proton
pumping seems to be important (four Na + /H + antiporters
and two proton P-type ATPases have been predicted) [10]. To
inhibit proton influx, the generation of a reverse membrane
potential (ψ) has been proposed to create a chemiosmotic
barrier [11].
The periplasmic compartment of Gram-negative organisms, however, is close to pH 3, and periplasmic proteins had
to adapt to function under such conditions. In the following
sections, we first describe A. ferrooxidans, followed by
characterization of its periplasmic iron-oxidation pathway,
thoroughly described in recent years, illustrating how the
pathway, as well as the periplasmic proteins involved in it,
function under such extreme conditions (iron and acid).
A. ferrooxidans: main characteristics
A. ferrooxidans, for which the genome has been sequenced [2],
is a Gram-negative rod-shaped bacterium that is commonly
found in deep caves or acid mine drainage [12,13]. Long
considered to be a member of the Gammaproteobacteria,
Williams et al. [14] proposed that A. ferrooxidans arose
Figure 1 Pyrite oxidation by micro-organisms
In water, pyrite (FeS2 ) is spontaneously oxidized to thiosulfate by ferric
iron (Fe3 + ), which in turn is reduced to give ferrous iron (Fe2 + ). This first
step is abiotic. The role of micro-organisms is essentially the regeneration
of the oxidant, Fe3 + . Using oxygen, bacteria can reoxidize Fe2 + again
to Fe3 + . Thiosulfate can also be oxidized by bacteria to give sulfate.
before the split between Gammaproteobacteria and Betaproteobacteria. It is strictly acidophilic and grows at an optimal
pH of 1.5–2.5. It is an obligate chemolithoautotroph that
uses for growth the energy produced by the oxidation of
reduced sulfur compounds and/or ferrous iron, using O2 as
oxidant, and it fixes atmospheric CO2 as a carbon source.
In its natural habitats, it derives Fe2 + from the insoluble
pyrite (Figure 1). This capacity renders A. ferrooxidans the
subject of considerable interest because of its use in industrial
bioleaching to facilitate the extraction of precious metals such
as copper and uranium from low-grade ores. Consequently,
the understanding of A. ferrooxidans metabolism not only
has a fundamental importance, but also has an impact on
biotechnological processes.
Iron-oxidation pathway: an
unconventional respiratory pathway in A.
ferrooxidans
Organization and function of the
electron-transport pathways
The iron-respiratory chain of A. ferrooxidans needed some
unusual characteristics owing to the non-conventional
properties enumerated above. For several years, scientists
have used distinct approaches, such as biochemistry,
molecular genetics, bioenergetics, bioinformatics, proteomics
and functional genomics, to understand how A. ferrooxidans
bypasses all of the locks described above. They were able
(i) to identify, characterize and test the functionality of the
proteins involved in the respiratory chain that couples the
oxidation of iron to the reduction of oxygen, as well as (ii)
to understand how reducing power is produced. It has been
shown that electrons from Fe2 + can either be transported
along a ‘downhill’ or a ‘uphill’ (or reverse) electron
pathway [15–17]. The majority of the electrons (estimated
at 90%) are transported through the downhill pathway
(thermodynamically favourable) to allow ATP synthesis. The
remaining 10% of the electrons are transported through
the uphill pathway (thermodynamically unfavourable in the
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Biochemical Society Transactions (2012) Volume 40, part 6
Figure 2 Metalloproteins and operons involved in ferrous iron oxidation in A. ferrooxidans
(A) The transcriptional unit called the rus operon [19,21,30] encodes proteins involved in the downhill pathway (light grey).
(B) The petI operon [20,30] encodes proteins involved in the uphill pathway (dark grey). Transcriptional start sites are
represented by bent arrows. acoP [38] encodes a chaperone-like protein. sdrA1 encodes a dehydrogenase (NDH-1). hyp1 is
a protein of unknown function. (C) Physicochemical properties of metalloproteins involved in both pathways are represented
by the same background shading. n.d., not determined.
standard state; the redox potential of the NAD + /NADH
couple is approximately + 0.32 V), to allow the production
of reducing power (NAD) for anabolic activities such as CO2
and N2 fixation. The energy to push electrons against this
thermodynamically unfavourable gradient is postulated to
come from the natural PMF.
Uphill and downhill pathways have been proposed to be
connected and to be regulated to balance ATP production
with the reconstitution of reducing power. The cellular
ATP/ADP ratio would regulate this balance [16]. Potential
regulators induced by Fe2 + have been identified in the
genome sequence (CtaR and RegAB). These regulators
could adjust the expression of proteins encoding the two
electron pathways [5]. Development of ‘-omics’ studies [3,18]
have demonstrated that two operons are critical for iron
oxidation: the petI and rus operons [19–21] (Figure 2).
Both encode metalloproteins that had been proposed to
belong to A. ferrooxidans electron-transport chains on the
basis of bioinformatics, protein subcellular localization,
spectroscopic properties or redox potentials characterization.
The spatial organization of the proteins involved in the
downhill pathway has been determined [7] (Figure 3).
A supramolecular organization of the respiratory chain
C The
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Authors Journal compilation involving various metalloproteins that spans the outer and
inner membranes has also been demonstrated [7]. After
purification under mild conditions, this supercomplex is
functional, as it has iron oxidase and oxygen reductase
activity. Proteins present in this complex have been identified
and are mainly encoded by the rus operon. Most of them
have been characterized individually, and some functional
interactions have been demonstrated. First, the primary
electron acceptor, the cytochrome Cyc2, is an outermembrane monohaem c-type cytochrome able to catalyse
iron oxidation [7,22]. Its high redox potential, unusual for a
c-type cytochrome, matches the high redox potential of the
entire pathway (Figure 2). Electrons are then transferred to
the periplasmic rusticyanin, a blue cupredoxin [23], and to the
dihaem cytochrome of the c4 -type (Cyc1) [24,25] (Figures 2
and 3). It has been demonstrated that the direct interaction
between these two proteins decreases the rusticyanin redox
potential by more than 100 mV, facilitating electron transfer
[26,27]. Next, Cyc1 transfers electrons to the terminal
electron acceptor, the cytochrome c oxidase [28] via an
essential tyrosine residue [27].
Rusticyanin and cytochrome c can individually account
for approximately 5–10% of the total cell protein. Owing to
Electron Transfer at the Microbe–Mineral Interface
Figure 3 Model of the iron-oxidation pathway in A. ferrooxidans
Fe2 + is oxidized by the outer membrane cytochrome c (Cyc2) outside the cells. Most of the electrons followed a downhill
pathway through several metalloproteins [rusticyanin (RcY), c4 -type cytochrome (Cyc1)] to reach the final electron acceptor,
the cytochrome c oxidase. AcoP, a copper protein, could stabilize the complex and protect the cytochrome c oxidase copper
centre from the acidic environment. This pathway allows the generation of ATP. Some of the electrons transit through an
uphill pathway to regenerate the reducing power. A c4 -type cytochrome (Cyc42) will interact with the rusticyanin (the
branching point of the two pathways) and transfer the electrons to a bc1 complex (working in reverse) [16] and reach finally
the complex I via the quinone pool (Q) to reduce NAD. Black circles represent the copper centre, crosses represent the haem
centre, diamond shapes represent the iron–sulfur cluster.
the low-energy substrate, they might constitute an important
electron reservoir in A. ferrooxidans [29].
In the purified supercomplex, a substoichiometric amount
of the bc1 complex (involved in the uphill pathway) has been
identified, providing some evidence for a possible physical
association of proteins involved in the downhill and uphill
pathways. The genes encoding the bc1 complex, as well as a
cytochrome of the c4 -type (Cyc42), are encoded by the petI
operon (Figure 2). It has been proposed that the branching
point between the downhill pathway and the uphill pathway
is at the level of the rusticyanin [7,30] (Figure 3).
After purification of the supercomplex, Omp40 has also
been detected (Figure 3). A role for this protein in the
interaction between the bacterium and the substrate has been
proposed [31]. However, the existence of excreted electron
carriers, as found in neutrophilic iron-reducing organisms,
cannot be ruled out and merits further attention. What is
known is that the primary attachment of A. ferrooxidans to
pyrite is mediated by exopolymer complexed with iron in
an electrostatic interaction with the negatively charged pyrite
surface [29,32].
This vertical spatial organization for a respiratory chain
had never been shown before and confirms the fact that
new concepts can be discovered by working on different
model organisms with different constraints. Different
hypotheses to explain such complex formation have been
advanced: it could help to overcome the low energy of the
substrate (optimization of the electron transfer) and/or to
prevent intracellular accumulation of a substrate prone
to precipitation (extracellular oxidation of the substrate)
and/or to protect against the acidic periplasm (a stabilization
of the system).
How periplasmic proteins adapt to low pH
In neutrophilic organisms such as enterobacteria, small
changes in the environmental pH have a strong impact on
the periplasmic proteins, as the outer membrane is permeable
to protons. A chaperone protein, HdeA, from Escherichia
coli prevents the aggregation of periplasmic proteins upon
acid stress [33]. The existence of such protection illustrates
the vulnerability of periplasmic proteins to face a pH change.
Periplasmic proteins from acidophile organisms had to adapt
to this ‘permanent-stress’ condition. Proteomic analysis of
131 periplasmic proteins from A. ferrooxidans have shown
that 70% are basic with a pI value of >7 [18], in contrast
with neutrophiles for which the pI of proteins is more evenly
distributed (40% are basic with a pI value of >7 in E. coli).
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Biochemical Society Transactions (2012) Volume 40, part 6
This result illustrates a general adaptation of the periplasmic
proteome of A. ferrooxidans.
The periplasmic metalloproteins described above have
common characteristics related to the unconventional
acid/iron pathway: a high redox potential (above 0.3 V), a
basic isoelectric focusing point and high stability to pH
variation. However, different strategies seem to have evolved
to maintain protein activity as well as stability at low pH,
especially for metalloproteins for which metal binding can
be affected by pH. As for hyperthermophilic proteins, no
general rules can be established, as the intrinsic stability can
be enhanced by local structural changes. The structures of
rusticyanin and of Cyc1 of A. ferrooxidans have been resolved
[34–36] and compared with their neutrophilic counterparts to
understand their high redox potentials and their pronounced
acid stability. Aspartate and glutamate residues reported for
c4 -type cytochromes from neutrophilic species are absent
in A. ferrooxidans proteins as they are protonated at pH 2,
preventing the formation of salt bridges involved in structural
stabilization in neutrophiles. An extensive internal hydrogenand hydrophobic bonding network surrounding the haems
has been proposed to be the stabilizing factor that could
explain its acid stability [24,35].
For the rusticyanin, intrinsic structural changes in the
immediate vicinity of the copper may explain its acid stability
[34,36]. Most type I copper proteins are unstable under acidic
conditions because of the protonation of one or both of the
histidine ligands making copper fairly labile. An explanation
for the acid stability of the copper site of the rusticyanin is
that its histidine ligands are more constrained due to the close
proximity of a number of hydrophobic groups (isoleucine
and phenylalanine). A high density of hydrophobic groups,
as well as the presence of aromatic and proline rings and
reduction in the number of pH-labile charge residues in the
immediate vicinity of the copper site, would explain its acid
stability.
Another metalloprotein of the iron-respiratory chain is
exposed to the low pH: the cytochrome c oxidase, a foursubunit complex (CoxA, CoxB, CoxC and CoxD) [37].
CoxB receives the electrons from the cytochrome Cyc1
and transfers them via its dinuclear copper centre (CuA ) to
the catalytic subunit CoxA, containing two haem centres
and a CuB centre where the reduction of water occurs. In
contrast with CoxA, CoxB is exposed to the acidic periplasm,
raising the question of the stability of its copper centre. On
the basis of structural modelling of the CoxB subunit, no
modification in the surroundings of CuA could be observed,
in contrast with the rusticyanin and the cytochrome Cyc1.
However, a protein of unknown function (AcoP) was found
in tight interaction with the cytochrome c oxidase [7]. An
alternative strategy to protect the metal centre from acid
stress via the presence of a supplementary protein (AcoP,
described as ‘chaperone-like’) seems thus to have evolved
for the cytochrome c oxidase [38]. Indeed, experimental data
show that AcoP maintains a stable and active conformation
of CoxB and consequently an optimal cytochrome c oxidase
activity in extreme acidic physiological conditions.
C The
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Authors Journal compilation Even though the molecular basis of acidophilic adaptation
remains obscure, mutative changes of amino acid sequences
as well as extrinsic factors may be part of the extremophilic
adaptation.
Conclusions
The studies of the iron oxidation pathway in A. ferrooxidans
provide new perceptions of how life could adapt to an
extremely acidic environment, as well as to the use of a lowenergy substrate with poor solubility. Information emerging
from other acidophiles such as Leptospirillum ferrooxidans,
Metallosphaera sedula and Sulfolobus metallicus show some
common features that are likely to be related to these
strong constraints: (i) all seem to accomplish the preliminary
oxidation of iron via an outer membrane cytochrome c, (ii)
the final electron acceptor is in most cases the cytochrome c
oxidase, as only the H2 O/O2 couple has a thermodynamic
potential superior to iron potential in acidic environment,
and (iii) they have the capacity to push electrons uphill to
reduce NAD via a bc complex working in reverse. Recent
advances on sequence information from several genomes and
metagenomes of acidophiles should help us to understand
the diversity as well as the common features of the pathway
involved in iron oxidation.
Funding
This work was supported by research grants from the Centre National
de la Recherche Scientifique (CNRS), Région Provence–Alpes–Côte
d’Azur (Région PACA) and the Agence Nationale de la Recherche
(ANR). M.R. has a fellowship of the French Ministry of Research
(Ministère de l’Enseignement Supérieur et de la Recherche).
References
1 Ingledew, W.J. (1982) Thiobacillus ferrooxidans: the bioenergetics of an
acidophilic chemolithotroph. Biochim. Biophys. Acta 683, 89–117
2 Valdes, J., Pedroso, I., Quatrini, R., Dodson, R.J., Tettelin, H., Blake, 2nd,
R., Eisen, J.A. and Holmes, D.S. (2008) Acidithiobacillus ferrooxidans
metabolism: from genome sequence to industrial applications. BMC
Genomics 9, 597
3 Bonnefoy, V. (2010) Bioinformatics and genomics of iron- and
sulfur-oxidizing acidophiles. In Geomicrobiology: Molecular and
Environmental Perspectives (Barton, L.L., Mandl, M. and Loy, A., eds),
pp. 169–192, Springer, Berlin
4 Bird, L.J., Bonnefoy, V. and Newman, D.K. (2011) Bioenergetic
challenges of microbial iron metabolisms. Trends Microbiol. 19, 330–340
5 Quatrini, R., Appia-Ayme, C., Denis, Y., Jedlicki, E., Holmes, D.S. and
Bonnefoy, V. (2009) Extending the models for iron and sulfur oxidation
in the extreme acidophile Acidithiobacillus ferrooxidans. BMC Genomics
10, 394
6 Bonnefoy, V. and Holmes, D.S. (2012) Genomic insights into microbial
iron oxidation and iron uptake strategies in extremely acidic
environments. Environ. Microbiol. 14, 1597–1611
7 Castelle, C., Guiral, M., Malarte, G., Ledgham, F., Leroy, G., Brugna, M.
and Giudici-Orticoni, M.T. (2008) A new iron-oxidizing/O2 -reducing
supercomplex spanning both inner and outer membranes, isolated from
the extreme acidophile Acidithiobacillus ferrooxidans. J. Biol. Chem. 283,
25803–25811
Electron Transfer at the Microbe–Mineral Interface
8 Hedrich, S., Schlomann, M. and Johnson, D.B. (2011) The iron-oxidizing
proteobacteria. Microbiology 157, 1551–1564
9 Emerson, D., Fleming, E.J. and McBeth, J.M. (2010) Iron-oxidizing
bacteria: an environmental and genomic perspective. Annu. Rev.
Microbiol. 64, 561–583
10 Baker-Austin, C. and Dopson, M. (2007) Life in acid: pH homeostasis in
acidophiles. Trends Microbiol. 15, 165–171
11 Matin, A. (1999) pH homeostasis in acidophiles. Novartis Found. Symp.
221, 152–163
12 Colmer, A.R., Temple, K.L. and Hinkle, M.E. (1950) An iron-oxidizing
bacterium from the acid drainage of some bituminous coal mines.
J. Bacteriol. 59, 317–328
13 Qiu, G.Z., Wan, M.X., Qian, L., Huang, Z.Y., Liu, K., Liu, X.D., Shi, W.Y. and
Yang, Y. (2008) Archaeal diversity in acid mine drainage from
Dabaoshan Mine, China. J. Basic Microbiol. 48, 401–409
14 Williams, K.P., Gillespie, J.J., Sobral, B.W., Nordberg, E.K., Snyder, E.E.,
Shallom, J.M. and Dickerman, A.W. (2010) Phylogeny of
Gammaproteobacteria. J. Bacteriol. 192, 2305–2314
15 Elbehti, A., Nitschke, W., Tron, P., Michel, C. and Lemesle-Meunier, D.
(1999) Redox components of cytochrome bc-type enzymes in
acidophilic prokaryotes. I. Characterization of the cytochrome bc1 -type
complex of the acidophilic ferrous ion-oxidizing bacterium Thiobacillus
ferrooxidans. J. Biol. Chem. 274, 16760–16765
16 Elbehti, A., Brasseur, G. and Lemesle-Meunier, D. (2000) First evidence
for existence of an uphill electron transfer through the bc1 and NADH-Q
oxidoreductase complexes of the acidophilic obligate chemolithotrophic
ferrous ion-oxidizing bacterium Thiobacillus ferrooxidans. J. Bacteriol.
182, 3602–3606
17 Brasseur, G., Levican, G., Bonnefoy, V., Holmes, D., Jedlicki, E. and
Lemesle-Meunier, D. (2004) Apparent redundancy of electron transfer
pathways via bc1 complexes and terminal oxidases in the extremophilic
chemolithoautotrophic Acidithiobacillus ferrooxidans. Biochim. Biophys.
Acta 1656, 114–126
18 Chi, A., Valenzuela, L., Beard, S., Mackey, A.J., Shabanowitz, J., Hunt, D.F.
and Jerez, C.A. (2007) Periplasmic proteins of the extremophile
Acidithiobacillus ferrooxidans: a high throughput proteomics analysis.
Mol. Cell. Proteomics 6, 2239–2251
19 Appia-Ayme, C., Guiliani, N., Ratouchniak, J. and Bonnefoy, V. (1999)
Characterization of an operon encoding two c-type cytochromes, an
aa3 -type cytochrome oxidase, and rusticyanin in Thiobacillus
ferrooxidans ATCC 33020. Appl. Environ. Microbiol. 65, 4781–4787
20 Levican, G., Bruscella, P., Guacunano, M., Inostroza, C., Bonnefoy, V.,
Holmes, D.S. and Jedlicki, E. (2002) Characterization of the petI and res
operons of Acidithiobacillus ferrooxidans. J. Bacteriol. 184, 1498–1501
21 Yarzabal, A., Appia-Ayme, C., Ratouchniak, J. and Bonnefoy, V. (2004)
Regulation of the expression of the Acidithiobacillus ferrooxidans rus
operon encoding two cytochromes c, a cytochrome oxidase and
rusticyanin. Microbiology 150, 2113–2123
22 Yarzabal, A., Brasseur, G., Ratouchniak, J., Lund, K., Lemesle-Meunier, D.,
DeMoss, J.A. and Bonnefoy, V. (2002) The high-molecular-weight
cytochrome c Cyc2 of Acidithiobacillus ferrooxidans is an outer
membrane protein. J. Bacteriol. 184, 313–317
23 Cox, J.C. and Boxer, D.H. (1978) The purification and some properties of
rusticyanin, a blue copper protein involved in iron(II) oxidation from
Thiobacillus ferro-oxidans. Biochem. J. 174, 497–502
24 Cavazza, C., Giudici-Orticoni, M.T., Nitschke, W., Appia, C., Bonnefoy, V.
and Bruschi, M. (1996) Characterisation of a soluble cytochrome c4
isolated from Thiobacillus ferrooxidans. Eur. J. Biochem. 242, 308–314
25 Giudici-Orticoni, M.T., Leroy, G., Nitschke, W. and Bruschi, M. (2000)
Characterization of a new dihemic c4 -type cytochrome isolated from
Thiobacillus ferrooxidans. Biochemistry 39, 7205–7211
26 Giudici-Orticoni, M.T., Guerlesquin, F., Bruschi, M. and Nitschke, W.
(1999) Interaction-induced redox switch in the electron transfer complex
rusticyanin–cytochrome c4 . J. Biol. Chem. 274, 30365–30369
27 Malarte, G., Leroy, G., Lojou, E., Abergel, C., Bruschi, M. and
Giudici-Orticoni, M.T. (2005) Insight into molecular stability and
physiological properties of the diheme cytochrome CYC41 from the
acidophilic bacterium Acidithiobacillus ferrooxidans. Biochemistry 44,
6471–6481
28 Kai, M., Yano, T., Fukumori, Y. and Yamanaka, T. (1989) Cytochrome
oxidase of an acidophilic iron-oxidizing bacterium, Thiobacillus
ferrooxidans, functions at pH 3.5. Biochem. Biophys. Res. Commun. 160,
839–843
29 Rohwerder, T., Gehrke, T., Kinzler, K. and Sand, W. (2003) Bioleaching
review part A: progress in bioleaching: fundamentals and mechanisms
of bacterial metal sulfide oxidation. Appl. Microbiol. Biotechnol. 63,
239–248
30 Bruscella, P., Appia-Ayme, C., Levican, G., Ratouchniak, J., Jedlicki, E.,
Holmes, D.S. and Bonnefoy, V. (2007) Differential expression of two bc1
complexes in the strict acidophilic chemolithoautotrophic bacterium
Acidithiobacillus ferrooxidans suggests a model for their respective roles
in iron or sulfur oxidation. Microbiology 153, 102–110
31 Arredondo, R., Garcia, A. and Jerez, C.A. (1994) Partial removal of
lipopolysaccharide from Thiobacillus ferrooxidans affects its adhesion to
solids. Appl. Environ. Microbiol. 60, 2846–2851
32 Gehrke, T., Telegdi, J., Thierry, D. and Sand, W. (1998) Importance of
extracellular polymeric substances from Thiobacillus ferrooxidans for
bioleaching. Appl. Environ. Microbiol. 64, 2743–2747
33 Tapley, T.L., Korner, J.L., Barge, M.T., Hupfeld, J., Schauerte, J.A., Gafni, A.,
Jakob, U. and Bardwell, J.C. (2009) Structural plasticity of an
acid-activated chaperone allows promiscuous substrate binding. Proc.
Natl. Acad. Sci. U.S.A. 106, 5557–5562
34 Botuyan, M.V., Toy-Palmer, A., Chung, J., Blake, R.C., 2nd, Beroza, P.,
Case, D.A. and Dyson, H.J. (1996) NMR solution structure of Cu(I)
rusticyanin from Thiobacillus ferrooxidans: structural basis for the
extreme acid stability and redox potential. J. Mol. Biol. 263,
752–767
35 Abergel, C., Nitschke, W., Malarte, G., Bruschi, M., Claverie, J.M. and
Giudici-Orticoni, M.T. (2003) The structure of Acidithiobacillus
ferrooxidans c4 -cytochrome: a model for complex-induced electron
transfer tuning. Structure 11, 547–555
36 Walter, R.L., Ealick, S.E., Friedman, A.M., Blake, 2nd, R.C., Proctor, P. and
Shoham, M. (1996) Multiple wavelength anomalous diffraction (MAD)
crystal structure of rusticyanin: a highly oxidizing cupredoxin with
extreme acid stability. J. Mol. Biol. 263, 730–751
37 Kai, M., Yano, T., Tamegai, H., Fukumori, Y. and Yamanaka, T. (1992)
Thiobacillus ferrooxidans cytochrome c oxidase: purification, and
molecular and enzymatic features. J. Biochem. 112, 816–821
38 Castelle, C., Ilbert, M., Infossi, P., Leroy, G. and Giudici-Orticoni, M.T.
(2010) An unconventional copper protein required for cytochrome c
oxidase respiratory function under extreme acidic conditions. J. Biol.
Chem. 285, 21519–21525
39 Ingledew, W.J. and Cobley, J.G. (1980) A potentiometric and kinetic study
on the respiratory chain of ferrous-iron-grown Thiobacillus ferrooxidans.
Biochim. Biophys. Acta 590, 141–158
40 Ronk, M., Shively, J.E., Shute, E.A. and Blake, 2nd, R.C. (1991) Amino acid
sequence of the blue copper protein rusticyanin from Thiobacillus
ferrooxidans. Biochemistry 30, 9435–9442
41 Brugna, M., Nitschke, W., Asso, M., Guigliarelli, B., Lemesle-Meunier, D.
and Schmidt, C. (1999) Redox components of cytochrome bc-type
enzymes in acidophilic prokaryotes. II. The Rieske protein of
phylogenetically distant acidophilic organisms. J. Biol. Chem. 274,
16766–16772
Received 19 June 2012
doi:10.1042/BST20120141
C The
C 2012 Biochemical Society
Authors Journal compilation 1329