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Genome wide identification of Acidithiobacillus ferrooxidans (ATCC 23270) transcription factors and comparative analysis of ArsR and MerR metal regulators

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Abstract

Acidithiobacillus ferrooxidans is a chemolithoautotrophic acidophilic bacterium that obtains its energy from the oxidation of ferrous iron, elemental sulfur, or reduced sulfur minerals. This capability makes it of great industrial importance due to its applications in biomining. During the industrial processes, A. ferrooxidans survives to stressing circumstances in its environment, such as an extremely acidic pH and high concentration of transition metals. In order to gain insight into the organization of A. ferrooxidans regulatory networks and to provide a framework for further studies in bacterial growth under extreme conditions, we applied a genome-wide annotation procedure to identify 87 A. ferrooxidans transcription factors. We classified them into 19 families that were conserved among diverse prokaryotic phyla. Our annotation procedure revealed that A. ferrooxidans genome contains several members of the ArsR and MerR families, which are involved in metal resistance and detoxification. Analysis of their sequences revealed known and potentially new mechanism to coordinate gene-expression in response to metal availability. A. ferrooxidans inhabit some of the most metal-rich environments known, thus transcription factors identified here seem to be good candidates for functional studies in order to determine their physiological roles and to place them into A. ferrooxidans transcriptional regulatory networks.

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Acknowledgments

This work was supported by Fondef D04I1257 (AM), Fondecyt 1090211 (VC), 1110427 (MG) and FONDAP-15090007(VC, AM and MG). CH was supported by a doctoral fellowship from Conicyt, a Dr. A. Stekel fellowship and a Postdoctoral grant Fondecyt 311019. The authors thank Marcel Spehr, Carito Vargas, Alvaro Graves and Nicolas Loira for their invaluable efforts on making to work the local GenDB installation. We also thank Burkhard Kinke and Alexander Goesmann at Bielefeld University; they were very helpful every time we reached them.

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Authors and Affiliations

  1. Laboratorio de Bioinformática y Expresión Génica, INTA, Universidad de Chile, El Libano 5524, Santiago, Chile

    Christian Hödar, Mauricio Latorre, Angélica Reyes-Jara, Mauricio González & Verónica Cambiazo

  2. Laboratorio de Bioinformática y Matemática del Genoma, Center for Mathematical Modeling, FCFM, Universidad de Chile, Santiago, Chile

    Pablo Moreno, Alex di Genova & Alejandro Maass

  3. Center for Genome Regulation, Universidad de Chile, Santiago, Chile

    Alejandro Maass & Mauricio González

Authors
  1. Christian Hödar
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  2. Pablo Moreno
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  3. Alex di Genova
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  4. Mauricio Latorre
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  5. Angélica Reyes-Jara
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  6. Alejandro Maass
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  7. Mauricio González
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  8. Verónica Cambiazo
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Corresponding author

Correspondence to Verónica Cambiazo.

Additional information

C. Hödar and P. Moreno contributed equally to this work.

Electronic supplementary material

Below is the link to the electronic supplementary material.

10534_2011_9484_MOESM1_ESM.pdf

Flowchart of transcription factor annotation procedure showing the different steps of the annotation procedure employed to obtain the repertoire of A. ferrooxidans TFs (PDF 124 kb)

10534_2011_9484_MOESM2_ESM.xls

The repertoire of candidate transcription factors. This file contains data of the 119 TFs obtained by our automatic annotation procedure. For each protein sequence (Gene Code column) we searched for several attributes in order to classify the protein as a transcription factor (see Methods). The last column contains the amino acid sequence used in blast and domain analyses (XLS 117 kb)

10534_2011_9484_MOESM3_ESM.pdf

Transcription factor families. After manual curation of data obtained by automatic annotation, 87 sequences were assigned to TFs families (PDF 525 kb)

10534_2011_9484_MOESM4_ESM.xls

Conservation of A. ferrooxidans TFs in prokaryotic genomes. Each column corresponds to an A. ferrooxidans TF and each row to a predicted proteome from 957 microorganisms classified into phyla. Numbers 1 or 0 indicate the presence or absence of orthologs of A. ferrooxidans TFs in each proteome after BBH procedure (XLS 629 kb)

10534_2011_9484_MOESM5_ESM.pdf

Multiple alignments of A. ferooxidans MerR transcriptional regulators. Sequences that had best BLASTp hits to predicted members of A. ferrooxidans MerR family were aligned using ClustalW. Identical residues are shaded in black and similar residues in grey. Black boxes represent the predicted HTH DNA-binding domain of A. ferrooxidans TFs. Secondary structure elements are represented above the sequences. Residues that represent potential amino acids involved in metal coordination are indicated in an orange box. Black asterisk, conserved Tyr residue within α2-helix; green asterisk, Ser76 (PDF 434 kb)

10534_2011_9484_MOESM6_ESM.pdf

Multiple alignments of AFE_2859 orthologs. Genes that were identified as orthologs of AFE_2859 were aligned using ClustalW. At the top of the image is shown the predicted secondary structure of AFE_2859, with α-helices in red and β-strands in blue. Black box represents the HTH DNA binding domain and orange box the MBD described for AFE_2859 protein. Aligned residues present in more than 60% of the sequences were shaded. Black and red asterisks indicate A. ferrooxidans ATCC 23270 and ATCC 53993, respectively (PDF 11907 kb)

10534_2011_9484_MOESM7_ESM.jpg

Phylogenetic reconstruction of AFE_2859 orthologs. The image shows the bootstrap consensus tree inferred from the alignment of AFE_2859 orthologs using Neighbor joining procedure. Three groups can be identified based on the number of cysteine residues present in the putative MBD of the orthologs. AFE_2859 (arrowhead) are more closely related to orthologs with three cysteine residues in the MBD. Putative ArsR regulators, AFE_2641 and AFE_2369 are more closely related to AFE_2859 orthologs with one or two cysteines in the MBD (insets) (JPG 652 kb)

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Hödar, C., Moreno, P., di Genova, A. et al. Genome wide identification of Acidithiobacillus ferrooxidans (ATCC 23270) transcription factors and comparative analysis of ArsR and MerR metal regulators. Biometals 25, 75–93 (2012). https://doi.org/10.1007/s10534-011-9484-8

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