Differential expression of two bc 1 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

University of Santiago, Chile, CiudadSantiago, Santiago Metropolitan, Chile
Microbiology (Impact Factor: 2.56). 02/2007; 153(Pt 1):102-10. DOI: 10.1099/mic.0.2006/000067-0
Source: PubMed


Three strains of the strict acidophilic chemolithoautotrophic Acidithiobacillus ferrooxidans, including the type strain ATCC 23270, contain a petIIABC gene cluster that encodes the three proteins, cytochrome c1, cytochrome b and a Rieske protein, that constitute a bc1 electron-transfer complex. RT-PCR and Northern blotting show that the petIIABC cluster is co-transcribed with cycA, encoding a cytochrome c belonging to the c4 family, sdrA, encoding a putative short-chain dehydrogenase, and hip, encoding a high potential iron-sulfur protein, suggesting that the six genes constitute an operon, termed the petII operon. Previous results indicated that A. ferrooxidans contains a second pet operon, termed the petI operon, which contains a gene cluster that is similarly organized except that it lacks hip. Real-time PCR and Northern blot experiments demonstrate that petI is transcribed mainly in cells grown in medium containing iron, whereas petII is transcribed in cells grown in media containing sulfur or iron. Primer extension experiments revealed possible transcription initiation sites for the petI and petII operons. A model is presented in which petI is proposed to encode the bc1 complex, functioning in the uphill flow of electrons from iron to NAD(P), whereas petII is suggested to be involved in electron transfer from sulfur (or formate) to oxygen (or ferric iron). A. ferrooxidans is the only organism, to date, to exhibit two functional bc1 complexes.

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Available from: David S Holmes
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    • "In contrast to A. ferrooxidans ATCC 23270, which was reported to use an aa 3 -type cytochrome c oxidase as terminal oxi- dase[41,77,85], " Ferrovum " strain JA12 was predicted to reduce oxygen via a cbb 3 -type cytochrome c oxidase similar to the neutrophilic iron oxidisers Mariprofundus ferrooxydans PV-1[82]and S. lithotrophicus ES-1[75]and similar to the acidophiles " F. myxofaciens " P3G[28]and Leptospirillum ferriphilum ML-4[29]. Although only genes predicted to encode the subunits I and II of the cbb 3 -type cytochrome c oxidase were identified in the genome of " Ferrovum " strain JA12, one of the co-localised c-type cytochromes (FERRO_02610, FERRO_02510) could substitute the missing subunit III, which also represents a c-type cyto- chrome[86](S4C Fig).Furthermore, two alternative terminal oxidases were predicted that use quinol as electron donor instead of the soluble c-type cytochromes: the cytochrome bo 3 ubiquinol oxidase and the cytochrome bd complex. " Ferrovum " strain JA12 presumably generates reduction equivalents for biosyntheses similar to A. ferrooxidans transferring electrons from the c-type cytochrome in the periplasm via the bc 1 complex and the quinol pool to the NADH-quinone oxidoreductase complex[41,77,85]. "
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    ABSTRACT: Background: Members of the genus "Ferrovum" are ubiquitously distributed in acid mine drainage (AMD) waters which are characterised by their high metal and sulfate loads. So far isolation and microbiological characterisation have only been successful for the designated type strain "Ferrovum myxofaciens" P3G. Thus, knowledge about physiological characteristics and the phylogeny of the genus "Ferrovum" is extremely scarce. Objective: In order to access the wider genetic pool of the genus "Ferrovum" we sequenced the genome of a "Ferrovum"-containing mixed culture and successfully assembled the almost complete genome sequence of the novel "Ferrovum" strain JA12. Phylogeny and lifestyle: The genome-based phylogenetic analysis indicates that strain JA12 and the type strain represent two distinct "Ferrovum" species. "Ferrovum" strain JA12 is characterised by an unusually small genome in comparison to the type strain and other iron oxidising bacteria. The prediction of nutrient assimilation pathways suggests that "Ferrovum" strain JA12 maintains a chemolithoautotrophic lifestyle utilising carbon dioxide and bicarbonate, ammonium and urea, sulfate, phosphate and ferrous iron as carbon, nitrogen, sulfur, phosphorous and energy sources, respectively. Unique metabolic features: The potential utilisation of urea by "Ferrovum" strain JA12 is moreover remarkable since it may furthermore represent a strategy among extreme acidophiles to cope with the acidic environment. Unlike other acidophilic chemolithoautotrophs "Ferrovum" strain JA12 exhibits a complete tricarboxylic acid cycle, a metabolic feature shared with the closer related neutrophilic iron oxidisers among the Betaproteobacteria including Sideroxydans lithotrophicus and Thiobacillus denitrificans. Furthermore, the absence of characteristic redox proteins involved in iron oxidation in the well-studied acidophiles Acidithiobacillus ferrooxidans (rusticyanin) and Acidithiobacillus ferrivorans (iron oxidase) indicates the existence of a modified pathway in "Ferrovum" strain JA12. Therefore, the results of the present study extend our understanding of the genus "Ferrovum" and provide a comprehensive framework for future comparative genome and metagenome studies.
    Full-text · Article · Jan 2016 · PLoS ONE
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    • "These operons are differentially transcribed in response to growth conditions. Namely, bc 1 complex form II encoded by the pet II operon is preferably expressed in S 0 -cells (Bruscella et al. 2007). Part of the pet II operon is a short-chain dehydrogenase/ reductase family protein (SdrA2; spot No. 318, AFE_0377). "
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    ABSTRACT: Elemental sulfur oxidation by ferric iron in Acidithiobacillus ferrooxidans was investigated. The apparent Michaelis constant for ferric iron was 18.6 mM. An absence of anaerobic ferric iron reduction ability was observed in bacteria maintained on elemental sulfur for an extended period of time. Upon transition from ferrous iron to elemental sulfur medium, the cells exhibited similar kinetic characteristics of ferric iron reduction under anaerobic conditions to those of cells that were originally maintained on ferrous iron. Nevertheless, a total loss of anaerobic ferric iron reduction ability after the sixth passage in elemental sulfur medium was demonstrated. The first proteomic screening of total cell lysates of anaerobically incubated bacteria resulted in the detection of 1599 protein spots in the master two-dimensional electrophoresis gel. A set of 59 more abundant and 49 less abundant protein spots that changed their protein abundances in an anaerobiosis-dependent manner was identified and compared to iron- and sulfur-grown cells, respectively. Proteomic analysis detected a significant increase in abundance under anoxic conditions of electron transporters, such as rusticyanin and cytochrome c(552), involved in the ferrous iron oxidation pathway. Therefore we suggest the incorporation of rus-operon encoded proteins in the anaerobic respiration pathway. Two sulfur metabolism proteins were identified, pyridine nucleotide-disulfide oxidoreductase and sulfide-quinone reductase. The important transcription regulator, ferric uptake regulation protein, was anaerobically more abundant. The anaerobic expression of several proteins involved in cell envelope formation indicated a gradual adaptation to elemental sulfur oxidation.
    Full-text · Article · Nov 2011 · Antonie van Leeuwenhoek
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    • "It was suggested about a decade ago that the cellular ATP/ADP ratio regulates the balance of reducing equivalents from Fe(II), favouring either the activation of the aa3 cytochrome oxidase and thus promote the downhill pathway or, conversely, the repression of the aa3 cytochrome oxidase promoting the use of the uphill pathway (Elbehti et al., 2000). In addition to regulatory decisions regarding the flux of electrons uphill or downhill, At. ferrooxidans also regulates enzymes and electron carriers depending on whether its energetic substrate is Fe(II) or RISCs (Yarzabal et al., 2004; Bruscella et al., 2007; Amouric et al., 2009; Quatrini et al., 2009). "
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    ABSTRACT: This minireview presents recent advances in our understanding of iron oxidation and homeostasis in acidophilic Bacteria and Archaea. These processes influence the flux of metals and nutrients in pristine and man-made acidic environments such as acid mine drainage and industrial bioleaching operations. Acidophiles are also being studied to understand life in extreme conditions and their role in the generation of biomarkers used in the search for evidence of existing or past extra-terrestrial life. Iron oxidation in acidophiles is best understood in the model organism Acidithiobacillus ferrooxidans. However, recent functional genomic analysis of acidophiles is leading to a deeper appreciation of the diversity of acidophilic iron-oxidizing pathways. Although it is too early to paint a detailed picture of the role played by lateral gene transfer in the evolution of iron oxidation, emerging evidence tends to support the view that iron oxidation arose independently more than once in evolution. Acidic environments are generally rich in soluble iron and extreme acidophiles (e.g. the Leptospirillum genus) have considerably fewer iron uptake systems compared with neutrophiles. However, some acidophiles have been shown to grow as high as pH 6 and, in the case of the Acidithiobacillus genus, to have multiple iron uptake systems. This could be an adaption allowing them to respond to different iron concentrations via the use of a multiplicity of different siderophores. Both Leptospirillum spp. and Acidithiobacillus spp. are predicted to synthesize the acid stable citrate siderophore for Fe(III) uptake. In addition, both groups have predicted receptors for siderophores produced by other microorganisms, suggesting that competition for iron occurs influencing the ecophysiology of acidic environments. Little is known about the genetic regulation of iron oxidation and iron uptake in acidophiles, especially how the use of iron as an energy source is balanced with its need to take up iron for metabolism. It is anticipated that integrated and complex regulatory networks sensing different environmental signals, such as the energy source and/or the redox state of the cell as well as the oxygen availability, are involved.
    Full-text · Article · Nov 2011 · Environmental Microbiology
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