The effects of modeled microgravity on growth kinetics, antibiotic susceptibility, cold growth, and the virulence potential of a yersinia pestis ymoa-deficient mutant and its isogenic parental strain

Astrobiology

Volumn 13, Issue 9, 2013, Pages 821-832

  Lawal, Abidat ^a   Kirtley, Michelle L ^b   Van Lier, Christina J ^b   Erova, Tatiana E ^b   Kozlova, Elena V ^b   Sha, Jian ^b   Chopra, Ashok K ^b   Rosenzweig, Jason A ^a  

^a TEXAS SOUTHERN UNIVERSITY   (United States)

^b University of Texas Medical Branch School of Medicine   (United States)

Author keywords

Cell culture infection models; High aspect ratio vessel; Low shear modeled microgravity; Mouse infection model; Type three secretion system (T3SS)

Indexed keywords

ANTIINFECTIVE AGENT; BACTERIAL ANTIGEN; BACTERIAL PROTEIN; LCRV PROTEIN, YERSINIA; PORE FORMING CYTOTOXIC PROTEIN;

ANIMAL; ANTIBIOTIC RESISTANCE; ARTICLE; COLD; DRUG EFFECT; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HELA CELL LINE; HUMAN; MICROBIAL SENSITIVITY TEST; MICROBIOLOGY; MOUSE; MUTATION; PATHOGENICITY; PATHOLOGY; PHENOTYPE; PLAGUE; ROTATION; SECRETION (PROCESS); VIRULENCE; WEIGHTLESSNESS; YERSINIA PESTIS;

ANIMALS; ANTI-BACTERIAL AGENTS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; COLD TEMPERATURE; DRUG RESISTANCE, MICROBIAL; FEMALE; HELA CELLS; HUMANS; MICE; MICROBIAL SENSITIVITY TESTS; MUTATION; PHENOTYPE; PLAGUE; PORE FORMING CYTOTOXIC PROTEINS; ROTATION; VIRULENCE; WEIGHTLESSNESS; YERSINIA PESTIS;

EID: 84884554092     PISSN: 15311074     EISSN: None     Source Type: Journal    
DOI: 10.1089/ast.2013.0968     Document Type: Article

References (45)

1. Allen, C.A., Niesel, D.W., and Torres, A.G. (2008) The effects of low-shear stress on adherent invasive Escherichia coli. Environ Microbiol 10:1512-1525.
2. Balsalobre, C., Juárez, A., Madrid, C., Mourin o, M., Prenafeta, A., and Mun oa, F.J. (1996) Complementation of the hha mutation in Escherichia coli by the ymoA gene from Yersinia enterocolitica: dependence on the gene dosage. Microbiology 142:1841-1846.
3. Bauer, A.W., Perry, D.M., and Kirby, W.M.M. (1959) Single disc antibiotic sensitivity testing of Staphylococci. AMA Arch Intern Med 104:208-216.
4. Bauer, A.W., Kirby, W.M.M., Sherris, J.C., and Turck, M. (1966) Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 36:493-496.
5. Beuls, E., Van Houdt, R., Leys, N., Dijkstra, C., Larkin, O., and Mahillon, J. (2009) Bacillus thuringiensis conjugation in simulated microgravity. Astrobiology 9:797-805.
6. Castro, S.L., Nelman-Gonzalez, M., Nickerson, C.A., and Ott, C.M. (2011) Induction of attachment-independent biofilm formation and repression of Hfq expression by low-fluidshear culture of Staphylococcus aureus. Appl Environ Microbiol 77:6368-6378.
7. Chopra, V., Fadl, A.A., Sha, J., Chopra, S., Galindo, C.L., and Chopra, A.K. (2006) Alterations in the virulence potential of enteric pathogens and bacterial-host cell interactions under simulated microgravity conditions. J Toxicol Environ Health A 69:1345-1370.
8. Cornelis, G.R. (2002) Yersinia type III secretion: send in the effectors. J Cell Biol 158:401-408.
9. Crabbé, A., De Boever, P., Van Houdt, R., Moors, H., Mergeay, M., and Cornelis, P. (2008) Use of the rotating wall vessel technology to study the effect of shear stress on growth behaviour of Pseudomonas aeruginosa PA01. Environ Microbiol 10:2098-2110.
10. Crabbé, A., Schurr, M.J., Monsieurs, P., Morici, L., Schurr, J., Wilson, J.W., Ott, C.M., Tsaprailis, G., Pierson, D.L., Stefanyshyn-Piper, H., and Nickerson, C.A. (2011) Transcriptional and proteomic responses of Pseudomonas aeruginosa PAO1 to spaceflight conditions involve Hfq regulation and reveal a role for oxygen. Appl Environ Microbiol 77:1221-1230.
11. Datsenko, K.A. and Wanner, B.L. (2000) One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci USA 97:6640-6645.
12. Day, J.B., Ferracci, F., and Plano, G.V. (2003) Translocation of YopE and YopN into eukaryotic cells by Yersinia pestis yopN, tyeA, sycN, yscB and lcrG deletion mutants measured using a phosphorylatable peptide tag and phosphospecific antibodies. Mol Microbiol 47:807-823.
13. Forman, S., Bobrov, A.G., Kirillina, O., Craig, S.K., Abney, J., Fetherston, J.D., and Perry, R.D. (2006) Identification of critical amino acid residues in the plague biofilm Hms proteins. Microbiology 152(Pt 11):3399-3410.
14. Goverde, R.L., Huis in't Veld, J.H., Kusters, J.G., and Mooi, F.R. (1998) The psychrotropic bacterium Yersinia enterocolitica requires expression of pnp, the gene for polynucleotide phosphorylase, for growth at low temperature (5 degrees C). Mol Microbiol 28:555-569.
15. Henry, A., Shanks, J., van Hoof, A., and Rosenzweig, J.A. (2012) The Yersinia pseudotuberculosis degradosome is required for oxidative stress, while its PNPase subunit plays a degradosome-independent role in cold growth. FEMS Microbiol Lett 336:139-147.
16. Holmström, A., Olsson, J., Cherepanov, P., Maier, E., Nordfelth, R., Pettersson, J., Benz, R., Wolf-Watz, H., and Forsberg, A. (2001) LcrV is a channel size-determining component of the Yop effector translocon of Yersinia. Mol Microbiol 39:620-632.
17. Hoson, T., Kamisaka, S., Masuda, Y., Yamashita, M., and Buchen, B. (1997) Evaluation of the three-dimensional clinostat as a simulator of weightlessness. Planta 203:S187-S197.
18. Inglesby, T.V., Dennis, D.T., Henderson, D.A., Bartlett, J.G., Ascher, M.S., Eitzen, E., Fine, A.D., Friedlander, A.M., Hauer, J., Koerner, J.F., Layton, M., McDade, J., Osterholm, M.T., O'Toole, T., Parker, G., Perl, T.M., Russell, P.K., Schoch-Spana, M., and Tonat, K. (2000) Plague as a biological weapon: medical and public health management. Working Group on Civilian Biodefense. JAMA 283:2281-2290.
19. Jackson, M.W., Silva-Herzog, E., and Plano, G.V. (2004) The ATP-dependent ClpXP and Lon proteases regulate expression of the Yersinia pestis type III secretion system via regulated proteolysis of YmoA, a small histone-like protein. Mol Microbiol 54:1364-1378.
20. Klaus, D.M. and Howard, H.N. (2006) Antibiotic efficacy and microbial virulence during space flight. Trends Biotechnol 24:131-136.
21. Kutyrev, V.V., Eroshenko, G.A., Popov, N.V., Vidiaeva, N.A., and Konnov, N.P (2009) Molecular mechanisms of interactions of plague causative agents with invertebrates. Molecular Genetics, Microbiology and Virology 24:169-176.
22. Lawal, A., Jejelowo, O.A., and Rosenzweig, J.A. (2010) The effects of low-shear mechanical stress on Yersinia pestis virulence. Astrobiology 10:881-888.
23. Lillard, J.W., Jr., Fetherston, J.D., Pedersen, L., Pendrak, M.L., and Perry, R.D. (1997) Sequence and genetic analysis of the hemin storage (hms) system of Yersinia pestis. Gene 193:13-21.
24. Lindler, L.E., Klempner, M.S., and Straley, S.C. (1990) Yersinia pestis pH 6 antigen: genetic, biochemical, and virulence characterization of a protein involved in the pathogenesis of bubonic plague. Infect Immun 58:2569-2577.
25. Liu, T., Agar, S.L., Sha, J., and Chopra, A.K. (2010) Deletion of Braun lipoprotein gene (lpp) attenuates Yersinia pestis KIM/ D27 strain: role of Lpp in modulating host immune response, NF-kappaB activation and cell death. Microb Pathog 48:42-52.
26. Lynch, S.V., Mukundakrishnan, K., Benoit, M.R., Ayyaswamy, P.S., and Matin, A. (2006) Escherichia coli biofilms formed under low-shear modeled microgravity in a ground-based system. Appl Environ Microbiol 72:7701-7710.
27. McLean, R.J., Cassanto, J.M., Barnes, M.B., and Koo, J.H. (2001) Bacterial biofilm formation under microgravity conditions. FEMS Microbiol Lett 195:115-119.
28. Neuhaus, K., Rapposch, S., Francis, K.P., and Scherer, S. (2000) Restart of exponential growth of cold-shocked Yersinia enterocolitica occurs after down-regulation of cspA1/A2 mRNA. J Bacteriol 182:3285-3288.
29. Nickerson, C.A., Ott, C.M., Mister, S.J., Morrow, B.J., Burns-Keliher, L., and Pierson, D.L. (2000) Microgravity as a novel environmental signal affecting Salmonella enteric serovar Typhimurium virulence. Infect Immun 68:3147-3152.
30. Nickerson, C.A., Ott, C.M., Wilson, J.W., Ramamurthy, R., LeBlanc, C.L., Honer zu Bentrup, K., Hammond, T., and Pierson, D.L. (2003) Low-shear modeled microgravity: a global environmental regulatory signal affecting bacterial gene expression, physiology, and pathogenesis. J Microbiol Methods 54:1-11.
31. Nickerson, C.A., Ott, C.M., Wilson, J.W., Ramamurthy, R., and Pierson, D.L. (2004) Microbial responses to microgravity and other low-shear environments. Microbiol Mol Biol Rev 68:345-361.
32. Pujol, C. and Bliska, J.B. (2005) Turning Yersinia pathogenesis outside in: subversion of macrophage function by intracellular yersiniae. Clin Immunol 114:216-226.
33. Rosenzweig, J.A., Weltman, G., Plano, G.V., and Schesser, K. (2005) Modulation of Yersinia type three secretion system by the S1 domain of polynucleotide phosphorylase. J Biol Chem 280:156-163.
34. Rosenzweig, J.A., Chromy, B., Echeverry, A., Yang, J., Adkins, B., Plano, G.V., McCutchen-Maloney, S., and Schesser, K. (2007) Polynucleotide phosphorylase independently controls virulence factor expression levels and export in Yersinia spp. FEMS Microbiol Lett 270:255-264.
35. Rosenzweig, J.A., Abogunde, O., Thomas, K., Lawal, A., Nguyen, Y.U., Sodipe, A., and Jejelowo, O. (2010) Spaceflight and modeled microgravity effects on microbial growth and virulence. Appl Microbiol Biotechnol 85:885-891.
36. Rosenzweig, J.A., Brackman, S.M., Kirtley, M.L., Sha, J., Erova, T.E., Yeager, L.A., Peterson, J.W., Xu, Z.Q., and Chopra, A.K. (2011) Cethromycin-mediated protection against the plague pathogen Yersinia pestis in a rat model of infection and comparison with levofloxacin. Antimicrob Agents Chemother 55:5034-5042.
37. Searless, S.C., Woolley, C.M., Peterson, R.A., Hyman, L.E., and Nielsen-Preiss, S.M. (2011) Modeled microgravity increases filamentation, biofilm formation, phenotypic switching, and antimicrobial resistance in Candida albicans. Astrobiology 11:825-836.
38. Sha, J., Agar, S.L., Baze, W.B., Olano, J.P., Fadl, A.A., Erova, T.E., Wang, S., Foltz, S.M., Suarez, G., Motin, V.L., Chauhan, S., Klimpel, G.R., Peterson, J.W., and Chopra, A.K. (2008) Braun lipoprotein (Lpp) contributes to virulence of yersiniae: potential role of Lpp in inducing bubonic and pneumonic plague. Infect Immun 76:1390-1409.
39. Sun, Y.C., Guo, X.P., Hinnebusch, B.J., and Darby, C. (2012) The Yersinia pestis Rcs phosphorelay inhibits biofilm formation by repressing transcription of the diguanylate cyclase gene hmsT. J Bacteriol 194:2020-2026.
40. Viboud, G.I. and Bliska, J.B. (2005) Yersinia outer proteins: role in the modulation of host cell signaling responses and pathogenesis. Annu Rev Microbiol 59:69-89.
41. Wilson, J.W., Ott, C.M., Ramamurthy, R., Porwollik, S., McClelland, M., Pierson, D.L., and Nickerson, C.A. (2002a) Low-shear modeled microgravity alters the Salmonella enteric serovar Typhimurium stress response in an RpoS-independent manner. Appl Environ Microbiol 68:5408-5416.
42. Wilson, J.W., Ramamurthy, R., Porwollik, S., McClelland, M., Hammond, T., Allen, P., Ott, C.M., Pierson, D.L., and Nickerson, C.A. (2002b) Microarray analysis identifies Salmonella genes belonging to the low-shear modeled microgravity regulon. Proc Natl Acad Sci USA 99:13807-13812.
43. Wilson, J.W., Ott, C.M., Höner zu Bentrup, K., Ramamurthy, R., Quick, L., Porwollik, S., Cheng, P., McClelland, M., Tsaprailis, G., Radabaugh, T., Hunt, A., Fernandez, D., Richter, E., Shah, M., Kilcoyne, M., Joshi, L., Nelman-Gonzalez, M., Hing, S., Parra, M., Dumars, P., Norwood, K., Bober, R., Devich, J., Ruggles, A., Goulart, C., Rupert, M., Stodieck, L., Stafford, P., Catella, L., Schurr, M.J., Buchanan, K., Morici, L., McCracken, J., Allen, P., Baker-Coleman, C., Hammond, T., Vogel, J., Nelson, R., Pierson, D.L., Stefanyshyn-Piper, H.M., and Nickerson, C.A. (2007) Space flight alters bacterial gene expression and virulence and reveals a role for global regulator Hfq. Proc Natl Acad Sci USA 104:16299-16304.
44. Wilson, J.W., Ott, C.M., Quick, L., Davis, R., Höner zu Bentrup, K., Crabbé, A., Richter, E., Sarker, S., Barrila, J., Porwollik, S., Cheng, P., McClelland, M., Tsaprailis, G., Radabaugh, T., Hunt, A., Shah, M., Nelman-Gonzalez, M., Hing, S., Parra, M., Dumars, P., Norwood, K., Bober, R., Devich, J., Ruggles, A., CdeBaca, A., Narayan, S., Benjamin, J., Goulart, C., Rupert, M., Catella, L., Schurr, M.J., Buchanan, K., Morici, L., McCracken, J., Porter, M.D., Pierson, D.L., Smith, S.M., Mergeay, M., Leys, N., Stefanyshyn-Piper, H.M., Gorie, D., and Nickerson, C.A. (2008) Media ion composition controls regulatory and virulence response of Salmonella in spaceflight. PLoS One 3:e3923.
45. Zhou, D. and Yang, R. (2011) Formation and regulation of Yersinia biofilms. Protein Cell 2:173-179.