Phylogenetic analysis of bacterial and archaeal arsC gene sequences suggests an ancient, common origin for arsenate reductase
Tóm tắt
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. 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 γ-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 (γ-Proteobacteria) possess similar plasmid-encoded arsC sequences. 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.
Tài liệu tham khảo
Tamaki S, Frankenberger WT: Environmental biochemistry of arsenic. Rev Environ Cont Toxicol. 1992, 124: 79-110.
Cervantes C, Ji G, Ramirez JL, Silver S: Resistance to arsenic compounds in microorganisms. FEMS Microbiol Rev. 1994, 15: 355-367. 10.1016/0168-6445(94)90069-8.
Anderson GL, Williams J, Hille R: The purification and characterization of arsenite oxidase from Alcaligenes faecalis, a molybdenum-containing hydroxylase. J Biol Chem. 1992, 267: 23674-23682.
Muller D, Lièvremont D, Simeonova DD, Hubert J-C, Lett M-C: Arsenite oxidase aox genes from a metal-resistant β-Proteobacterium. J Bacteriol. 2003, 185: 135-141. 10.1128/JB.185.1.135-141.2003.
Abdrashitova SA, Abdullina GG, Ilyaletdinov AN: Role of arsenites in lipid peroxidation in Pseudomonas putida cells oxidizing arsenite. Mikrobiologiya. 1986, 55: 212-216.
Abdrashitova SA, Abdullina GG, Mynbaeva BN, Ilyaletdinov AN: Oxidation of iron and manganese by arsenic-oxidizing bacteria. Mikrobiologiya. 1990, 59: 85-89.
Ahmann D, Roberts AL, Krumholz LR, Morel FMM: Microbe grows by reducing arsenic. Nature. 1994, 371: 750-10.1038/371750a0.
Newman DK, Ahmann D, Morel FMM: A brief review of microbial arsenate respiration. Geomicrobiol. 1998, 15: 255-268.
Stolz JF, Oremland RS: Bacterial respiration of arsenic and selenium. FEMS Microbiol Rev. 1999, 23: 615-627. 10.1016/S0168-6445(99)00024-8.
Huber R, Sacher M, Vollmann A, Huber H, Rose D: Respiration of arsenate and selenate by hyperthermophilic archaea. System Appl Microbiol. 2000, 23: 305-314.
Ilyaletdinov AN, Abdrashitova SA: Autotrophic oxidation of arsenic by a culture of Pseudomonas arsenitoxidans. Mikrobiologiya. 1981, 50: 197-204.
Santini JM, Sly LI, Schnagl RD, Macy JM: A new chemolithoautotrophic arsenite-oxidizing bacterium isolated from a gold mine: phylogenetic, physiological, and preliminary biochemical studies. Appl Environ Microbiol. 2000, 66: 92-97.
Ji G, Silver S, Garber EAE, Ohtake H, Cervantes C, Corbisier P: Bacterial molecular genetics and enzymatic transformations of arsenate, arsenite, and chromate. In Biohydrometallurgical Technologies. Edited by: Torma AE, Apel ML, Brierly CL. 1993, Warrendale, PA: The Minerals, Metals & Materials Society, 529-539.
Kaur P, Rosen BP: Plasmid-encoded resistance to arsenic and antimony. Plasmid. 1992, 27: 29-40.
Wu J, Rosen BP: The arsD gene encodes a second trans-acting regulatory protein of the plasmid-encoded arsenical resistance operon. Mol Microbiol. 1993, 8: 615-623.
Neyt CN, Iriarte M, Thi VH, Cornelis GR: Virulence and arsenic resistance in Yersiniae. J Bacteriol. 1997, 179: 612-619.
Ji G, Silver S: Regulation and expression of the arsenic resistance operon from Staphylococcus aureus plasmid pI258. J Bacterio. 1992, 174: 3684-3694.
Rosenstein R, Peschel A, Wieland B, Gotz F: Expression and regulation of the antimonite, arsenite, and arsenate resistance operon of the Staphylococcus xylosus plasmid pSX267. J Bacteriol. 1992, 174: 3676-3683.
Carlin A, Shi W, Dey S, Rosen BP: The ars operon of Escherichia coli confers arsenical and antimonial resistance. J Bacteriol. 1995, 177: 981-986.
Diorio C, Cai J, Marmor J, Shinder R, DuBrow MS: An Escherichia coli chromosomal ars operon homolog is functional in arsenic detoxification and is conserved in Gram-negative bacteria. J Bacteriol. 1995, 177: 2050-2056.
Suzuki K, Wakao N, Kimura T, Sakka K, Ohmiya K: Expression and regulation of the arsenic resistance operon of Acidiphilum multivorum AIU 301 plasmid pKW301 in Escherichia coli. Appl Environ Microbiol. 1998, 64: 411-418.
Sato T, Kobayashi Y: The ars operon in the skin element of Bacillus subtilis confers resistance to arsenate and arsenite. J Bacteriol. 1998, 180: 1655-1661.
Cai J, Salmon K, DuBrow MS: A chromosomal ars operon homologue of Pseudomonas aeruginosa confers increased resistance to arsenic and antimony in Escherichia coli . Microbiology. 1998, 144: 2705-2713.
Bobrowicz P, Wysocki R, Owsianik G, Goffeau A, Ulaszewski S: Isolation of three contiguous genes, ACR1, ACR2 and ACR3, involved in resistance to arsenic compounds in the yeast Saccharomyces cerevisiae. Yeast. 1997, 13: 819-828. 10.1002/(SICI)1097-0061(199707)13:9<819::AID-YEA142>3.0.CO;2-Y.
Cullen WR, Reimer KJ: Arsenic speciation in the environment. Rev. 1989, 89: 713-764.
Ferguson JF, Gavis J: A review of the arsenic cycle in natural waters. Water Res. 1972, 6: 1259-1274. 10.1016/0043-1354(72)90052-8.
Butcher BG, Deane SM, Rawlings DE: The chromosomal arsenic resistance genes of Thiobacillus ferrooxidans have an unusual arrangement and confer increased arsenic and antimony resistance to Escherichia coli. Appl Environ Microbiol. 2000, 66: 1826-1833. 10.1128/AEM.66.5.1826-1833.2000.
Saltikov CW, Olson BH: Homology of Escherichia coli R773 arsA ,arsB, and arsC genes in arsenic-resistant bacteria isolated from raw sewage and arsenic-enriched creek waters. Appl Environ Microbiol. 2002, 68: 280-288. 10.1128/AEM.68.1.280-288.2002.
Jackson CR, Jackson EF, Dugas SL, Gamble K, Williams SE: Microbial transformations of arsenite and arsenate in natural environments. Recent Res Devel Microbiol. 2003,
Mukhopadhyay R, Rosen BP, Phung LT, Silver S: Microbial arsenic: from geocycles to genes and enzymes. FEMS Microbiol Rev. 2002, 26: 311-325. 10.1016/S0168-6445(02)00112-2.
Woese CR: Bacterial evolution. Microbiol Rev. 1987, 51: 221-271.
Wolf YI, Rogozin IB, Grishin NV, Tatusov RL, Koonin EV: Genome trees constructed using five different approaches suggest new major bacterial clades. BMC Evolutionary Biology. 2001, 1: 8-10.1186/1471-2148-1-8.
Doolittle RF: Convergent evolution: The need to be explicit. Trends Biochem Sci. 1994, 19: 15-18. 10.1016/0968-0004(94)90167-8.
Nei M, Kumar S: Molecular Evolution and Phylogenetics. 2000, New York: Oxford University Press
Aravind L, Tatusov RL, Wolf YI, Walker DR, Koonin EV: Evidence for massive gene exchange between archaeal and bacterial hyperthermophiles. Trends Genet. 1998, 14: 442-444. 10.1016/S0168-9525(98)01553-4.
Brown JR, Doolittle WF: Archaea and the prokaryote-to-eukaryote transition. Microbiol Mol Biol Rev. 1997, 61: 456-502.
Mirkin BG, Fenner TI, Galperin MY, Koonin EV: Algorithms for computing parsimonious evolutionary scenarios for genome evolution, the last universal common ancestor and dominance of horizontal gene transfer in the evolution of prokaryotes. BMC Evolutionary Biology. 2003, 3: 2-10.1186/1471-2148-3-2.
LeBrun E, Brugna M, Baymann F, Muller D, Lièvremont D, Lett M-C, Nitschke W: Arsenite oxidase, and ancient bioenergetic enzyme. Mol Biol Evol. 2003, 20: 686-693. 10.1093/molbev/msg071.
Russell MJ, Hall AJ: The emergence of life from iron monosulphide bubbles at a submarine hydrothermal redox and pH front. J Geol Soc Lond. 1997, 154: 377-402.
Martin W, Russell MJ: On the origin of cells: a hypothesis for the evolutionary transitions from abiotic geochemistry to chemoautotrophic prokaryotes, and from prokaryotes to nucleated cells. Phil Trans R Soc Lond. 2003, 358: 59-85. 10.1098/rstb.2002.1183.
Langner HW, Jackson CR, McDermott TR, Inskeep WP: Rapid oxidation of arsenite in a hot spring ecosystem in Yellowstone National Park. Environ Sci Technol. 2001, 35: 3302-3309. 10.1021/es0105562.
Jackson CR, Langner HW, Donahoe-Christiansen J, Inskeep WP, McDermott TR: Molecular analysis of microbial community structure in an arsenite-oxidizing acidic thermal spring. Environ Microbiol. 2001, 3: 532-542. 10.1046/j.1462-2920.2001.00221.x.
Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Rapp BA, Wheeler DL: GenBank. Nucleic Acids Res. 2000, 28: 15-18. 10.1093/nar/28.1.15.
Martin P, DeMel S, Shi J, Gladysheva T, Gatti DL, Rosen BP, Edwards BF: Insights into the structure, solvation, and mechanism of ArsC arsenate reductase, a novel arsenic detoxification enzyme. Structure. 2001, 9: 1071-1081. 10.1016/S0969-2126(01)00672-4.
Maidak BL, Cole JR, Lilburn TG, Parker CT, Saxman PR, Stredwick JM, Garrity GM, Li B, Olsen GJ, Pramanik S, Schmidt TM, Tiedje JM: The RDP (Ribosomal Database Project) continues. Nucleic Acids Re. 2000, 28: 173-174. 10.1093/nar/28.1.173.
Saitou N, Nei M: The neighbor-joining method: A new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987, 4: 406-425.
