Extending the models for iron and sulfur oxidation in the extreme Acidophile Acidithiobacillus ferrooxidans

Center for Bioinformatics and Genome Biology, MIFAB, Fundación Ciencia para la Vida and Depto. de Ciencias Biologicas, Universidad Andres Bello, Santiago, Chile.
BMC Genomics (Impact Factor: 4.04). 09/2009; 10:394. DOI: 10.1186/1471-2164-10-394
Source: PubMed

ABSTRACT Acidithiobacillus ferrooxidans gains energy from the oxidation of ferrous iron and various reduced inorganic sulfur compounds at very acidic pH. Although an initial model for the electron pathways involved in iron oxidation has been developed, much less is known about the sulfur oxidation in this microorganism. In addition, what has been reported for both iron and sulfur oxidation has been derived from different A. ferrooxidans strains, some of which have not been phylogenetically characterized and some have been shown to be mixed cultures. It is necessary to provide models of iron and sulfur oxidation pathways within one strain of A. ferrooxidans in order to comprehend the full metabolic potential of the pangenome of the genus.
Bioinformatic-based metabolic reconstruction supported by microarray transcript profiling and quantitative RT-PCR analysis predicts the involvement of a number of novel genes involved in iron and sulfur oxidation in A. ferrooxidans ATCC23270. These include for iron oxidation: cup (copper oxidase-like), ctaABT (heme biogenesis and insertion), nuoI and nuoK (NADH complex subunits), sdrA1 (a NADH complex accessory protein) and atpB and atpE (ATP synthetase F0 subunits). The following new genes are predicted to be involved in reduced inorganic sulfur compounds oxidation: a gene cluster (rhd, tusA, dsrE, hdrC, hdrB, hdrA, orf2, hdrC, hdrB) encoding three sulfurtransferases and a heterodisulfide reductase complex, sat potentially encoding an ATP sulfurylase and sdrA2 (an accessory NADH complex subunit). Two different regulatory components are predicted to be involved in the regulation of alternate electron transfer pathways: 1) a gene cluster (ctaRUS) that contains a predicted iron responsive regulator of the Rrf2 family that is hypothesized to regulate cytochrome aa3 oxidase biogenesis and 2) a two component sensor-regulator of the RegB-RegA family that may respond to the redox state of the quinone pool.
Bioinformatic analysis coupled with gene transcript profiling extends our understanding of the iron and reduced inorganic sulfur compounds oxidation pathways in A. ferrooxidans and suggests mechanisms for their regulation. The models provide unified and coherent descriptions of these processes within the type strain, eliminating previous ambiguity caused by models built from analyses of multiple and divergent strains of this microorganism.

Download full-text


Available from: Violaine Bonnefoy, Aug 17, 2015
    • "(1)) [7] [8]. The intermediary sulfur compounds formed in the reaction, such as thiosulfate and elemental sulfur, can be further oxidized to sulfate [8] [9] [10]. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Inorganic sulfur compounds, such as tetrathionate, are often present in mining process and waste waters. The biodegradation of tetrathionate was studied under acidic conditions in aerobic batch cultivations and in anaerobic anodes of two-chamber flow-through microbial fuel cells (MFCs). All four cultures originating from biohydrometallurgical process waters from multimetal ore heap bioleaching oxidized tetrathionate aerobically at pH below 3 with sulfate as the main soluble metabolite. In addition, all cultures generated electricity from tetrathionate in MFCs at pH below 2.5 with ferric iron as the terminal cathodic electron acceptor. The maximum current and power densities during MFC operation and in the performance analysis were 79.6 mA m−2 and 13.9 mW m−2 and 433 mA m−2 and 17.6 mW m−2, respectively. However, the low coulombic efficiency (below 5%) indicates that most of the electrons were directed to other processes, such as aerobic oxidation of tetrathionate and unmeasured intermediates. The microbial community analysis revealed that the dominant species both in the anolyte and on the anode electrode surface of the MFCs were Acidithiobacillus spp. and Ferroplasma spp. This study provides a proof of concept that tetrathionate serves as electron donor for biological electricity production in the pH range of 1.2–2.5.
    Journal of Hazardous Materials 11/2014; 284. DOI:10.1016/j.jhazmat.2014.10.045 · 4.33 Impact Factor
  • Source
    • "Indeed, the B1A ecosystem was the sample with a high abundance of genes for rusticyanins, sulphocyanins and cbb 3 -type cytochrome c oxidases (B2-and 1.3-fold more abundant than in B1B and B2) and enzymes (e.g., TusD and DsrE) for the oxidation of sulphide (HS À ), which were B3-fold less abundant in B1B and absent in B2. Enzymes indicative of the putative presence of sulphur or reduced inorganic sulphur compounds metabolism such as sulphide:quinone reductases, often associated with acidophilic bacteria (Quatrini et al., 2009; Liljeqvist et al., 2011; Liljeqvist et al., 2013), were also encountered in all three metagenomes , although at very similarly low abundance level. Interestingly, whereas genes encoding nitrogenase MoFe proteins for nitrogen fixation were present at similar levels in B1A and B1B but absent in B2, those for nitrate reduction were most abundant in B2 and B1B (B2-fold more abundant than in B1A). "
    [Show abstract] [Hide abstract]
    ABSTRACT: Macroscopic growths at geographically separated acid mine drainages (AMDs) exhibit distinct populations. Yet, local heterogeneities are poorly understood. To gain novel mechanistic insights into this, we used OMICs tools to profile microbial populations coexisting in a single pyrite gallery AMD (pH ∼2) in three distinct compartments: two from a stratified streamer (uppermost oxic and lowermost anoxic sediment-attached strata) and one from a submerged anoxic non-stratified mat biofilm. The communities colonising pyrite and those in the mature formations appear to be populated by the greatest diversity of bacteria and archaea (including 'ARMAN' (archaeal Richmond Mine acidophilic nano-organisms)-related), as compared with the known AMD, with ∼44.9% unclassified sequences. We propose that the thick polymeric matrix may provide a safety shield against the prevailing extreme condition and also a massive carbon source, enabling non-typical acidophiles to develop more easily. Only 1 of 39 species were shared, suggesting a high metabolic heterogeneity in local microenvironments, defined by the O2 concentration, spatial location and biofilm architecture. The suboxic mats, compositionally most similar to each other, are more diverse and active for S, CO2, CH4, fatty acid and lipopolysaccharide metabolism. The oxic stratum of the streamer, displaying a higher diversity of the so-called 'ARMAN'-related Euryarchaeota, shows a higher expression level of proteins involved in signal transduction, cell growth and N, H2, Fe, aromatic amino acids, sphingolipid and peptidoglycan metabolism. Our study is the first to highlight profound taxonomic and functional shifts in single AMD formations, as well as new microbial species and the importance of H2 in acidic suboxic macroscopic growths.The ISME Journal advance online publication, 16 January 2014; doi:10.1038/ismej.2013.242.
    The ISME Journal 01/2014; 8(6). DOI:10.1038/ismej.2013.242 · 9.27 Impact Factor
  • Source
    • "Sulfur produced by SOB can be stored in sulfur globules, located inside and/or outside the bacterial cell (He et al., 2010); (Kleinjan et al., 2003). Although the biochemical fundamentals of sulfur oxidation are very complex, several models for the oxidation of RISCs have been developed (Friedrich et al., 2005; Quatrini et al., 2009; Valdés et al., 2008). According to these models, S 0 is activated firstly by reacting with reactive thiol groups (\SH) of outer membrane proteins, forming \S n H (n ≥ 2) complexes, and then transported into periplasmic space for further oxidation. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The differential expression of extracellular thiol groups by Acidithiobacillus ferrooxidans grown on substrates Fe(2+) and S(0) was investigated by using synchrotron radiation based scanning transmission X-ray microscopy (STXM) imaging and microbeam X-ray fluorescence (μ-XRF) mapping. The extracellular thiol groups (SH) were first alkylated by iodoacetic acid forming Protein-SCH2COOH and then the P-SCH2COOH was marked by calcium ions forming P-SCH2COOCa. The STXM imaging and μ-XRF mapping of SH were based on analysis of SCH2COO-bonded Ca(2+). The results indicated the thiol group content of A. ferrooxidans grown on S(0) is 3.88 times to that on Fe(2+). Combined with selectively labeling of SH by Ca(2+), the STXM imaging and μ-XRF mapping provided an in situ and rapid analysis of differential expression of extracellular thiol groups.
    Journal of microbiological methods 07/2013; 94(3). DOI:10.1016/j.mimet.2013.06.030 · 2.10 Impact Factor
Show more