Novel acid resistance genes from the metagenome of the Tinto River, an extremely acidic environment

Environmental Microbiology

Volumn 15, Issue 4, 2013, Pages 1088-1102

  Guazzaroni, María Eugenia ^a   Morgante, Verónica ^a   Mirete, Salvador ^a   González Pastor, José E ^a  

^a CENTRO DE ASTROBIOLOGÍA CSIC INTA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

ACID; BACTERIAL PROTEIN; CLPXP PROTEASE, E COLI; ENDOPEPTIDASE CLP; ESCHERICHIA COLI PROTEIN; LEXA PROTEIN, BACTERIA; RNA BINDING PROTEIN; SERINE PROTEINASE;

ANTIBIOTIC RESISTANCE; ARTICLE; BACILLUS SUBTILIS; BACTERIUM; CHEMISTRY; ESCHERICHIA COLI; GENETICS; METAGENOME; MICROBIOLOGY; PH; PLANKTON; PSEUDOMONAS PUTIDA; RHIZOSPHERE; RIVER; SPAIN;

ACIDS; BACILLUS SUBTILIS; BACTERIA; BACTERIAL PROTEINS; DRUG RESISTANCE, BACTERIAL; ENDOPEPTIDASE CLP; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HYDROGEN-ION CONCENTRATION; METAGENOME; PLANKTON; PSEUDOMONAS PUTIDA; RHIZOSPHERE; RIVERS; RNA-BINDING PROTEINS; SERINE ENDOPEPTIDASES; SPAIN;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PSEUDOMONAS PUTIDA;

EID: 84875877949     PISSN: 14622912     EISSN: 14622920     Source Type: Journal    
DOI: 10.1111/1462-2920.12021     Document Type: Article

References (71)

1. Aguilera, A., Zettler, E., Gomez, F., Amaral-Zettler, L., Rodriguez, N., and Amils, R. (2007) Distribution and seasonal variability in the benthic eukaryotic community of Rio Tinto (SW, Spain), an acidic, high metal extreme environment. Syst Appl Microbiol 30: 531-546.
2. Amaro, A.M., Chamorro, D., Seeger, M., Arredondo, R., Peirano, I., and Jerez, C.A. (1991) Effect of external pH perturbations on in vivo protein synthesis by the acidophilic bacterium Thiobacillus ferrooxidans. J Bacteriol 173: 910-915.
3. Andersen, J.B., Sternberg, C., Poulsen, L.K., Bjorn, S.P., Givskov, M., and Molin, S. (1998) New unstable variants of green fluorescent protein for studies of transient gene expression in bacteria. Appl Environ Microbiol 64: 2240-2246.
4. Ausubel, F.M., Brent, R., Kingston, R.E., Moore, D.D., Seidman, J.G., Smith, J.A., and Struhl, K. (1994) Current Protocols in Molecular Biology. New York, NY, USA: John Wiley & Sons.
5. Bagdasarian, M., Lurz, R., Ruckert, B., Franklin, F.C., Bagdasarian, M.M., Frey, J., and Timmis, K.N. (1981) Specific-purpose plasmid cloning vectors. II. Broad host range, high copy number, RSF1010-derived vectors, and a host-vector system for gene cloning in Pseudomonas. Gene 16: 237-247.
6. Baker-Austin, C., and Dopson, M. (2007) Life in acid: pH homeostasis in acidophiles. Trends Microbiol 15: 165-171.
7. Baross, J.A., and Hoffman, S.E. (1985) Submarine hydrothermal vents and associated gradient environments as sites for the origin and evolution of life. Orig Life Evol Biosph 15: 327-345.
8. Batrakov, S.G., Pivovarova, T.A., Esipov, S.E., Sheichenko, V.I., and Karavaiko, G.I. (2002) Beta-D-glucopyranosyl caldarchaetidylglycerol is the main lipid of the acidophilic, mesophilic, ferrous iron-oxidising archaeon Ferroplasma acidiphilum. Biochim Biophys Acta 1581: 29-35.
9. Beuttler, H., Hoffmann, J., Jeske, M., Hauer, B., Schmid, R.D., Altenbuchner, J., and Urlacher, V.B. (2011) Biosynthesis of zeaxanthin in recombinant Pseudomonas putida. Appl Microbiol Biotechnol 89: 1137-1147.
10. Booth, I.R., Cash, P., and O'Byrne, C. (2002) Sensing and adapting to acid stress. Antonie Van Leeuwenhoek 81: 33-42.
11. Chandu, D., and Nandi, D. (2004) Comparative genomics and functional roles of the ATP-dependent proteases Lon and Clp during cytosolic protein degradation. Res Microbiol 155: 710-719.
12. Chang, Y.Y., and Cronan, J.E., Jr (1999) Membrane cyclopropane fatty acid content is a major factor in acid resistance of Escherichia coli. Mol Microbiol 33: 249-259.
13. Choi, S.H., Baumler, D.J., and Kaspar, C.W. (2000) Contribution of dps to acid stress tolerance and oxidative stress tolerance in Escherichia coli O157:H7. Appl Environ Microbiol 66: 3911-3916.
14. Chong, M.L., Sabaratnam, V., Shirai, Y., and Hassan, M.A. (2009) Biohydrogen production from biomass and industrial wastes by dark fermentation. Int J Hydrogen Energy 34: 3277-3287.
15. Cox, M.M. (2001) Recombinational DNA repair of damaged replication forks in Escherichia coli: questions. Annu Rev Genet 35: 53-82.
16. Craig, J.W., Chang, F.Y., Kim, J.H., Obiajulu, S.C., and Brady, S.F. (2010) Expanding small-molecule functional metagenomics through parallel screening of broad-host-range cosmid environmental DNA libraries in diverse proteobacteria. Appl Environ Microbiol 76: 1633-1641.
17. D'Andrea, L.D., and Regan, L. (2003) TPR proteins: the versatile helix. Trends Biochem Sci 28: 655-662.
18. Dri, A.M., and Moreau, P.L. (1994) Control of the LexA regulon by pH: evidence for a reversible inactivation of the LexA repressor during the growth cycle of Escherichia coli. Mol Microbiol 12: 621-629.
19. van Duuren, J.B., Wijte, D., Karge, B., dos Santos, V.A., Yang, Y., Mars, A.E., and Eggink, G. (2012) pH-stat fed-batch process to enhance the production of cis, cis-muconate from benzoate by Pseudomonas putida KT2440-JD1. Biotechnol Prog 28: 85-92.
20. Earl, A.M., Losick, R., and Kolter, R. (2008) Ecology and genomics of Bacillus subtilis. Trends Microbiol 16: 269-275.
21. Enderle, P.J., and Farwell, M.A. (1998) Electroporation of freshly plated Escherichia coli and Pseudomonas aeruginosa cells. Biotechniques 25: 954-956, 958.
22. Fernandez-Arrojo, L., Guazzaroni, M.E., Lopez-Cortes, N., Beloqui, A., and Ferrer, M. (2010) Metagenomic era for biocatalyst identification. Curr Opin Biotechnol 21: 725-733.
23. Ferrero, R.L., Cussac, V., Courcoux, P., and Labigne, A. (1992) Construction of isogenic urease-negative mutants of Helicobacter pylori by allelic exchange. J Bacteriol 174: 4212-4217.
24. Foster, J.W. (2004) Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Microbiol 2: 898-907.
25. Frees, D., and Ingmer, H. (1999) ClpP participates in the degradation of misfolded protein in Lactococcus lactis. Mol Microbiol 31: 79-87.
26. Fütterer, O., Angelov, A., Liesegang, H., Gottschalk, G., Schleper, C., Schepers, B., etal. (2004) Genome sequence of Picrophilus torridus and its implications for life around pH 0. Proc Natl Acad Sci USA 101: 9091-9096.
27. Gabor, E.M., Alkema, W.B., and Janssen, D.B. (2004) Quantifying the accessibility of the metagenome by random expression cloning techniques. Environ Microbiol 6: 879-886.
28. Gajiwala, K.S., and Burley, S.K. (2000) HDEA, a periplasmic protein that supports acid resistance in pathogenic enteric bacteria. J Mol Biol 295: 605-612.
29. Ghrist, A.C., and Stauffer, G.V. (1995) Characterization of the Escherichia coli gcvR gene encoding a negative regulator of gcv expression. J Bacteriol 177: 4980-4984.
30. Golyshina, O.V., Pivovarova, T.A., Karavaiko, G.I., Kondrateva, T.F., Moore, E.R., Abraham, W.R., etal. (2000) Ferroplasma acidiphilum gen. nov., sp. nov., an acidophilic, autotrophic, ferrous-iron-oxidizing, cell-wall-lacking, mesophilic member of the Ferroplasmaceae fam. nov., comprising a distinct lineage of the Archaea. Int J Syst Evol Microbiol 50: 997-1006.
31. González-Toril, E., Llobet-Brossa, E., Casamayor, E.O., Amann, R., and Amils, R. (2003) Microbial ecology of an extreme acidic environment, the Tinto River. Appl Environ Microbiol 69: 4853-4865.
32. Goto, Y., Calciano, L.J., and Fink, A.L. (1990) Acid-induced folding of proteins. Proc Natl Acad Sci USA 87: 573-577.
33. Gottesman, S. (1996) Proteases and their targets in Escherichia coli. Annu Rev Genet 30: 465-506.
34. Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41: 95-98.
35. Hong, W., Jiao, W., Hu, J., Zhang, J., Liu, C., Fu, X., etal. (2005) Periplasmic protein HdeA exhibits chaperone-like activity exclusively within stomach pH range by transforming into disordered conformation. J Biol Chem 280: 27029-27034.
36. Johnson, D.B., and Hallberg, K.B. (2005) Acid mine drainage remediation options: a review. Sci Total Environ 338: 3-14.
37. Katayama, Y., Gottesman, S., Pumphrey, J., Rudikoff, S., Clark, W.P., and Maurizi, M.R. (1988) The two-component, ATP-dependent Clp protease of Escherichia coli. Purification, cloning, and mutational analysis of the ATP-binding component. J Biol Chem 263: 15226-15236.
38. Kern, R., Malki, A., Abdallah, J., Tagourti, J., and Richarme, G. (2007) Escherichia coli HdeB is an acid stress chaperone. J Bacteriol 189: 603-610.
39. Lehninger, A.L., Nelson, D.L., and Cox, M.M. (1993) Principles of Biochemistry, 2nd edn. New York, NY, USA: Worth Publishers.
40. Lim, E.M., Ehrlich, S.D., and Maguin, E. (2000) Identification of stress-inducible proteins in Lactobacillus delbrueckii subsp. bulgaricus. Electrophoresis 21: 2557-2561.
41. Little, J.W. (1984) Autodigestion of lexA and phage lambda repressors. Proc Natl Acad Sci USA 81: 1375-1379.
42. Little, J.W., and Mount, D.W. (1982) The SOS regulatory system of Escherichia coli. Cell 29: 11-22.
43. Lopez-Archilla, A.I., Marin, I., and Amils, R. (2001) Microbial community composition and ecology of an acidic aquatic environment: the Tinto River, Spain. Microb Ecol 41: 20-35.
44. Martinez, A., and Kolter, R. (1997) Protection of DNA during oxidative stress by the nonspecific DNA-binding protein Dps. J Bacteriol 179: 5188-5194.
45. Martínez-García, E., Calles, B., Arevalo-Rodriguez, M., and de Lorenzo, V. (2011) pBAM1: an all-synthetic genetic tool for analysis and construction of complex bacterial phenotypes. BMC Microbiol 11: 38.
46. Maurizi, M.R., Clark, W.P., Katayama, Y., Rudikoff, S., Pumphrey, J., Bowers, B., and Gottesman, S. (1990) Sequence and structure of Clp P, the proteolytic component of the ATP-dependent Clp protease of Escherichia coli. J Biol Chem 265: 12536-12545.
47. Mirete, S., de Figueras, C.G., and Gonzalez-Pastor, J.E. (2007) Novel nickel resistance genes from the rhizosphere metagenome of plants adapted to acid mine drainage. Appl Environ Microbiol 73: 6001-6011.
48. Oberto, J., Nabti, S., Jooste, V., Mignot, H., and Rouviere-Yaniv, J. (2009) The HU regulon is composed of genes responding to anaerobiosis, acid stress, high osmolarity and SOS induction. PLoS ONE 4: e4367.
49. Rappe, M.S., and Giovannoni, S.J. (2003) The uncultured microbial majority. Annu Rev Microbiol 57: 369-394.
50. Richard, H., and Foster, J.W. (2004) Escherichia coli glutamate- and arginine-dependent acid resistance systems increase internal pH and reverse transmembrane potential. J Bacteriol 186: 6032-6041.
51. Rosenfeld, N., Elowitz, M.B., and Alon, U. (2002) Negative autoregulation speeds the response times of transcription networks. J Mol Biol 323: 785-793.
52. Sambrook, J., and Russell, D. (2001) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY, USA: CSHL Press.
53. Scheufler, C., Brinker, A., Bourenkov, G., Pegoraro, S., Moroder, L., Bartunik, H., etal. (2000) Structure of TPR domain-peptide complexes: critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell 101: 199-210.
54. Shimada, H., Nemoto, N., Shida, Y., Oshima, T., and Yamagishi, A. (2002) Complete polar lipid composition of Thermoplasma acidophilum HO-62 determined by high-performance liquid chromatography with evaporative light-scattering detection. J Bacteriol 184: 556-563.
55. Silva-Rocha, R., and de Lorenzo, V. (2011) Implementing an OR-NOT (ORN) logic gate with components of the SOS regulatory network of Escherichia coli. Mol Biosyst 7: 2389-2396.
56. Silva-Rocha, R., Martínez-García, E., Calles, B., Chavarría, M., Arce-Rodríguez, A., de las Heras, A., etal. (2012) The Standard European Vector Architecture (SEVA): a coherent platform for the analysis and deployment of complex prokaryotic phenotypes. Nucleic Acids Res (accepted).
57. Small, P., Blankenhorn, D., Welty, D., Zinser, E., and Slonczewski, J.L. (1994) Acid and base resistance in Escherichia coli and Shigella flexneri: role of rpoS and growth pH. J Bacteriol 176: 1729-1737.
58. Smith, J.L. (2003) The role of gastric acid in preventing foodborne disease and how bacteria overcome acid conditions. J Food Prot 66: 1292-1303.
59. Sommer, M.O., Church, G.M., and Dantas, G. (2010) A functional metagenomic approach for expanding the synthetic biology toolbox for biomass conversion. Mol Syst Biol 6: 360.
60. Sousa, F.J., Lima, L.M., Pacheco, A.B., Oliveira, C.L., Torriani, I., Almeida, D.F., etal. (2006) Tetramerization of the LexA repressor in solution: implications for gene regulation of the E.coli SOS system at acidic pH. J Mol Biol 359: 1059-1074.
61. Spizizen, J. (1958) Transformation of biochemically deficient strains of Bacillus subtilis by deoxyribonucleate. Proc Natl Acad Sci USA 44: 1072-1078.
62. Streit, W.R., and Schmitz, R.A. (2004) Metagenomics-the key to the uncultured microbes. Curr Opin Microbiol 7: 492-498.
63. Tapley, T.L., Korner, J.L., Barge, M.T., Hupfeld, J., Schauerte, J.A., Gafni, A., etal. (2009) Structural plasticity of an acid-activated chaperone allows promiscuous substrate binding. Proc Natl Acad Sci USA 106: 5557-5562.
64. Thompson, S.A., and Blaser, M.J. (1995) Isolation of the Helicobacter pylori recA gene and involvement of the recA region in resistance to low pH. Infect Immun 63: 2185-2193.
65. Tucker, D.L., Tucker, N., and Conway, T. (2002) Gene expression profiling of the pH response in Escherichia coli. J Bacteriol 184: 6551-6558.
66. Wen, Y., Marcus, E.A., Matrubutham, U., Gleeson, M.A., Scott, D.R., and Sachs, G. (2003) Acid-adaptive genes of Helicobacter pylori. Infect Immun 71: 5921-5939.
67. Wertman, K.F., and Mount, D.W. (1985) Nucleotide sequence binding specificity of the LexA repressor of Escherichia coli K-12. J Bacteriol 163: 376-384.
68. Woo, K.M., Chung, W.J., Ha, D.B., Goldberg, A.L., and Chung, C.H. (1989) Protease Ti from Escherichia coli requires ATP hydrolysis for protein breakdown but not for hydrolysis of small peptides. J Biol Chem 264: 2088-2091.
69. Wu, Y.E., Hong, W., Liu, C., Zhang, L., and Chang, Z. (2008) Conserved amphiphilic feature is essential for periplasmic chaperone HdeA to support acid resistance in enteric bacteria. Biochem J 412: 389-397.
70. Wyman, C.E., Dale, B.E., Elander, R.T., Holtzapple, M., Ladisch, M.R., and Lee, Y.Y. (2005) Coordinated development of leading biomass pretreatment technologies. Bioresour Technol 96: 1959-1966.
71. Youngman, P., Perkins, J.B., and Losick, R. (1984) Construction of a cloning site near one end of Tn917 into which foreign DNA may be inserted without affecting transposition in Bacillus subtilis or expression of the transposon-borne erm gene. Plasmid 12: 1-9.