Thermoregulation of prodigiosin biosynthesis by Serratia marcescens is controlled at the transcriptional level and requires HexS

• Autorzy: Romanowski E.G. , Lehner K.M. , Martin E.C. , Patel K.R. , Callaghan J.D. , Stella N.A. , Shanks N.M.Q.
• Języki publikacji: EN

Abstrakty

EN

Several biotypes of the Gram-negative bacterium Serratia marcescens produce the tri-pyrole pigment and secondary metabolite prodigiosin. The biological activities of this pigment have therapeutic potential. For over half a century it has been known that biosynthesis of prodi giosin is inhibited when bacteria are grown at elevated temperatures, yet the fundamental mechanism underlying this thermoregulation has not been characterized. In this study, chromosomal and plasmid-borne luxCDABE transcriptional reporters revealed reduced transcription of the prodigiosin biosynthetic operon at 37°C compared to 30°C indicating transcriptional control of pigment production. Moreover, induced expression of the prodigiosin biosynthetic operon at 37°C was able to produce pigmented colonies and cultures demonstrating that physiological conditions at 37°C allow prodigiosin production and indicating that post-transcriptional control is not a major con-tributor to the thermoregulation of prodigiosin pigmentation. Genetic experiments support the model that the HexS transcription factor is a key contributor to thermoregulation of pigmentation, whereas CRP plays a minor role, and a clear role for EepR and PigP was not observed. Together, these data indicate that thermoregulation of prodigiosin production at elevated temperatures is controlled largely, if not exclusively, at the transcriptional level.

• Wydawca: -
• Czasopismo: Polish Journal of Microbiology
• Rocznik: 2019
• Tom: 68
• Numer: 1
• Opis fizyczny: p.43-50,fig.,ref.

Twórcy

autor

Romanowski E.G.

• Charles T. Campbell Laboratory of Ophthalmic Microbiology, Department of Ophthalmology, University of Pittsburgh, Pittsburgh PA, USA

autor

Lehner K.M.

• Charles T. Campbell Laboratory of Ophthalmic Microbiology, Department of Ophthalmology, University of Pittsburgh, Pittsburgh PA, USA

autor

Martin E.C.

• Charles T. Campbell Laboratory of Ophthalmic Microbiology, Department of Ophthalmology, University of Pittsburgh, Pittsburgh PA, USA

autor

Patel K.R.

• Charles T. Campbell Laboratory of Ophthalmic Microbiology, Department of Ophthalmology, University of Pittsburgh, Pittsburgh PA, USA

autor

Callaghan J.D.

• Charles T. Campbell Laboratory of Ophthalmic Microbiology, Department of Ophthalmology, University of Pittsburgh, Pittsburgh PA, USA

autor

Stella N.A.

• Charles T. Campbell Laboratory of Ophthalmic Microbiology, Department of Ophthalmology, University of Pittsburgh, Pittsburgh PA, USA

autor

Shanks N.M.Q.

• Charles T. Campbell Laboratory of Ophthalmic Microbiology, Department of Ophthalmology, University of Pittsburgh, Pittsburgh PA, USA

Bibliografia

• Barriuso J, Hogan DA, Keshavarz T, Martínez MJ. Role of quo-rum sensing and chemical communication in fungal biotechno-logy and pathogenesis. FEMS Microbiol Rev. 2018;42(5):627–638. doi:10.1093/femsre/fuy022 Medline
• Benedetti IM, de Lorenzo V, Silva-Rocha R. Quantitative, non-disruptive monitoring of transcription in single cells with a broad-host range GFP-luxCDABE dual reporter system. PLoS One. 2012;7(12):e52000. doi:10.1371/journal.pone.0052000 Medline
• Bertani G. Studies on lysogenesis. I. The mode of phage libera-tion by lysogenic Escherichia coli. J Bacteriol. 1951;62(3):293–300. Medline
• Blizzard JL, Peterson GE. Selective inhibition of proline-induced pigmentation in washed cells of Serratia marcescens. J Bacteriol. 1963;85:1136–1140. Medline
• Cheng MF, Lin CS, Chen YH, Sung PJ, Lin SR, Tong YW, Weng CF. Inhibitory growth of oral squamous cell carcinoma cancer via bacterial prodigiosin. Mar Drugs. 2017;15(7):224.doi:10.3390/md15070224 Medline
• Chiang SL, Rubin EJ. Construction of a mariner-based transpo-son for epitope-tagging and genomic targeting. Gene. 2002;296(1–2):179–185.doi:10.1016/S0378-1119(02)00856-9 Medline
• Choi SY, Im H, Mitchell RJ. Violacein and bacterial predation: promising alternatives for priority multidrug resistant human patho-gens. Future Microbiol. 2017;12(10):835–838.doi:10.2217/fmb-2017-0090 Medline
• Choudhary E, Bishai W, Agarwal N. Expression of a subset of heat stress induced genes of Mycobacterium tuberculosis is regulated by 3’,5’-cyclic AMP. PLoS One. 2014;9(2):e89759.doi:10.1371/journal.pone.0089759 Medline
• Danevčič T, Borić Vezjak M, Tabor M, Zorec M, Stopar D. Prodigiosin induces autolysins in actively grown Bacillus subtilis cells. Front Microbiol. 2016a;7:27. doi:10.3389/fmicb.2016.00027 Medline
• Danevčič T, Borić Vezjak M, Zorec M, Stopar D. Prodigiosin– A multifaceted Escherichia coli antimicrobial agent. PLoS One. 2016b;11(9):e0162412. doi:10.1371/journal.pone.0162412 Medline
• Daniels R, Vanderleyden J, Michiels J. Quorum sensing and swarm-ing migration in bacteria. FEMS Microbiol Rev. 2004;28(3):261–289. doi:10.1016/j.femsre.2003.09.004 Medline
• Demain AL, Fang A. The natural functions of secondary metabo-lites. Adv Biochem Eng Biotechnol. 2000;69:1–39.doi:10.1007/3-540-44964-7_1 Medline
• Fender JE, Bender CM, Stella NA, Lahr RM, Kalivoda EJ, Shanks RMQ.Serratia marcescens quinoprotein glucose dehy-drogenase activity mediates medium acidification and inhibition of prodigiosin production by glucose. Appl Environ Microbiol. 2012;78(17):6225–6235. doi:10.1128/AEM.01778-12 Medline
• Fineran PC, Slater H, Everson L, Hughes K, Salmond GPC. Bio-synthesis of tripyrrole and β-lactam secondary metabolites in Ser-ratia : integration of quorum sensing with multiple new regulatory components in the control of prodigiosin and carbapenem antibiotic production. Mol Microbiol. 2005;56(6):1495–1517.doi:10.1111/j.1365-2958.2005.04660.x Medline
• Haddix PL, Jones S, Patel P, Burnham S, Knights K, Powell JN, LaForm A. Kinetic analysis of growth rate, ATP, and pigmenta-tion suggests an energy-spilling function for the pigment prodigi-osin of Serratia marcescens. J Bacteriol. 2008;190(22):7453–7463. doi:10.1128/JB.00909-08 Medline
• Haddix PL, Shanks RMQ. Prodigiosin pigment of Serratia marces-cens is associated with increased biomass production. Arch Micro-biol. 2018;200(7):989–999. doi:10.1007/s00203-018-1508-0 Medline
• Hage-Hülsmann J, Grünberger A, Thies S, Santiago-Schübel B, Klein AS, Pietruszka J, Binder D, Hilgers F, Domröse A, Drep-per T, et al. Natural biocide cocktails: combinatorial antibiotic effects of prodigiosin and biosurfactants. PLoS One. 2018;13(7):e0200940. doi:10.1371/journal.pone.0200940 Medline
• Heinemann B, Howard AJ, Palocz HJ. Influence of dissolved oxygen levels on production of L-asparaginase and prodigiosin by Serratia marcescens. Appl Microbiol. 1970;19(5):800–804. Medline
• Hidalgo-Romano B, Gollihar J, Brown SA, Whiteley M, Valen-zuela E Jr, Kaplan HB, Wood TK, McLean RJC. Indole inhibi-tion of N-acylated homoserine lactone-mediated quorum sig-nalling is widespread in Gram-negative bacteria. Microbiology. 2014;160(Pt_11):2464–2473. doi:10.1099/mic.0.081729-0 Medline
• Hoefler BC, Stubbendieck RM, Josyula NK, Moisan SM, Schulze EM, Straight PD. A Link between linearmycin biosynthe-sis and extracellular vesicle genesis connects specialized metabo-lism and bacterial membrane physiology. Cell Chem Biol. 2017;24:1238–1249.e7. doi:10.1016/j.chembiol.2017.08.008 Medline
• Horng YT, Chang KC, Liu YN, Lai HC, Soo PC. The RssB/RssA two-component system regulates biosynthesis of the tripyrrole antibiotic, prodigiosin, in Serratia marcescens. Int J Med Microbiol. 2010;300(5):304–312.doi:10.1016/j.ijmm.2010.01.003 Medline
• Im H, Choi SY, Son S, Mitchell RJ. Combined application of bacte-rial predation and violacein to kill polymicrobial pathogenic com-munities. Sci Rep. 2017;7(1):14415.doi:10.1038/s41598-017-14567-7 Medline
• Kadouri DE, Shanks RMQ. Identification of a methicillin-resistant Staphylococcus aureus inhibitory compound isolated from Serratia marcescens. Res Microbiol. 2013;164(8):821–826.doi:10.1016/j.resmic.2013.06.002 Medline
• Kalivoda EJ, Stella NA, Aston MA, Fender JE, Thompson PP, Kowalski RP, Shanks RMQ. Cyclic AMP negatively regulates prodigiosin production by Serratia marcescens. Res Microbiol. 2010;161(2):158–167. doi:10.1016/j.resmic.2009.12.004 Medline
• Khan A, Singh P, Srivastava A. Synthesis, nature and utility of universal iron chelator – Siderophore: A review. Microbiol Res. 2018;212-213:103–111. doi:10.1016/j.micres.2017.10.012 Medline
• Klein AS, Brass HUC, Klebl DP, Classen T, Loeschcke A, Drepper T, Sievers S, Jaeger KE, Pietruszka J. Preparation of cyclic prodigi-nines by mutasynthesis in Pseudomonas putida KT2440. Chembio-chem. 2018;19:1445–1552. Medline
• Klein AS, Domröse A, Bongen P, Brass HUC, Classen T,Loeschcke A, Drepper T, Laraia L, Sievers S, Jaeger KE, et al. New prodigiosin derivatives obtained by mutasynthesis in Pseudomonas putida. ACS Synth Biol. 2017;6(9):1757–1765.doi:10.1021/acssynbio.7b00099 Medline
• Lin SR, Fu YS, Tsai MJ, Cheng H, Weng CF. Natural compounds from herbs that can potentially execute as autophagy inducers for cancer therapy. Int J Mol Sci. 2017;18(7):1412.doi:10.3390/ijms18071412 Medline
• Nagai H, Yano R, Erickson JW, Yura T. Transcriptional regulationof the heat shock regulatory gene rpoH in Escherichia coli: invol -ve ment of a novel catabolite-sensitive promoter. J Bacteriol. 1990; 172(5):2710–2715. doi:10.1128/jb.172.5.2710-2715.1990 Medline
• Pérez-Tomás R, Montaner B, Llagostera E, Soto-Cerrato V. The prodigiosins, proapoptotic drugs with anticancer properties. Bio-chem Pharmacol. 2003;66(8):1447–1452.doi:10.1016/S0006-2952(03)00496-9 Medline
• Pérez-Tomás R, Viñas M. New insights on the antitumoral prop-erties of prodiginines. Curr Med Chem. 2010;17(21):2222–2231. doi:10.2174/092986710791331103 Medline
• Shanks RMQ, Caiazza NC, Hinsa SM, Toutain CM, O’Toole GA.Saccharomyces cerevisiae-based molecular tool kit for manipulation of genes from gram-negative bacteria. Appl Environ Microbiol. 2006;72(7):5027–5036.doi:10.1128/AEM.00682-06 Medline
• Shanks RMQ, Kadouri DE, MacEachran DP, O’Toole GA. New yeast recombineering tools for bacteria. Plasmid. 2009;62(2):88–97.doi:10.1016/j.plasmid.2009.05.002 Medline
• Shanks RMQ, Lahr RM, Stella NA, Arena KE, Brothers KM,Kwak DH, Liu X, Kalivoda EJ. A Serratia marcescens PigP homo-log controls prodigiosin biosynthesis, swarming motility and hemolysis and is regulated by cAMP-CRP and HexS. PLoS One. 2013;8(3):e57634. doi:10.1371/journal.pone.0057634 Medline
• Shanks RMQ, Stella NA, Lahr RM, Aston MA, Brothers KM, Callaghan JD, Sigindere C, Liu X. Suppressor analysis of eepRmutant defects reveals coordinate regulation of secondary metabo-lites and serralysin biosynthesis by EepR and HexS. Microbiology. 2017;163(2):280–288. doi:10.1099/mic.0.000422 Medline
• Slater H, Crow M, Everson L, Salmond GPC. Phosphate avail-ability regulates biosynthesis of two antibiotics, prodigiosin and carbapenem, in Serratia via both quorum-sensing-dependent and -independent pathways. Mol Microbiol. 2003;47(2):303–320. doi:10.1046/j.1365-2958.2003.03295.x Medline
• Stella NA, Brothers KM, Callaghan JD, Passerini AM, Sigindere C, Hill PJ, Liu X, Wozniak DJ, Shanks RMQ. An IgaA/UmoB-family protein from Serratia marcescens regulates motility, capsular polysac-charide, and secondary metabolite production. Appl Environ Micro-biol. 2018;84(6):e02575-17. doi:10.1128/AEM.02575-17 Medline
• Stella NA, Fender JE, Lahr RM, Kalivoda EJ, Shanks RM. The LysR transcription factor, HexS, is required for glucose inhibition of prodigiosin production by Serratia marcescens. Adv Microbiol. 2012;2(4):511–517. doi:10.4236/aim.2012.24065 Medline
• Stella NA, Lahr RM, Brothers KM, Kalivoda EJ, Hunt KM,Kwak DH, Liu X, Shanks RMQ.Serratia marcescens cyclic AMP-receptor protein controls transcription of EepR, a novel regulator of antimicrobial secondary metabolites. J Bacteriol. 2015;197(15): 2468–2478. doi:10.1128/JB.00136-15 Medline
• Stella NA, Shanks RMQ. Cyclic-AMP inhibition of fimbriae and prodigiosin production by Serratia marcescens is strain-dependent. Arch Microbiol. 2014;196(5):323–330.doi:10.1007/s00203-014-0970-6 Medline
• Tanaka Y, Yuasa J, Baba M, Tanikawa T, Nakagawa Y, Mat-suyama T. Temperature-dependent bacteriostatic activity of Serratia marcescens. Microbes Environ. 2004;19(3):236–240.doi:10.1264/jsme2.19.236
• Tanikawa T, Nakagawa Y, Matsuyama T. Transcriptional down-re gulator hexS controlling prodigiosin and serrawettin W1 biosynthe-sis in Serratia marcescens. Microbiol Immunol. 2006;50(8):587–596.doi:10.1111/j.1348-0421.2006.tb03833.x Medline
• Vining LC. Functions of secondary metabolites. Annu Rev Micro-biol. 1990;44(1):395–427.doi:10.1146/annurev.mi.44.100190.002143 Medline
• Waters CM, Bassler BL. Quorum sensing: cell-to-cell communi-cation in bacteria. Annu Rev Cell Dev Biol. 2005;21(1):319–346. doi:10.1146/annurev.cellbio.21.012704.131001 MedlineWilliams RP, Goldschmidt ME, Gott CL. Inhibition by tempera-ture of the terminal step in biosynthesis of prodigiosin. Biochem Biophys Res Commun. 1965;19(2):177–181.doi:10.1016/0006-291X(65)90500-0 Medline
• Williamson NR, Fineran PC, Leeper FJ, Salmond GPC. The bio-synthesis and regulation of bacterial prodiginines. Nat Rev Micro-biol. 2006;4(12):887–899. doi:10.1038/nrmicro1531 Medline

Identyfikatory

DOI

10.21307/pjm-2019-005