The PAMP c-di-AMP Is Essential for Listeria monocytogenes Growth in Rich but Not Minimal Media due to a Toxic Increase in (p)ppGpp

Cell Host and Microbe

Volumn 17, Issue 6, 2015, Pages 788-798

  Whiteley, Aaron T ^a   Pollock, Alex J ^a   Portnoy, Daniel A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE PHOSPHATE; BACTERIAL PROTEIN; CYCLIC DI ADENOSINE MONOPHOSPHATE; DIADENYLATE CYCLASE; GUANOSINE 3' DIPHOSPHATE 5' TRIPHOSPHATE; SYNTHETASE; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; ADENYLATE CYCLASE; CULTURE MEDIUM; CYCLIC DIADENOSINE PHOSPHATE; DINUCLEOSIDE PHOSPHATE;

ARTICLE; BACTERIAL GROWTH; BACTERIUM MUTANT; CONTROLLED STUDY; GENE MUTATION; GENETIC ANALYSIS; HOST CELL; LISTERIA MONOCYTOGENES; MACROPHAGE CULTURE; NONHUMAN; PRIORITY JOURNAL; WILD TYPE; ANIMAL; CHEMISTRY; CULTURE MEDIUM; FEMALE; GENE EXPRESSION REGULATION; GENE REPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; INBRED MOUSE STRAIN; METABOLISM; PATHOGENICITY;

ADENYLYL CYCLASES; ANIMALS; BACTERIAL PROTEINS; CULTURE MEDIA; DINUCLEOSIDE PHOSPHATES; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; GUANOSINE PENTAPHOSPHATE; LISTERIA MONOCYTOGENES; MICE, INBRED STRAINS; SUPPRESSION, GENETIC;

EID: 84930031805     PISSN: 19313128     EISSN: 19346069     Source Type: Journal    
DOI: 10.1016/j.chom.2015.05.006     Document Type: Article

References (61)

1. Abranches, J., Martinez, A.R., Kajfasz, J.K., Chávez, V., Garsin, D.A., Lemos, J.A., The molecular alarmone (p)ppGpp mediates stress responses, vancomycin tolerance, and virulence in Enterococcus faecalis. J. Bacteriol. 191 (2009), 2248–2256.
2. Archer, K.A., Durack, J., Portnoy, D.A., STING-dependent type I IFN production inhibits cell-mediated immunity to Listeria monocytogenes. PLoS Pathog., 10, 2014, e1003861.
3. Barker, J.R., Koestler, B.J., Carpenter, V.K., Burdette, D.L., Waters, C.M., Vance, R.E., Valdivia, R.H., STING-Dependent Recognition of Cyclic di-AMP Mediates Type I Interferon Responses during Chlamydia trachomatis Infection. MBio., 4, 2013, 10.1128/mBio.00018-13.
4. Bennett, H.J., Pearce, D.M., Glenn, S., Taylor, C.M., Kuhn, M., Sonenshein, A.L., Andrew, P.W., Roberts, I.S., Characterization of relA and codY mutants of Listeria monocytogenes: identification of the CodY regulon and its role in virulence. Mol. Microbiol. 63 (2007), 1453–1467.
5. Borezee, E., Pellegrini, E., Berche, P., OppA of Listeria monocytogenes, an oligopeptide-binding protein required for bacterial growth at low temperature and involved in intracellular survival. Infect. Immun. 68 (2000), 7069–7077.
6. Brinsmade, S.R., Alexander, E.L., Livny, J., Stettner, A.I., Segrè, D., Rhee, K.Y., Sonenshein, A.L., Hierarchical expression of genes controlled by the Bacillus subtilis global regulatory protein CodY. Proc. Natl. Acad. Sci. USA 111 (2014), 8227–8232.
7. Chico-Calero, I., Suárez, M., González-Zorn, B., Scortti, M., Slaghuis, J., Goebel, W., Vázquez-Boland, J.A., European Listeria Genome Consortium. Hpt, a bacterial homolog of the microsomal glucose- 6-phosphate translocase, mediates rapid intracellular proliferation in Listeria. Proc. Natl. Acad. Sci. USA 99 (2002), 431–436.
8. Corrigan, R.M., Gründling, A., Cyclic di-AMP: another second messenger enters the fray. Nat. Rev. Microbiol. 11 (2013), 513–524.
9. Corrigan, R.M., Abbott, J.C., Burhenne, H., Kaever, V., Gründling, A., c-di-AMP is a new second messenger in Staphylococcus aureus with a role in controlling cell size and envelope stress. PLoS Pathog., 7, 2011, e1002217.
10. Corrigan, R.M., Campeotto, I., Jeganathan, T., Roelofs, K.G., Lee, V.T., Gründling, A., Systematic identification of conserved bacterial c-di-AMP receptor proteins. Proc. Natl. Acad. Sci. USA 110 (2013), 9084–9089.
11. Corrigan, R.M., Bowman, L., Willis, A.R., Kaever, V., Gründling, A., Cross-talk between two nucleotide-signaling pathways in Staphylococcus aureus. J. Biol. Chem. 290 (2015), 5826–5839.
12. Cossart, P., Illuminating the landscape of host-pathogen interactions with the bacterium Listeria monocytogenes. Proc. Natl. Acad. Sci. USA 108 (2011), 19484–19491.
13. Crimmins, G.T., Herskovits, A.A., Rehder, K., Sivick, K.E., Lauer, P., Dubensky, T.W. Jr., Portnoy, D.A., Listeria monocytogenes multidrug resistance transporters activate a cytosolic surveillance pathway of innate immunity. Proc. Natl. Acad. Sci. USA 105 (2008), 10191–10196.
14. Dalebroux, Z.D., Swanson, M.S., ppGpp: magic beyond RNA polymerase. Nat. Rev. Microbiol. 10 (2012), 203–212.
15. Danilchanka, O., Mekalanos, J.J., Cyclic dinucleotides and the innate immune response. Cell 154 (2013), 962–970.
16. De Las Peñas, A., Connolly, L., Gross, C.A., SigmaE is an essential sigma factor in Escherichia coli. J. Bacteriol. 179 (1997), 6862–6864.
17. Epstein, W., The roles and regulation of potassium in bacteria. Prog. Nucleic Acid Res. Mol. Biol. 75 (2003), 293–320.
18. Freitag, N.E., Port, G.C., Miner, M.D., Listeria monocytogenes - from saprophyte to intracellular pathogen. Nat. Rev. Microbiol. 7 (2009), 623–628.
19. Geiger, T., Wolz, C., Intersection of the stringent response and the CodY regulon in low GC Gram-positive bacteria. Int. J. Med. Microbiol. 304 (2014), 150–155.
20. Geiger, T., Kästle, B., Gratani, F.L., Goerke, C., Wolz, C., Two small (p)ppGpp synthases in Staphylococcus aureus mediate tolerance against cell envelope stress conditions. J. Bacteriol. 196 (2014), 894–902.
21. Hogg, T., Mechold, U., Malke, H., Cashel, M., Hilgenfeld, R., Conformational antagonism between opposing active sites in a bifunctional RelA/SpoT homolog modulates (p)ppGpp metabolism during the stringent response. Cell 117 (2004), 57–68.
22. Huynh, T.N., Luo, S., Pensinger, D., Sauer, J.-D., Tong, L., Woodward, J.J., An HD-domain phosphodiesterase mediates cooperative hydrolysis of c-di-AMP to affect bacterial growth and virulence. Proc. Natl. Acad. Sci. USA 112 (2015), E747–E756.
23. Joseph, B., Goebel, W., Life of Listeria monocytogenes in the host cells’ cytosol. Microbes Infect. 9 (2007), 1188–1195.
24. Jutras, B.L., Chenail, A.M., Rowland, C.L., Carroll, D., Miller, M.C., Bykowski, T., Stevenson, B., Eubacterial SpoVG homologs constitute a new family of site-specific DNA-binding proteins. PLoS ONE, 8, 2013, e66683.
25. Kaplan Zeevi, M., Shafir, N.S., Shaham, S., Friedman, S., Sigal, N., Nir Paz, R., Boneca, I.G., Herskovits, A.A., Listeria monocytogenes multidrug resistance transporters and cyclic di-AMP, which contribute to type I interferon induction, play a role in cell wall stress. J. Bacteriol. 195 (2013), 5250–5261.
26. Kriel, A., Bittner, A.N., Kim, S.H., Liu, K., Tehranchi, A.K., Zou, W.Y., Rendon, S., Chen, R., Tu, B.P., Wang, J.D., Direct regulation of GTP homeostasis by (p)ppGpp: a critical component of viability and stress resistance. Mol. Cell 48 (2012), 231–241.
27. Kriel, A., Brinsmade, S.R., Tse, J.L., Tehranchi, A.K., Bittner, A.N., Sonenshein, A.L., Wang, J.D., GTP dysregulation in Bacillus subtilis cells lacking (p)ppGpp results in phenotypic amino acid auxotrophy and failure to adapt to nutrient downshift and regulate biosynthesis genes. J. Bacteriol. 196 (2014), 189–201.
28. Lemos, J.A., Lin, V.K., Nascimento, M.M., Abranches, J., Burne, R.A., Three gene products govern (p)ppGpp production by Streptococcus mutans. Mol. Microbiol. 65 (2007), 1568–1581.
29. Liu, S., Bayles, D.O., Mason, T.M., Wilkinson, B.J., A cold-sensitive Listeria monocytogenes mutant has a transposon insertion in a gene encoding a putative membrane protein and shows altered (p)ppGpp levels. Appl. Environ. Microbiol. 72 (2006), 3955–3959.
30. Lobel, L., Sigal, N., Borovok, I., Ruppin, E., Herskovits, A.A., Integrative genomic analysis identifies isoleucine and CodY as regulators of Listeria monocytogenes virulence. PLoS Genet., 8, 2012, e1002887.
31. Lobel, L., Sigal, N., Borovok, I., Belitsky, B.R., Sonenshein, A.L., Herskovits, A.A., The metabolic regulator CodY links Listeria monocytogenes metabolism to virulence by directly activating the virulence regulatory gene prfA. Mol. Microbiol. 95 (2014), 624–644.
32. Luo, Y., Helmann, J.D., Analysis of the role of Bacillus subtilis σ(M) in β-lactam resistance reveals an essential role for c-di-AMP in peptidoglycan homeostasis. Mol. Microbiol. 83 (2012), 623–639.
33. Matsuno, K., Sonenshein, A.L., Role of SpoVG in asymmetric septation in Bacillus subtilis. J. Bacteriol. 181 (1999), 3392–3401.
34. McLaggan, D., Logan, T.M., Lynn, D.G., Epstein, W., Involvement of gamma-glutamyl peptides in osmoadaptation of Escherichia coli. J. Bacteriol. 172 (1990), 3631–3636.
35. McLaggan, D., Naprstek, J., Buurman, E.T., Epstein, W., Interdependence of K+ and glutamate accumulation during osmotic adaptation of Escherichia coli. J. Biol. Chem. 269 (1994), 1911–1917.
36. Mechold, U., Cashel, M., Steiner, K., Gentry, D., Malke, H., Functional analysis of a relA/spoT gene homolog from Streptococcus equisimilis. J. Bacteriol. 178 (1996), 1401–1411.
37. Mehne, F.M.P., Gunka, K., Eilers, H., Herzberg, C., Kaever, V., Stülke, J., Cyclic di-AMP homeostasis in Bacillus subtilis: both lack and high-level accumulation of the nucleotide are detrimental for cell growth. J. Biol. Chem. 288 (2013), 2004–2017.
38. Meier, S., Goerke, C., Wolz, C., Seidl, K., Homerova, D., Schulthess, B., Kormanec, J., Berger-Bächi, B., Bischoff, M., sigmaB and the sigmaB-dependent arlRS and yabJ-spoVG loci affect capsule formation in Staphylococcus aureus. Infect. Immun. 75 (2007), 4562–4571.
39. Nanamiya, H., Kasai, K., Nozawa, A., Yun, C.-S., Narisawa, T., Murakami, K., Natori, Y., Kawamura, F., Tozawa, Y., Identification and functional analysis of novel (p)ppGpp synthetase genes in Bacillus subtilis. Mol. Microbiol. 67 (2008), 291–304.
40. Nelson, J.W., Sudarsan, N., Furukawa, K., Weinberg, Z., Wang, J.X., Breaker, R.R., Riboswitches in eubacteria sense the second messenger c-di-AMP. Nat. Chem. Biol. 9 (2013), 834–839.
41. O'Riordan, M., Yi, C.H., Gonzales, R., Lee, K.-D., Portnoy, D.A., Innate recognition of bacteria by a macrophage cytosolic surveillance pathway. Proc. Natl. Acad. Sci. USA 99 (2002), 13861–13866.
42. Phan-Thanh, L., Gormon, T., A chemically defined minimal medium for the optimal culture of Listeria. Int. J. Food Microbiol. 35 (1997), 91–95.
43. Rallu, F., Gruss, A., Ehrlich, S.D., Maguin, E., Acid- and multistress-resistant mutants of Lactococcus lactis : identification of intracellular stress signals. Mol. Microbiol. 35 (2000), 517–528.
44. Rao, F., See, R.Y., Zhang, D., Toh, D.C., Ji, Q., Liang, Z.-X., YybT is a signaling protein that contains a cyclic dinucleotide phosphodiesterase domain and a GGDEF domain with ATPase activity. J. Biol. Chem. 285 (2010), 473–482.
45. Reniere, M.L., Whiteley, A.T., Hamilton, K.L., John, S.M., Lauer, P., Brennan, R.G., Portnoy, D.A., Glutathione activates virulence gene expression of an intracellular pathogen. Nature 517 (2015), 170–173.
46. Schär, J., Stoll, R., Schauer, K., Loeffler, D.I.M., Eylert, E., Joseph, B., Eisenreich, W., Fuchs, T.M., Goebel, W., Pyruvate carboxylase plays a crucial role in carbon metabolism of extra- and intracellularly replicating Listeria monocytogenes. J. Bacteriol. 192 (2010), 1774–1784.
47. Shetron-Rama, L.M., Marquis, H., Bouwer, H.G.A., Freitag, N.E., Intracellular induction of Listeria monocytogenes actA expression. Infect. Immun. 70 (2002), 1087–1096.
48. Somerville, G.A., Proctor, R.A., At the crossroads of bacterial metabolism and virulence factor synthesis in Staphylococci. Microbiol. Mol. Biol. Rev. 73 (2009), 233–248.
49. Sonenshein, A.L., Control of key metabolic intersections in Bacillus subtilis. Nat. Rev. Microbiol. 5 (2007), 917–927.
50. Sun, A.N., Camilli, A., Portnoy, D.A., Isolation of Listeria monocytogenes small-plaque mutants defective for intracellular growth and cell-to-cell spread. Infect. Immun. 58 (1990), 3770–3778.
51. Sureka, K., Choi, P.H., Precit, M., Delince, M., Pensinger, D.A., Huynh, T.N., Jurado, A.R., Goo, Y.A., Sadilek, M., Iavarone, A.T., et al. The cyclic dinucleotide c-di-AMP is an allosteric regulator of metabolic enzyme function. Cell 158 (2014), 1389–1401.
52. Tadmor, K., Pozniak, Y., Burg Golani, T., Lobel, L., Brenner, M., Sigal, N., Herskovits, A.A., Listeria monocytogenes MDR transporters are involved in LTA synthesis and triggering of innate immunity during infection. Front. Cell Infect. Microbiol., 4, 2014, 16.
53. Tagami, K., Nanamiya, H., Kazo, Y., Maehashi, M., Suzuki, S., Namba, E., Hoshiya, M., Hanai, R., Tozawa, Y., Morimoto, T., et al. Expression of a small (p)ppGpp synthetase, YwaC, in the (p)ppGpp(0) mutant of Bacillus subtilis triggers YvyD-dependent dimerization of ribosome. Microbiologyopen 1 (2012), 115–134.
54. Taylor, C.M., Beresford, M., Epton, H.A.S., Sigee, D.C., Shama, G., Andrew, P.W., Roberts, I.S., Listeria monocytogenes relA and hpt mutants are impaired in surface-attached growth and virulence. J. Bacteriol. 184 (2002), 621–628.
55. Tsai, H.-N., Hodgson, D.A., Development of a synthetic minimal medium for Listeria monocytogenes. Appl. Environ. Microbiol. 69 (2003), 6943–6945.
56. Vance, R.E., Isberg, R.R., Portnoy, D.A., Patterns of pathogenesis: discrimination of pathogenic and nonpathogenic microbes by the innate immune system. Cell Host Microbe 6 (2009), 10–21.
57. Wang, J.D., Sanders, G.M., Grossman, A.D., Nutritional control of elongation of DNA replication by (p)ppGpp. Cell 128 (2007), 865–875.
58. Witte, G., Hartung, S., Büttner, K., Hopfner, K.-P., Structural biochemistry of a bacterial checkpoint protein reveals diadenylate cyclase activity regulated by DNA recombination intermediates. Mol. Cell 30 (2008), 167–178.
59. Witte, C.E., Whiteley, A.T., Burke, T.P., Sauer, J.-D., Portnoy, D.A., Woodward, J.J., Cyclic di-AMP is critical for Listeria monocytogenes growth, cell wall homeostasis, and establishment of infection. MBio, 4, 2013 e00282–e13.
60. Woodward, J.J., Iavarone, A.T., Portnoy, D.A., c-di-AMP secreted by intracellular Listeria monocytogenes activates a host type I interferon response. Science 328 (2010), 1703–1705.
61. Yang, J., Bai, Y., Zhang, Y., Gabrielle, V.D., Jin, L., Bai, G., Deletion of the cyclic di-AMP phosphodiesterase gene (cnpB) in Mycobacterium tuberculosis leads to reduced virulence in a mouse model of infection. Mol. Microbiol. 93 (2014), 65–79.