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Phylogenetic analysis of bacterial and archaeal arsC gene sequences suggests an ancient, common origin for arsenate reductase.

Jackson CR, Dugas SL - BMC Evol. Biol. (2003)

Bottom Line: The overall phylogeny of the arsenate reductases suggests a single, early origin of the arsC gene and subsequent sequence divergence to give the distinct arsC classes that exist today.Discrepancies between 16S rRNA and arsC phylogenies support the role of horizontal gene transfer (HGT) in the evolution of arsenate reductases, with a number of instances of HGT early in bacterial arsC evolution.Overall, arsC phylogeny is complex and is likely the result of a number of evolutionary mechanisms.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biological Sciences, SLU 10736, Southeastern Louisiana University, Hammond, LA 70402, USA. cjackson@selu.edu

ABSTRACT

Background: The ars gene system provides arsenic resistance for a variety of microorganisms and can be chromosomal or plasmid-borne. The arsC gene, which codes for an arsenate reductase is essential for arsenate resistance and transforms arsenate into arsenite, which is extruded from the cell. A survey of GenBank shows that arsC appears to be phylogenetically widespread both in organisms with known arsenic resistance and those organisms that have been sequenced as part of whole genome projects.

Results: Phylogenetic analysis of aligned arsC sequences shows broad similarities to the established 16S rRNA phylogeny, with separation of bacterial, archaeal, and subsequently eukaryotic arsC genes. However, inconsistencies between arsC and 16S rRNA are apparent for some taxa. Cyanobacteria and some of the gamma-Proteobacteria appear to possess arsC genes that are similar to those of Low GC Gram-positive Bacteria, and other isolated taxa possess arsC genes that would not be expected based on known evolutionary relationships. There is no clear separation of plasmid-borne and chromosomal arsC genes, although a number of the Enterobacteriales (gamma-Proteobacteria) possess similar plasmid-encoded arsC sequences.

Conclusion: The overall phylogeny of the arsenate reductases suggests a single, early origin of the arsC gene and subsequent sequence divergence to give the distinct arsC classes that exist today. Discrepancies between 16S rRNA and arsC phylogenies support the role of horizontal gene transfer (HGT) in the evolution of arsenate reductases, with a number of instances of HGT early in bacterial arsC evolution. Plasmid-borne arsC genes are not monophyletic suggesting multiple cases of chromosomal-plasmid exchange and subsequent HGT. Overall, arsC phylogeny is complex and is likely the result of a number of evolutionary mechanisms.

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Maximum parsimony tree based on arsC gene sequences.The tree was constructed using the same 408 informative positions used in the ED analysis. Numbers represent percentages of 1000 bootstraps and are only shown for bootstrap values <80%. Plasmid-borne arsC genes are indicated by "plasmid" following the organism name. Names in boxes represent branches that are inconsistent with the 16S rRNA tree.
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Figure 3: Maximum parsimony tree based on arsC gene sequences.The tree was constructed using the same 408 informative positions used in the ED analysis. Numbers represent percentages of 1000 bootstraps and are only shown for bootstrap values <80%. Plasmid-borne arsC genes are indicated by "plasmid" following the organism name. Names in boxes represent branches that are inconsistent with the 16S rRNA tree.

Mentions: The arsC phylogenies obtained by evolutionary distance (ED) analysis (Figure 2) and maximum parsimony (MP; Figure 3) showed a number of broad similarities to the 16S rRNA tree. There was clear separation of Archaea and Bacteria (with the sole eukaryote, S. cerevisiae, grouping towards Archaea), and also general grouping of the different bacterial divisions; all the archaeal arsC genes were from the Euryarchaeota so it was not possible to examine division level phylogeny for Archaea. Both treeing methods support the existence of at least three major classes of arsC genes, corresponding to the Archaea/Eukarya, the Enterobacteriales (enteric γ-Proteobacteria) and α-Proteobacteria, and the Low GC Gram-positive Bacteria. At a basic level, these broad groupings of arsC correspond to the three distinct classes of arsenate reductases that others have observed [30], and these three groups had low sequence similarity to each other (less than 33% similarity between the Bacteria and Archaea/Eukarya, and 48% similarity between the two major bacterial groups). However, the analysis reported here includes more diverse arsC sequences and suggests that other deeply branching types of arsC exist. For example, the arsC sequences from major divisions of Bacteria such as the Green Sulfur Bacteria (represented by Chlorobium tepidum) and the Deinococcales (represented by D. radiodurans) are loosely associated with either the Enterobacteriales/α-Proteobacteria (Figure 2) or Low GC Gram-positive Bacteria (Figure 3) depending upon the analysis used, but in either case diverge to form their own deep branches, suggesting that they possess distinct arsenate reductases. Thus, the suggestion that the three previously reported classes of arsenate reductases developed through convergent evolution [30] seems flawed: not only does arsC phylogeny show broad parallels to the accepted 16S rRNA phylogeny, but deep bacterial divisions appear to possess the distinct arsenate reductases that would be expected from divergence from a common origin. Given the alternate hypotheses of (1) Common origin followed by sequence divergence, or (2) Independent origin of multiple arsC sequence types with broadly similar reaction centers and general mechanisms, based on the phylogenies observed and the general rarity of convergent evolution at a sequence level [33,34] we suggest that the former is more likely.


Phylogenetic analysis of bacterial and archaeal arsC gene sequences suggests an ancient, common origin for arsenate reductase.

Jackson CR, Dugas SL - BMC Evol. Biol. (2003)

Maximum parsimony tree based on arsC gene sequences.The tree was constructed using the same 408 informative positions used in the ED analysis. Numbers represent percentages of 1000 bootstraps and are only shown for bootstrap values <80%. Plasmid-borne arsC genes are indicated by "plasmid" following the organism name. Names in boxes represent branches that are inconsistent with the 16S rRNA tree.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC183826&req=5

Figure 3: Maximum parsimony tree based on arsC gene sequences.The tree was constructed using the same 408 informative positions used in the ED analysis. Numbers represent percentages of 1000 bootstraps and are only shown for bootstrap values <80%. Plasmid-borne arsC genes are indicated by "plasmid" following the organism name. Names in boxes represent branches that are inconsistent with the 16S rRNA tree.
Mentions: The arsC phylogenies obtained by evolutionary distance (ED) analysis (Figure 2) and maximum parsimony (MP; Figure 3) showed a number of broad similarities to the 16S rRNA tree. There was clear separation of Archaea and Bacteria (with the sole eukaryote, S. cerevisiae, grouping towards Archaea), and also general grouping of the different bacterial divisions; all the archaeal arsC genes were from the Euryarchaeota so it was not possible to examine division level phylogeny for Archaea. Both treeing methods support the existence of at least three major classes of arsC genes, corresponding to the Archaea/Eukarya, the Enterobacteriales (enteric γ-Proteobacteria) and α-Proteobacteria, and the Low GC Gram-positive Bacteria. At a basic level, these broad groupings of arsC correspond to the three distinct classes of arsenate reductases that others have observed [30], and these three groups had low sequence similarity to each other (less than 33% similarity between the Bacteria and Archaea/Eukarya, and 48% similarity between the two major bacterial groups). However, the analysis reported here includes more diverse arsC sequences and suggests that other deeply branching types of arsC exist. For example, the arsC sequences from major divisions of Bacteria such as the Green Sulfur Bacteria (represented by Chlorobium tepidum) and the Deinococcales (represented by D. radiodurans) are loosely associated with either the Enterobacteriales/α-Proteobacteria (Figure 2) or Low GC Gram-positive Bacteria (Figure 3) depending upon the analysis used, but in either case diverge to form their own deep branches, suggesting that they possess distinct arsenate reductases. Thus, the suggestion that the three previously reported classes of arsenate reductases developed through convergent evolution [30] seems flawed: not only does arsC phylogeny show broad parallels to the accepted 16S rRNA phylogeny, but deep bacterial divisions appear to possess the distinct arsenate reductases that would be expected from divergence from a common origin. Given the alternate hypotheses of (1) Common origin followed by sequence divergence, or (2) Independent origin of multiple arsC sequence types with broadly similar reaction centers and general mechanisms, based on the phylogenies observed and the general rarity of convergent evolution at a sequence level [33,34] we suggest that the former is more likely.

Bottom Line: The overall phylogeny of the arsenate reductases suggests a single, early origin of the arsC gene and subsequent sequence divergence to give the distinct arsC classes that exist today.Discrepancies between 16S rRNA and arsC phylogenies support the role of horizontal gene transfer (HGT) in the evolution of arsenate reductases, with a number of instances of HGT early in bacterial arsC evolution.Overall, arsC phylogeny is complex and is likely the result of a number of evolutionary mechanisms.

View Article: PubMed Central - HTML - PubMed

Affiliation: Department of Biological Sciences, SLU 10736, Southeastern Louisiana University, Hammond, LA 70402, USA. cjackson@selu.edu

ABSTRACT

Background: The ars gene system provides arsenic resistance for a variety of microorganisms and can be chromosomal or plasmid-borne. The arsC gene, which codes for an arsenate reductase is essential for arsenate resistance and transforms arsenate into arsenite, which is extruded from the cell. A survey of GenBank shows that arsC appears to be phylogenetically widespread both in organisms with known arsenic resistance and those organisms that have been sequenced as part of whole genome projects.

Results: Phylogenetic analysis of aligned arsC sequences shows broad similarities to the established 16S rRNA phylogeny, with separation of bacterial, archaeal, and subsequently eukaryotic arsC genes. However, inconsistencies between arsC and 16S rRNA are apparent for some taxa. Cyanobacteria and some of the gamma-Proteobacteria appear to possess arsC genes that are similar to those of Low GC Gram-positive Bacteria, and other isolated taxa possess arsC genes that would not be expected based on known evolutionary relationships. There is no clear separation of plasmid-borne and chromosomal arsC genes, although a number of the Enterobacteriales (gamma-Proteobacteria) possess similar plasmid-encoded arsC sequences.

Conclusion: The overall phylogeny of the arsenate reductases suggests a single, early origin of the arsC gene and subsequent sequence divergence to give the distinct arsC classes that exist today. Discrepancies between 16S rRNA and arsC phylogenies support the role of horizontal gene transfer (HGT) in the evolution of arsenate reductases, with a number of instances of HGT early in bacterial arsC evolution. Plasmid-borne arsC genes are not monophyletic suggesting multiple cases of chromosomal-plasmid exchange and subsequent HGT. Overall, arsC phylogeny is complex and is likely the result of a number of evolutionary mechanisms.

Show MeSH
Related in: MedlinePlus