Tanscriptional profiling of staphylococcus aureus during growth in 2 M NaCl leads to clarification of physiological roles for Kdp and Ktr K+ uptake systems

mBio

Volumn 4, Issue 4, 2013, Pages

  Price Whelan, Alexa ^a   Poon, Chun Kit ^a   Benson, Meredith A ^b   Eidem, Tess T ^c   Roux, Christelle M ^c   Boyd, Jeffrey M ^d   Dunman, Paul M ^c   Torres, Victor J ^b   Krulwich, Terry A ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^d The State University of New Jersey   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

KDP PROTEIN; KDPDE PROTEIN; KTR PROTEIN; KTRB PROTEIN; KTRC PROTEIN; KTRD PROTEIN; MEMBRANE PROTEIN; POTASSIUM ION; SIALIC ACID; SODIUM CHLORIDE; SODIUM ION; SUGAR; UNCLASSIFIED DRUG;

AMINO ACID METABOLISM; ARTICLE; BACTERIAL CAPSULE; BACTERIAL GENE; BACTERIAL GROWTH; BACTERIAL METABOLISM; BACTERIUM MUTANT; BIOSYNTHESIS; CAP5 GENE; CAP5B GENE; CONTROLLED STUDY; CULTURE MEDIUM; GENE LOCUS; GENETIC TRAIT; KDP GENE; KDPA GENE; NONHUMAN; OSMOLALITY; OSMOTIC STRESS; PHENOTYPE; POLYMERASE CHAIN REACTION; POTASSIUM CELL LEVEL; POTASSIUM TRANSPORT; PRIORITY JOURNAL; PROTEIN FUNCTION; SODIUM TRANSPORT; STAPHYLOCOCCUS AUREUS; TRANSCRIPTOMICS;

STAPHYLOCOCCUS AUREUS;

EID: 85052488804     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00407-13     Document Type: Article

References (62)

1. Measures JC. 1975. Role of amino acids in osmoregulation of nonhalophilic bacteria. Nature 257:398-400.
2. Chapman GH. 1945. The significance of sodium chloride in studies of staphylococci. J. Bacteriol. 50:201-203.
3. Kahl BC, Duebbers A, Lubritz G, Haeberle J, Koch HG, Ritzerfeld B, Reilly M, Harms E, Proctor RA, Herrmann M, Peters G. 2003. Population dynamics of persistent Staphylococcus aureus isolated from the airways of cystic fibrosis patients during a 6-year prospective study. J. Clin. Microbiol. 41:4424-4427.
4. Graham JE, Wilkinson BJ. 1992. Staphylococcus aureus osmoregulation: roles for choline, glycine betaine, proline, and taurine. J. Bacteriol. 174: 2711-2716.
5. Csonka LN. 1989. Physiological and genetic responses of bacteria to osmotic stress. Microbiol. Rev. 53:121-147.
6. Christian JH, Waltho JA. 1961. The sodium and potassium content of non-halophilic bacteria in relation to salt tolerance. J. Gen. Microbiol. 25:97-102.
7. Epstein W, Schultz SG. 1965. Cation transport in Escherichia coli: V. Regulation of cation content. J. Gen. Physiol. 49:221-234.
8. Ørskov SL. 1948. Experiments on active and passive permeability of Bacillus coli communis. Acta Pathol. Microbiol. Scand. 25:277-283.
9. Tempest DW, Meers JL, Brown CM. 1970. Influence of environment on the content and composition of microbial free amino acid pools. J. Gen. Microbiol. 64:171-185.
10. Bremer E. 2002. Adaptation to changing osmolarity, p 385-391. In Sonenshein AL, Hoch JA, Losick R (ed), Bacillus subtilis and its closest relatives: from genes to cells. ASM Press, Washington, DC.
11. Christian JH, Waltho JA. 1964. The composition of Staphylococcus aureus in relation to the water activity of the growth medium. J. Gen. Microbiol. 35:205-213.
12. Padan E, Bibi E, Ito M, Krulwich TA. 2005. Alkaline pH homeostasis in bacteria: new insights. Biochim. Biophys. Acta 1717:67-88.
13. Miller KJ, Zelt SC, Bae JH. 1991. Glycine betaine and proline are the principal compatible solutes of Staphylococcus aureus. Curr. Microbiol. 23:131-137.
14. Pourkomailian B, Booth IR. 1994. Glycine betaine transport by Staphylococcus aureus: evidence for feedback regulation of the activity of the two transport systems. Microbiology 140:3131-3138.
15. Townsend DE, Wilkinson BJ. 1992. Proline transport in Staphylococcus aureus: a high-affinity system and a low-affinity system involved in osmoregulation. J. Bacteriol. 174:2702-2710.
16. Scybert S, Pechous R, Sitthisak S, Nadakavukaren MJ, Wilkinson BJ, Jayaswal RK. 2003. NaCl-sensitive mutant of Staphylococcus aureus has a Tn917-lacZ insertion in its ars operon. FEMS Microbiol. Lett. 222: 171-176.
17. Vijaranakul U, Xiong A, Lockwood K, Jayaswal RK. 1998. Cloning and nucleotide sequencing of a Staphylococcus aureus gene encoding a branched-chain-amino-acid transporter. Appl. Environ. Microbiol. 64: 763-767.
18. Vijaranakul U, Nadakavukaren MJ, Bayles DO, Wilkinson BJ, Jayaswal RK. 1997. Characterization of an NaCl-sensitive Staphylococcus aureus mutant and rescue of the NaCl-sensitive phenotype by glycine betaine but not by other compatible solutes. Appl. Environ. Microbiol. 63:1889-1897.
19. Domínguez-Ferreras A, Muñoz S, Olivares J, Soto MJ, Sanjuán J. 2009. Role of potassium uptake systems in Sinorhizobium meliloti osmoadaptation and symbiotic performance. J. Bacteriol. 191:2133-2143.
20. Gowrishankar J. 1985. Identification of osmoresponsive genes in Escherichia coli: evidence for participation of potassium and proline transport systems in osmoregulation. J. Bacteriol. 164:434-445.
21. Laimins LA, Rhoads DB, Epstein W. 1981. Osmotic control of kdp operon expression in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 78: 464-468.
22. Matsunaga J, Coutinho ML. 2012. Positive regulation of Leptospira interrogans kdp expression by KdpE as demonstrated with a novel betagalactosidase reporter in Leptospira biflexa. Appl. Environ. Microbiol. 78: 5699-5707.
23. Polarek JW, Williams G, Epstein W. 1992. The products of the kdpDE operon are required for expression of the Kdp ATPase of Escherichia coli. J. Bacteriol. 174:2145-2151.
24. Walderhaug MO, Polarek JW, Voelkner P, Daniel JM, Hesse JE, Altendorf K, Epstein W. 1992. KdpD and KdpE, proteins that control expression of the kdpABC operon, are members of the two-component sensoreffector class of regulators. J. Bacteriol. 174:2152-2159.
25. Xue T, You Y, Hong D, Sun H, Sun B. 2011. The Staphylococcus aureus KdpDE two-component system couples extracellular K+ sensing and Agr signaling to infection programming. Infect. Immun. 79:2154-2167.
26. Zhao L, Xue T, Shang F, Sun H, Sun B. 2010. Staphylococcus aureus AI-2 quorum sensing associates with the KdpDE two-component system to regulate capsular polysaccharide synthesis and virulence. Infect. Immun. 78:3506-3515.
27. O'Riordan K, Lee JC. 2004. Staphylococcus aureus capsular polysaccharides. Clin. Microbiol. Rev. 17:218-234.
28. Townsend DE, Kaenjak A, Jayaswal RK, Wilkinson BJ. 1996. Proline is biosynthesized from arginine in Staphylococcus aureus. Microbiology 142: 1491-1497.
29. Zaprasis A, Brill J, Thüring M, Wünsche G, Heun M, Barzantny H, Hoffmann T, Bremer E. 2013. Osmoprotection of Bacillus subtilis through import and proteolysis of proline-containing peptides. Appl. Environ. Microbiol. 79:576-587.
30. Stapleton MR, Horsburgh MJ, Hayhurst EJ, Wright L, Jonsson IM, Tarkowski A, Kokai-Kun JF, Mond JJ, Foster SJ. 2007. Characterization of IsaA and SceD, two putative lytic transglycosylases of Staphylococcus aureus. J. Bacteriol. 189:7316-7325.
31. Olson ME, King JM, Yahr TL, Horswill AR. 2013. Sialic acid catabolism in Staphylococcus aureus. J. Bacteriol. 195:1779-1788.
32. Almagro-Moreno S, Boyd EF. 2009. Insights into the evolution of sialic acid catabolism among bacteria. BMC Evol. Biol. 9:118. doi:10.1186/ 1471-2148-9-118.
33. Kluytmans J, van Belkum A, Verbrugh H. 1997. Nasal carriage of Staphylococcus aureus: epidemiology, underlying mechanisms, and associated risks. Clin. Microbiol. Rev. 10:505-520.
34. Corratgé-Faillie C, Jabnoune M, Zimmermann S, Véry AA, Fizames C, Sentenac H. 2010. Potassium and sodium transport in non-animal cells: the Trk/Ktr/HKT transporter family. Cell. Mol. Life Sci. 67:2511-2532.
35. Roosild TP, Castronovo S, Miller S, Li C, Rasmussen T, Bartlett W, Gunasekera B, Choe S, Booth IR. 2009. KTN (RCK) domains regulate K+ channels and transporters by controlling the dimer-hinge conformation. Structure 17:893-903.
36. Kröning N, Willenborg M, Tholema N, Hänelt I, Schmid R, Bakker EP. 2007. ATP binding to the KTN/RCK subunit KtrA from the K+-uptake system KtrAB of Vibrio alginolyticus: its role in the formation of the KtrAB complex and its requirement in vivo. J. Biol. Chem. 282:14018-14027.
37. Holtmann G, Bakker EP, Uozumi N, Bremer E. 2003. KtrAB and KtrCD: two K+ uptake systems in Bacillus subtilis and their role in adaptation to hypertonicity. J. Bacteriol. 185:1289-1298.
38. Ballal A, Basu B, Apte SK. 2007. The Kdp-ATPase system and its regulation. J. Biosci. 32:559-568.
39. Vieira-Pires RS, Szollosi A, Morais-Cabral JH. 2013. The structure of the KtrAB potassium transporter. Nature 496:323-328.
40. Fey PD, Endres JL, Yajjala VK, Widhelm TJ, Boissy RJ, Bose JL, Bayles KW. 2013. A genetic resource for rapid and comprehensive phenotype screening of nonessential Staphylococcus aureus genes. mBio 4(1):e00537-12. doi:10.1128/mBio.00537-12.
41. Corrigan RM, Campeotto I, Jeganathan T, Roelofs KG, Lee VT, Gründling A. 2013. Systematic identification of conserved bacterial c-di-AMP receptor proteins. Proc. Natl. Acad. Sci. U. S. A. 110:9084-9089.
42. Valihrach L, Demnerova K. 2012. Impact of normalization method on experimental outcome using RT-qPCR in Staphylococcus aureus. J. Microbiol. Methods 90:214-216.
43. Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT. 2009. The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin. Chem. 55:611-622.
44. Bertani G. 2004. Lysogeny at mid-twentieth century: P1, P2, and other experimental systems. J. Bacteriol. 186:595-600.
45. Pattee PA, Neveln DS. 1975. Transformation analysis of three linkage groups in Staphylococcus aureus. J. Bacteriol. 124:201-211.
46. Sambrook J, Russell DW. 2001. Molecular cloning: a laboratory manual, 3rd ed, p. 7.31-7.34. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
47. Dunman PM, Murphy E, Haney S, Palacios D, Tucker-Kellogg G, Wu S, Brown EL, Zagursky RJ, Shlaes D, Projan SJ. 2001. Transcription profiling-based identification of Staphylococcus aureus genes regulated by the agr and/or sarA loci. J. Bacteriol. 183:7341-7353.
48. Beenken KE, Dunman PM, McAleese F, Macapagal D, Murphy E, Projan SJ, Blevins JS, Smeltzer MS. 2004. Global gene expression in Staphylococcus aureus biofilms. J. Bacteriol. 186:4665-4684.
49. Bischoff M, Dunman P, Kormanec J, Macapagal D, Murphy E, Mounts W, Berger-Bächi B, Projan S. 2004. Microarray-based analysis of the Staphylococcus aureus sigmaB regulon. J. Bacteriol. 186:4085-4099.
50. Anderson KL, Roberts C, Disz T, Vonstein V, Hwang K, Overbeek R, Olson PD, Projan SJ, Dunman PM. 2006. Characterization of the Staphylococcus aureus heat shock, cold shock, stringent, and SOS responses and their effects on log-phase mRNA turnover. J. Bacteriol. 188:6739-6756.
51. Roberts C, Anderson KL, Murphy E, Projan SJ, Mounts W, Hurlburt B, Smeltzer M, Overbeek R, Disz T, Dunman PM. 2006. Characterizing the effect of the Staphylococcus aureus virulence factor regulator, SarA, on log-phase mRNA half-lives. J. Bacteriol. 188:2593-2603.
52. Yuen T, Zhang W, Ebersole BJ, Sealfon SC. 2002. Monitoring G-protein-coupled receptor signaling with DNA microarrays and realtime polymerase chain reaction. Methods Enzymol. 345:556-569.
53. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T) method. Methods 25:402-408.
54. Theis T, Skurray RA, Brown MH. 2007. Identification of suitable internal controls to study expression of a Staphylococcus aureus multidrug resistance system by quantitative real-time PCR. J. Microbiol. Methods 70: 355-362.
55. Wörmann ME, Reichmann NT, Malone CL, Horswill AR, Gründling A. 2011. Proteolytic cleavage inactivates the Staphylococcus aureus lipoteichoic acid synthase. J. Bacteriol. 193:5279-5291.
56. Arnaud M, Chastanet A, Débarbouillé M. 2004. New vector for efficient allelic replacement in naturally nontransformable, low-GC-content, gram-positive bacteria. Appl. Environ. Microbiol. 70:6887-6891.
57. Memmi G, Filipe SR, Pinho MG, Fu Z, Cheung A. 2008. Staphylococcus aureus PBP4 is essential for beta-lactam resistance in communityacquired methicillin-resistant strains. Antimicrob. Agents Chemother. 52: 3955-3966.
58. Horton RM. 1995. PCR-mediated recombination and mutagenesis. SOEing together tailor-made genes. Mol. Biotechnol. 3:93-99.
59. Kennedy AD, Otto M, Braughton KR, Whitney AR, Chen L, Mathema B, Mediavilla JR, Byrne KA, Parkins LD, Tenover FC, Kreiswirth BN, Musser JM, DeLeo FR. 2008. Epidemic community-associated methicillin-resistant Staphylococcus aureus: recent clonal expansion and diversification. Proc. Natl. Acad. Sci. U. S. A. 105:1327-1332.
60. Horsburgh MJ, Aish JL, White IJ, Shaw L, Lithgow JK, Foster SJ. 2002. sigmaB modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J. Bacteriol. 184:5457-5467.
61. O'Neill AJ. 2010. Staphylococcus aureus SH1000 and 8325-4: comparative genome sequences of key laboratory strains in staphylococcal research. Lett. Appl. Microbiol. 51:358-361.
62. Woodcock DM, Crowther PJ, Doherty J, Jefferson S, DeCruz E, Noyer-Weidner M, Smith SS, Michael MZ, Graham MW. 1989. Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucleic Acids Res. 17: 3469-3478.