Three functional β-carbonic anhydrases in Pseudomonas aeruginosa PAO1: Role in survival in ambient air

Microbiology (United Kingdom)

Volumn 159, Issue 8, 2013, Pages 1748-1759

  Lotlikar, Shalaka R ^a   Hnatusko, Shane ^a   Dickenson, Nicholas E ^a   Choudhari, Shyamal P ^a   Picking, Wendy L ^a   Patrauchan, Marianna A ^a  

^a OKLAHOMA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BICARBONATE; CARBON DIOXIDE; CARBONATE DEHYDRATASE I;

AMBIENT AIR; AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; CATALYSIS; CIRCULAR DICHROISM; CLADISTICS; GENOME; GENOME ANALYSIS; HYDRATION; IMMUNOBLOTTING; NONHUMAN; PH; PRIORITY JOURNAL; PSEUDOMONAS AERUGINOSA; TRANSPOSON;

AIR; BICARBONATES; BLOTTING, WESTERN; CARBON DIOXIDE; CARBONIC ANHYDRASES; CIRCULAR DICHROISM; CLONING, MOLECULAR; CLUSTER ANALYSIS; COENZYMES; COMPUTATIONAL BIOLOGY; CONSERVED SEQUENCE; DNA TRANSPOSABLE ELEMENTS; ENZYME STABILITY; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENOME, BACTERIAL; HYDROGEN-ION CONCENTRATION; MICROBIAL VIABILITY; MOLECULAR CONFORMATION; MUTAGENESIS, INSERTIONAL; PSEUDOMONAS AERUGINOSA; RECOMBINANT PROTEINS; SEQUENCE HOMOLOGY, AMINO ACID; ZINC;

EID: 84881252319     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.066357-0     Document Type: Article

References (70)

1. Aguilera, J., Petit, T., de Winde, J. H. & Pronk, J. T. (2005). Physiological and genome-wide transcriptional responses of Saccharomyces cerevisiae to high carbon dioxide concentrations. FEMS Yeast Res 5, 579-593.
2. Alber, B. E. & Ferry, J. G. (1994). A carbonic anhydrase from the archaeon Methanosarcina thermophila. Proc Natl Acad Sci U S A 91, 6909-6913.
3. Amoroso, G., Morell-Avrahov, L., Müller, D., Klug, K. & Sültemeyer, D. (2005). The gene NCE103 (YNL036w) from Saccharomyces cerevisiae encodes a functional carbonic anhydrase and its transcription is regulated by the concentration of inorganic carbon in the medium. Mol Microbiol 56, 549-558.
4. Braus-Stromeyer, S. A., Schnappauf, G., Braus, G. H., Gössner, A. S. & Drake, H. L. (1997). Carbonic anhydrase in Acetobacterium woodii and other acetogenic bacteria. J Bacteriol 179, 7197-7200.
5. 2 deprivation. Microbios 3, 241-246.
6. Brunzelle, J. S., Wawrzak, Z., Onopriyenko, O., Anderson, W. F. & Savchenko, A. (2011). 1.54a resolution crystal structure of a betacarbonic anhydrase from Salmonella enterica subsp. enterica serovar Typhimurium str. lt2.
7. Burghout, P., Cron, L. E., Gradstedt, H., Quintero, B., Simonetti, E., Bijlsma, J. J. E., Bootsma, H. J. & Hermans, P. W. M. (2010). Carbonic anhydrase is essential for Streptococcus pneumoniae growth in environmental ambient air. J Bacteriol 192, 4054-4062.
8. Burghout, P., Vullo, D., Scozzafava, A., Hermans, P. W. M. & Supuran, C. T. (2011). Inhibition of the b-carbonic anhydrase from Streptococcus pneumoniae by inorganic anions and small molecules: Toward innovative drug design of antiinfectives? Bioorg Med Chem 19, 243-248.
9. Bury-Moné, S., Mendz, G. L., Ball, G. E., Thibonnier, M., Stingl, K., Ecobichon, C., Avé, P., Huerre, M., Labigne, A. & other authors (2008). Roles of alpha and beta carbonic anhydrases of Helicobacter pylori in the urease-dependent response to acidity and in colonization of the murine gastric mucosa. Infect Immun 76, 497-509.
10. Covarrubias, A., Larsson, A. M., Högbom, M., Lindberg, J., Bergfors, T., Björkelid, C., Mowbray, S. L., Unge, T. & Jones, T. A. (2005). Structure and function of carbonic anhydrases from Mycobacterium tuberculosis. J Biol Chem 280, 18782-18789.
11. Covarrubias, A. S., Bergfors, T., Jones, T. A. & Högbom, M. (2006). Structural mechanics of the pH-dependent activity of b-carbonic anhydrase from Mycobacterium tuberculosis. J Biol Chem 281, 4993-4999.
12. Cronk, J. D., Endrizzi, J. A., Cronk, M. R., O'neill, J. W. & Zhang, K. Y. J. (2001). Crystal structure of E. coli beta-carbonic anhydrase, an enzyme with an unusual pH-dependent activity. Protein Sci 10, 911-922.
13. Cronk, J. D., Rowlett, R. S., Zhang, K. Y., Tu, C., Endrizzi, J. A., Lee, J., Gareiss, P. C. & Preiss, J. R. (2006). Identification of a novel noncatalytic bicarbonate binding site in eubacterial beta-carbonic anhydrase. Biochemistry 45, 4351-4361.
14. 2 of the growth and metabolism of micro-organisms. J Appl Bacteriol 67, 109-136.
15. Dobrinski, K. P., Boller, A. J. & Scott, K. M. (2010). Expression and function of four carbonic anhydrase homologs in the deep-sea chemolithoautotroph Thiomicrospira crunogena. Appl Environ Microbiol 76, 3561-3567.
16. Elleuche, S. & Pöggeler, S. (2010). Carbonic anhydrases in fungi. Microbiology 15, 23-29.
17. Enfors, S. O. & Molin, G. (1980). Effect of high concentrations of carbon dioxide on growth rate of Pseudomonas fragi, Bacillus cereus and Streptococcus cremoris. J Appl Bacteriol 48, 409-416.
18. Felce, J. & Saier, M. H., Jr (2004). Carbonic anhydrases fused to anion transporters of the SulP family: evidence for a novel type of bicarbonate transporter. J Mol Microbiol Biotechnol 8, 169-176.
19. Fukuzawa, H., Suzuki, E., Komukai, Y. & Miyachi, S. (1992). A gene homologous to chloroplast carbonic anhydrase (icfA) is essential to photosynthetic carbon dioxide fixation by Synechococcus PCC7942. Proc Natl Acad Sci U S A 89, 4437-4441.
20. Gill, C. O. & Tan, K. H. (1979). Effect of carbon dioxide on growth of Pseudomonas fluorescens. Appl Environ Microbiol 38, 237-240.
21. Guilloton, M. B., Korte, J. J., Lamblin, A. F., Fuchs, J. A. & Anderson, P. M. (1992). Carbonic anhydrase in Escherichia coli. A product of the cyn operon. J Biol Chem 267, 3731-3734.
22. Guilloton, M. B., Lamblin, A. F., Kozliak, E. I., Gerami-Nejad, M., Tu, C., Silverman, D., Anderson, P. M. & Fuchs, J. A. (1993). A physiological role for cyanate-induced carbonic anhydrase in Escherichia coli. J Bacteriol 175, 1443-1451.
23. 2 partial pressure. Biosci Biotechnol Biochem 67, 919-922.
24. Hewett-Emmett, D. & Tashian, R. E. (1996). Functional diversity, conservation, and convergence in the evolution of the alpha-, beta-, and gamma-carbonic anhydrase gene families. Mol Phylogenet Evol 5, 50-77.
25. Hoffmann, K. M., Samardzic, D., Heever, K. & Rowlett, R. S. (2011). Co(II)-substituted Haemophilus influenzae b-carbonic anhydrase: spectral evidence for allosteric regulation by pH and bicarbonate ion. Arch Biochem Biophys 511, 80-87.
26. Høiby, N. (2006). P. aeruginosa in cystic fibrosis patients resists host defenses, antibiotics. Microbe 1, 571-577.
27. Innocenti, A. & Supuran, C. T. (2010). Paraoxon, 4-nitrophenyl phosphate and acetate are substrates of a- but not of b-, c- and fcarbonic anhydrases. Bioorg Med Chem Lett 20, 6208-6212.
28. Iverson, T. M., Alber, B. E., Kisker, C., Ferry, J. G. & Rees, D. C. (2000). A closer look at the active site of c-class carbonic anhydrases: high-resolution crystallographic studies of the carbonic anhydrase from Methanosarcina thermophila. Biochemistry 39, 9222-9231.
29. Joseph, P., Turtaut, F., Ouahrani-Bettache, S., Montero, J. L., Nishimori, I., Minakuchi, T., Vullo, D., Scozzafava, A., Köhler, S. & other authors (2010). Cloning, characterization, and inhibition studies of a beta-carbonic anhydrase from Brucella suis. J Med Chem 53, 2277-2285.
30. Joseph, P., Ouahrani-Bettache, S., Montero, J. L., Nishimori, I., Minakuchi, T., Vullo, D., Scozzafava, A., Winum, J. Y., Köhler, S. & Supuran, C. T. (2011). A new b-carbonic anhydrase from Brucella suis, its cloning, characterization, and inhibition with sulfonamides and sulfamates, leading to impaired pathogen growth. Bioorg Med Chem 19, 1172-1178.
31. Kalai, S., Achour, W., Abdeladhim, A., Bejaoui, M. & Ben Hassen, A. (2005). [Pseudomonas aeruginosa isolated in immunocompromised patients: antimicrobial resistance, serotyping, and molecular typing]. Med Mal Infect 35, 530-535 (in French).
32. Kaur, S., Mishra, M. N. & Tripathi, A. K. (2009). Regulation of expression and biochemical characterization of a b-class carbonic anhydrase from the plant growth-promoting rhizobacterium, Azospirillum brasilense Sp7. FEMS Microbiol Lett 299, 149-158.
33. 2 on the growth rate of the Pneumococcus. J Bacteriol 43, 387-396.
34. King, A. D. & Nagel, C. W. (1975). Influence of carbon dioxide upon the metabolism of Pseudomonas aeruginosa. J Food Sci 40, 362-366.
35. 2 concentrations. J Bacteriol 184, 5018-5026.
36. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A. & other authors (2007). CLUSTAL W and CLUSTAL_X version 2.0. Bioinformatics 23, 2947-2948.
37. Mach, H., Middaugh, C. R. & Lewis, R. V. (1992). Statistical determination of the average values of the extinction coefficients of tryptophan and tyrosine in native proteins. Anal Biochem 200, 74-80.
38. Marchler-Bauer, A., Lu, S., Anderson, J. B., Chitsaz, F., Derbyshire, M. K., DeWeese-Scott, C., Fong, J. H., Geer, L. Y., Geer, R. C. & other authors (2011). CDD: a Conserved Domain Database for the functional annotation of proteins. Nucleic Acids Res 39 (Database issue), D225-D229.
39. Merlin, C., Masters, M., McAteer, S. & Coulson, A. (2003). Why is carbonic anhydrase essential to Escherichia coli? J Bacteriol 185, 6415-6424.
40. Mesaros, N., Nordmann, P., Plésiat, P., Roussel-Delvallez, M., Van Eldere, J., Glupczynski, Y., Van Laethem, Y., Jacobs, F., Lebecque, P. & other authors (2007). Pseudomonas aeruginosa: resistance and therapeutic options at the turn of the new millennium. Clin Microbiol Infect 13, 560-578.
41. Mitsuhashi, S., Ohnishi, J., Hayashi, M. & Ikeda, M. (2004). A gene homologous to b-type carbonic anhydrase is essential for the growth of Corynebacterium glutamicum under atmospheric conditions. Appl Microbiol Biotechnol 63, 592-601.
42. Mukherjee, S., Saha, B. & Das, A. K. (2009). Differential chemical and thermal unfolding pattern of Rv3588c and Rv1284 of Mycobacterium tuberculosis - a comparison by fluorescence and circular dichroism spectroscopy. Biophys Chem 141, 94-104.
43. Nishimori, I., Minakuchi, T., Kohsaki, T., Onishi, S., Takeuchi, H., Vullo, D., Scozzafava, A. & Supuran, C. T. (2007). Carbonic anhydrase inhibitors: the beta-carbonic anhydrase from Helicobacter pylori is a new target for sulfonamide and sulfamate inhibitors. Bioorg Med Chem Lett 17, 3585-3594.
44. Nishimori, I., Minakuchi, T., Vullo, D., Scozzafava, A., Innocenti, A. & Supuran, C. T. (2009). Carbonic anhydrase inhibitors. Cloning, characterization, and inhibition studies of a new beta-carbonic anhydrase from Mycobacterium tuberculosis. J Med Chem 52, 3116-3120.
45. Nishimori, I., Minakuchi, T., Maresca, A., Carta, F., Scozzafava, A. & Supuran, C. T. (2010). The b-carbonic anhydrases from Mycobacterium tuberculosis as drug targets. Curr Pharm Des 16, 3300-3309.
46. Nishimori, I., Minakuchi, T., Vullo, D., Scozzafava, A. & Supuran, C. T. (2011). Inhibition studies of the b-carbonic anhydrases from the bacterial pathogen Salmonella enterica serovar Typhimurium with sulfonamides and sulfamates. Bioorg Med Chem 19, 5023-5030.
47. Ohri, L. K. & Plummer, S. (2004). Prevention and control of nosocomial infections, 4th edition. Ann Pharmacother 38, 515-516.
48. Park, H.-M., Park, J. H., Choi, J. W., Lee, J., Kim, B. Y., Jung, C. H. & Kim, J. S. (2012). Structures of the c-class carbonic anhydrase homologue YrdA suggest a possible allosteric switch. Acta Crystallogr D Biol Crystallogr 68, 920-926.
49. Ramanan, R., Kannan, K., Vinayagamoorthy, N., Ramkumar, K., Sivanesan, S. & Chakrabarti, T. (2009). Purification and characterization of a novel plant-type carbonic anhydrase from Bacillus subtilis. Biotechnol Bioprocess Eng 14, 32-37.
50. Richard, P., Le Floch, R., Chamoux, C., Pannier, M., Espaze, E. & Richet, H. (1994). Pseudomonas aeruginosa outbreak in a burn unit: role of antimicrobials in the emergence of multiply resistant strains. J Infect Dis 170, 377-383.
51. Rowlett, R. S. (2010). Structure and catalytic mechanism of the bcarbonic anhydrases. Biochim Biophys Acta 1804, 362-373.
52. Sawaya, M. R., Cannon, G. C., Heinhorst, S., Tanaka, S., Williams, E. B., Yeates, T. O. & Kerfeld, C. A. (2006). The structure of beta- \carbonic anhydrase from the carboxysomal shell reveals a distinct subclass with one active site for the price of two. J Biol Chem 281, 7546-7555.
53. 2 at the cellmembrane. J GenPhysiol 44, 869-887.
54. Şentürk, M., Gülçin, I., Beydemir, Ş, Küfrevioǧlu, Ö. Ş. & Supuran, C. T. (2011). In vitro inhibition of human carbonic anhydrase I and II isozymes with natural phenolic compounds. Chem Biol Drug Des 77, 494-499.
55. Smith, K. S. & Ferry, J. G. (1999). A plant-type (beta-class) carbonic anhydrase in the thermophilic methanoarchaeon Methanobacterium thermoautotrophicum. J Bacteriol 181, 6247-6253.
56. Smith, K. S. & Ferry, J. G. (2000). Prokaryotic carbonic anhydrases. FEMS Microbiol Rev 24, 335-366.
57. Smith, K. S., Jakubzick, C., Whittam, T. S. & Ferry, J. G. (1999). Carbonic anhydrase is an ancient enzyme widespread in prokaryotes. Proc Natl Acad Sci U S A 96, 15184-15189.
58. Smith, K. S., Cosper, N. J., Stalhandske, C., Scott, R. A. & Ferry, J. G. (2000). Structural and kinetic characterization of an archaeal betaclass carbonic anhydrase. J Bacteriol 182, 6605-6613.
59. So, A. K. C. & Espie, G. S. (1998). Cloning, characterization and expression of carbonic anhydrase from the cyanobacterium Synechocystis PCC6803. Plant Mol Biol 37, 205-215.
60. Son, M. S., Matthews, W. J., Jr, Kang, Y., Nguyen, D. T. & Hoang, T. T. (2007). In vivo evidence of Pseudomonas aeruginosa nutrient acquisition and pathogenesis in the lungs of cystic fibrosis patients. Infect Immun 75, 5313-5324.
61. Supuran, C. T. (2007a). Novel targets against Helicoblacter pylori: a bioinformatic approach. Future Microbiol 2, 111-114.
62. Supuran, C. T. (2007b). Carbonic anhydrases as drug targets-an overview. Curr Top Med Chem 7, 825-833.
63. Supuran, C. T. (2008). Carbonic anhydrases-an overview. Curr Pharm Des 14, 603-614.
64. Supuran, C. T. (2011). Bacterial carbonic anhydrases as drug targets: towards novel antibiotics? Front Pharmacol 2, 1-6.
65. Supuran, C. T. & Scozzafava, A. (2007). Carbonic anhydrases as targets for medicinal chemistry. Bioorg Med Chem 15, 4336-4350.
66. Tripp, B. C., Smith, K. & Ferry, J. G. (2001). Carbonic anhydrase: new insights for an ancient enzyme. J Biol Chem 276, 48615-48618.
67. Valdivia, R. H. & Falkow, S. (1997). Fluorescence-based isolation of bacterial genes expressed within host cells. Science 277, 2007-2011.
68. Vullo, D., Nishimori, I., Minakuchi, T., Scozzafava, A. & Supuran, C. T. (2011). Inhibition studies with anions and small molecules of two novel b-carbonic anhydrases from the bacterial pathogen Salmonella enterica serovar Typhimurium. Bioorg Med Chem Lett 21, 3591-3595.
69. Winum, J. Y., Köhler, S. & Supuran, C. T. (2010). Brucella carbonic anhydrases: new targets for designing anti-infective agents. Curr Pharm Des 16, 3310-3316.
70. Xu, Y., Feng, L., Jeffrey, P. D., Shi, Y. & Morel, F. M. M. (2008). Structure and metal exchange in the cadmium carbonic anhydrase of marine diatoms. Nature 452, 56-61.