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Comparative Genome Analysis of Acidithiobacillus Ferrooxidans, A Hydrometallurgy 94 (2008) 180–184 Contents lists available at ScienceDirect Hydrometallurgy journal homepage: www.elsevier.com/locate/hydromet Comparative genome analysis of Acidithiobacillus ferrooxidans, A. thiooxidans and A. caldus: Insights into their metabolism and ecophysiology Jorge Valdés 1, Inti Pedroso, Raquel Quatrini, David S. Holmes ⁎ Center for Bioinformatics and Genome Biology, Life Science Foundation, MIFAB and Andrés Bello University, Santiago, Chile ARTICLE INFO ABSTRACT Available online 2 July 2008 Draft genome sequences of Acidthiobacillus thiooxidans and A. caldus have been annotated and compared to the previously annotated genome of A. ferrooxidans. This has allowed the prediction of metabolic and Keywords: regulatory models for each species and has provided a unique opportunity to undertake comparative Acidithiobacillus genomic studies of this group of related bioleaching bacteria. In this paper, the presence or absence of Bioinformatics predicted genes for eleven metabolic processes, electron transfer pathways and other phenotypic Comparative genomics fi Metabolic integration characteristics are reported for the three acidithiobacilli: CO2 xation, the TCA cycle, sulfur oxidation, sulfur reduction, iron oxidation, iron assimilation, quorum sensing via the acyl homoserine lactone mechanism, hydrogen oxidation, flagella formation, Che signaling (chemotaxis) and nitrogen fixation. Predicted transcriptional and metabolic interplay between pathways pinpoints possible coordinated responses to environmental signals such as energy source, oxygen and nutrient limitations. The predicted pathway for nitrogen fixation in A. ferrooxidans will be described as an example of such an integrated response. Several responses appear to be especially characteristic of autotrophic microorganisms and may have direct implications for metabolic processes of critical relevance to the understanding of how these microorganisms survive and proliferate in extreme environments, including industrial bioleaching operations. © 2008 Elsevier B.V. All rights reserved. 1. Introduction biologist to focus on key issues suggested by the bioinformatic predictions, thus saving considerable time and resources (Quatrini Acidophilic prokaryotes involved in bioleaching process have been et al., 2007a). the subject of active research from the viewpoints of microbiology, The bioinformatic analysis of the genome sequence of the γ- biophysics, biochemistry and genetics. With the advent of genome proteobacterium A. ferrooxidans has led to the generation of several sequencing and the continuously decreasing costs and time needed to metabolic and regulatory models some of which have been experimen- sequence new genomes, novel opportunities and challenges have tally validated in part, such as sulfur uptake and assimilation (Valdés et arisen for developing integrative metabolic and regulatory models al., 2003), iron uptake and assimilation (Quatrini et al., 2005; Osorio et that couple traditional experimental data sources with information al., 2008-this issue), Fur regulatory gene circuits (Quatrini et al., 2007b), obtained from computationally-derived comparative genome infor- quorum sensing (Rivas et al., 2005; Farah et al., 2005; Rivas et al., 2007), mation. Advanced bioinformatic tools, developed in the last few years, biofilm formation (Barreto et al., 2005), small regulatory RNA gene have allowed relatively rapid ways to generate initial models of prediction (Shmaryahu and Holmes, unpublished results) and carbon metabolic and regulatory features potentially encoded within a metabolism (Barreto et al., 2003; Appia-Ayme et al., 2006). An analysis of genome and to pinpoint key features that can be highlighted for the genome of A. ferrooxidans has also supported and extended earlier subsequent experimental validation. models of iron and sulfur oxidation in this microorganism (Quatrini Chemolithoautotrophic microorganisms in general, and the extreme et al., 2006; Valdés et al., unpublished results). acidophilic ones in particular, are difficult to handle experimentally and Large-scale comparisons of genomes address basic questions, such can be recalcitrant to genetic manipulation. These hurdles can be as the number of functional genes, identification of species-specific compensated for, in part, by the enormous amount of information that genes, distribution of genes among functional families, gene density, can be extracted by careful genome analysis, allowing the experimental preservation of gene order, mechanisms of genome reshuffling, the rate of sequence divergence, etc. (Hardison, 2003). In general, the choice of species that mark evolutionary distances for comparative genomics depends on the aim of the analysis. ⁎ Corresponding author. Tel.: +56 2 239 8969; fax: +56 2 237 2259. In the present study, the genomes of three closely related gram- E-mail addresses: [email protected] (J. Valdés), [email protected] (D.S. Holmes). negative, chemoautotrophic bioleaching microorganisms, A. ferroox- 1 Fax: +56 2 237 2259. idans, A. thiooxidans and A. caldus, were compared, anticipating that 0304-386X/$ – see front matter © 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.hydromet.2008.05.039 J. Valdés et al. / Hydrometallurgy 94 (2008) 180–184 181 such a study would help to consolidate the prediction and identifica- tion of genes and conserved gene clusters involved in various predicted metabolic models and that the identification of conserved intergenic regions between the three species would facilitate the prediction of small regulatory RNA genes and transcriptional regulatory regions. It was also hoped that it would allow the identification of genes involved in iron oxidation specificto A. ferrooxidans and might, in the long term, suggest the genetic basis of other potential differences between the three species such as the ability of A. caldus to grow at 45–55 °C compared to the mesophilic temperatures of the other two species (Hallberg and Lindstrom, 1994). Most importantly, it was hoped that a comparative genomics study could identify novel genetic differences between the three species, suggest models of the evolution of their respective genomes and allows the prediction of mutual interactions between the three acidithiobacilli that might occur in their natural environment and in biomining operations (ecophysiology). 2. Methods The complete genome sequence of Acidithiobacillus ferrooxidans ATCC 23270 was obtained from the Institute for Genomic Research database (TIGR, Valdés et al., unpublished results). Draft genome sequences of Fig. 1. Schematic representation of the bioinformatics pipeline used in this study. A. thiooxidans ATCC 19377 and A. caldus ATCC 51756 were obtained from Abbreviations: ACT, Artemis comparison tool; NR-DB, Non-redundant database; MG- the Center for Bioinformatics and Genome Biology (CBGB), Santiago, DB, microbial genomes database. Additional information can be found in the Methods. Chile. Candidate protein coding genes were identified in genome sequences using Glimmer (Salzberg et al., 1998), Critica (Badger and 3.2. Whole genome comparison Olsen,1999)andBlastX(Altschul et al.,1997). The 5′ and 3′regions of each ORF were inspected to define initiation codons using homologies, To identify genomic regions with significant similarity, predicted position of ribosomal binding sites, and transcriptional terminators. protein comparisons were performed between the A. ferrooxidans The following bioinformatic programs were used to further complete genome sequence and the two draft genomes sequences of characterize candidate genes and their predicted protein products: A. caldus and A. thiooxidans. Fig. 2 shows a similarity map that BlastP and PsiBlast (Altschul et al., 1997), the suite of protein facilitates the identification of regions in the A. ferrooxidans genome comparison and classification programs available in InterproScan that have no counterparts in the other two genomes. This first step is (Mulder and Apweiler, 2007). Model metabolic pathways were required for a rapid identification of potential functional modules reconstructed using PRIAM (Claudel-Renard et al., 2003)and present in the model organism A. ferrooxidans and their respective compared to those obtained from BIOCYC (Caspi et al., 2008), KEGG locations in the genome sequence. Most of the exclusive regions of the (Kanehisa et al., 2008) and ERGO (Overbeek et al., 2003). Amino acid A. ferrooxidans genome are characterized by abnormal GC content and sequences derived for the genes identified in the genome sequence of GC skew signatures. Fig. 2 has four highlighted regions that A. ferrooxidans ATCC 23270 and draft genome sequences for A. caldus correspond to examples of conserved/non-conserved genomic loci: ATCC 51756 and A. thiooxidans ATCC 19377 were annotated, analyzed (A) pet-I and rus operons involved in iron oxidation in A. ferrooxidans. and compared to known metabolic models using perl scripts These loci are absent in the other two acidithiobacilli. They are located developed in our laboratory. The annotated genomes were displayed close to, and on either side of, the origin of replication; a position which in the interactive format of Artemis (Rutherford et al., 2000). provides duplicated copies early in the DNA replication cycle. It is not The genomes were compared at the amino acid level using tblastx known whether this location is important to augment the copy number − 5 (Altschul et al., 1997) using an e-value of 10 as cutoff to identify of the iron oxidation genes
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