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Articles

Transcriptional response to metal starvation in the emerging pathogen Mycoplasma genitalium is mediated by Fur-dependent and –independent regulatory pathways

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Pages 5-19 | Received 06 Jul 2019, Accepted 08 Nov 2019, Published online: 20 Dec 2019

References

  • Moi H, Blee K, Horner PJ. Management of non-gonococcal urethritis. BMC Infect Dis. 2015;15, doi:10.1186/s12879-015-1043-4.
  • Horner PJ, Blee K, Falk L, et al. 2016 European guideline on the management of non-gonococcal urethritis. Int J STD AIDS. 2016;27:928–937. doi:10.1177/0956462416648585.
  • McGowin CL, Totten PA. The unique microbiology and molecular pathogenesis of Mycoplasma genitalium. J Infect Dis. 2017;216:S382–S388. doi:10.1093/infdis/jix172.
  • Jensen JS. Mycoplasma genitalium : yet another challenging STI. Lancet Infect Dis. 2017;17:795–796. doi:10.1016/S1473-3099(17)30364-X.
  • Bradshaw CS, Horner PJ, Jensen JS, et al. Syndromic management of STIs and the threat of untreatable Mycoplasma genitalium. Lancet Infect Dis. 2018;18:251–252. doi:10.1016/s1473-3099(18)30080-x.
  • Anagrius C, Loré B, Jensen JS. Mycoplasma genitalium: prevalence, clinical significance, and transmission. Sex Transm Infect. 2005;81:458–462. doi:10.1136/sti.2004.012062.
  • Soni S, Alexander S, Verlander N, et al. The prevalence of urethral and rectal Mycoplasma genitalium and its associations in men who have sex with men attending a genitourinary medicine clinic. Sex Transm Infect. 2010;86:21–24. doi:10.1136/sti.2009.038190.
  • Martin DH, Manhart LE, Workowski KA. Mycoplasma genitalium from basic science to public health: summary of the results from a National Institute of Allergy and Infectious Disease Technical Consultation and consensus Recommendations for Future Research Priorities. J Infect Dis. 2017;216:S427–S430. doi:10.1093/infdis/jix147.
  • Deguchi T. Proposed treatment strategies for non-gonococcal urethritis. Lancet Infect Dis. 2017;17:1121–1122. doi:10.1016/s1473-3099(17)30571-6.
  • Jensen JS, Cusini M, Gomberg M, et al. 2016 European guideline on Mycoplasma genitalium infections. J Eur Acad Dermatol Venereol. 2016;30:1650–1656. doi:10.1111/jdv.13849.
  • Neumann W, Gulati A, Nolan EM. Metal homeostasis in infectious disease: recent advances in bacterial metallophores and the human metal-withholding response. Curr Opin Chem Biol. 2017;37:10–18. doi:10.1016/j.cbpa.2016.09.012.
  • Merrell DS, Thompson LJ, Kim CC, et al. Growth phase-dependent response of Helicobacter pylori to iron starvation. Infect Immun. 2003;71:6510–6525. doi:10.1128/IAI.71.11.6510-6525.2003.
  • Litwin CM, Calderwood SB. Role of iron in regulation of virulence genes. Clin Microbiol Rev. 1993;6:137–149. doi:10.1128/CMR.6.2.137.
  • Tan S, Tompkins LS, Amieva MR. Helicobacter pylori usurps cell polarity to turn the cell surface into a replicative niche. PLoS Pathog. 2009;5:e1000407. doi:10.1371/journal.ppat.1000407.
  • Tan S, Noto JM, Romero-Gallo J, et al. Helicobacter pylori perturbs iron trafficking in the epithelium to grow on the cell surface. PLoS Pathog. 2011;7:e1002050. doi:10.1371/journal.ppat.1002050.
  • Troxell B, Hassan HM. Transcriptional regulation by ferric uptake regulator (Fur) in pathogenic bacteria. Front Cell Infect Microbiol. 2013;3. doi:10.3389/fcimb.2013.00059.
  • Lee JW, Helmann JD. Functional specialization within the fur family of metalloregulators. BioMetals. 2007;20:485–499. doi:10.1007/s10534-006-9070-7.
  • Pich OQ, Merrell DS. The ferric uptake regulator of Helicobacter pylori: a critical player in the battle for iron and colonization of the stomach. Future Microbiol. 2013;8:725–738. doi:10.2217/fmb.13.43.
  • Madsen ML, Nettleton D, Thacker EL, et al. Transcriptional profiling of Mycoplasma hyopneumoniae during iron depletion using microarrays. Microbiology. 2006;152:937–944. doi:10.1099/mic.0.28674-0.
  • Yus E, Lloréns-Rico V, Martínez S, et al. Determination of the gene regulatory network of a genome-reduced bacterium highlights alternative regulation independent of transcription factors. Cell Syst. 2019;9:143–158.e13. doi:10.1016/j.cels.2019.07.001.
  • Torres-Puig S, Broto A, Querol E, et al. A novel sigma factor reveals a unique regulon controlling cell-specific recombination in Mycoplasma genitalium. Nucleic Acids Res. 2015;43:4923–4936. doi:10.1093/nar/gkv422.
  • Torres-Puig S, Martínez-Torró C, Granero-Moya I, et al. Activation of σ20-dependent recombination and horizontal gene transfer in Mycoplasma genitalium. DNA Res. 2018;25:383–393. doi:10.1093/dnares/dsy011.
  • Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9:357–359. doi:10.1038/nmeth.1923.
  • Li H, Handsaker B, Wysoker A, et al. The sequence alignment/Map format and SAMtools. Bioinformatics. 2009;25:2078–2079. doi:10.1093/bioinformatics/btp352.
  • Liao Y, Smyth GK, Shi W. Featurecounts: An efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 2014;30:923–930. doi:10.1093/bioinformatics/btt656.
  • Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15. doi:10.1186/s13059-014-0550-8.
  • Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001;29:e45. doi: 10.1093/nar/29.9.e45
  • Párraga-Niño N, Colomé-Calls N, Canals F, et al. A comprehensive proteome of Mycoplasma genitalium. J Proteome Res. 2012;11:3305–3316. doi:10.1021/pr300084c.
  • Williams CL, Neu HM, Michel SLJ, et al. Measuring intracellular metal concentration via ICP-MS following copper exposure. Methods Mol Biol. 2019;1946:195–205. doi:10.1007/978-1-4939-9118-1_19.
  • Waterhouse A, Bertoni M, Bienert S, et al. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res. 2018;46:W296–W303. doi:10.1093/nar/gky427.
  • Kingsford CL, Ayanbule K, Salzberg SL. Rapid, accurate, computational discovery of Rho-independent transcription terminators illuminates their relationship to DNA uptake. Genome Biol. 2007;8:R22. doi:10.1186/gb-2007-8-2-r22.
  • Shimizu T, Kida Y, Kuwano K. A triacylated lipoprotein from Mycoplasma genitalium activates NF-κB through Toll-like receptor 1 (TLR1) and TLR2. Infect Immun. 2008;76:3672–3678. doi:10.1128/IAI.00257-08.
  • Hood MI, Skaar EP. Nutritional immunity: transition metals at the pathogen-host interface. Nat Rev Microbiol. 2012;10:525–537. doi:10.1038/nrmicro2836.
  • Tryon VV, Baseman JB. The acquisition of human lactoferrin by Mycoplasma pneumoniae. Microb Pathog. 1987;3:437–443. doi:10.1016/0882-4010(87)90013-1.
  • Bullen JJ, Rogers HJ, Spalding PB, et al. Iron and infection: the heart of the matter. FEMS Immunol Med Microbiol. 2005;43:325–330. doi:10.1016/j.femsim.2004.11.010.
  • Musatovova O, Dhandayuthapani S, Baseman JB. Transcriptional heat shock response in the smallest known self-replicating cell, Mycoplasma genitalium. J Bacteriol. 2006;188:2845–2855. doi:10.1128/JB.188.8.2845-2855.2006.
  • Hauryliuk V, Atkinson GC, Murakami KS, et al. Recent functional insights into the role of (p)ppGpp in bacterial physiology. Nat Rev Microbiol. 2015;13:298–309. doi:10.1038/nrmicro3448.
  • Hempel K, Herbst FA, Moche M, et al. Quantitative proteomic view on secreted, cell surface-associated, and cytoplasmic proteins of the methicillin-resistant human pathogen Staphylococcus aureus under iron-limited conditions. J Proteome Res. 2011;10:1657–1666. doi:10.1021/pr1009838.
  • Letoffe S, Delepelaire P, Wandersman C. The housekeeping dipeptide permease is the Escherichia coli heme transporter and functions with two optional peptide binding proteins. Proc Natl Acad Sci. 2006;103:12891–12896. doi:10.1073/pnas.0605440103.
  • Hiron A, Posteraro B, Carrière M, et al. A nickel ABC-transporter of Staphylococcus aureus is involved in urinary tract infection. Mol Microbiol. 2010;77:1246–1260. doi:10.1111/j.1365-2958.2010.07287.x.
  • Tanaka KJ, Pinkett HW. Oligopeptide-binding protein from nontypeable Haemophilus influenzae has ligand-specific sites to accommodate peptides and heme in the binding pocket. J Biol Chem. 2019;294:1070–1082. doi:10.1074/jbc.RA118.004479.
  • Tseng C-W, Chiu C-J, Kanci A, et al. The oppD gene and putative peptidase genes may be required for virulence in Mycoplasma gallisepticum. Infect Immun. 2017;85. doi:10.1128/iai.00023-17.
  • Pilo P, Vilei EM, Peterhans E, et al. A metabolic enzyme as a primary virulence factor of Mycoplasma mycoides subsp. mycoides small colony. J Bacteriol. 2005;187:6824–6831. doi:10.1128/JB.187.19.6824-6831.2005.
  • Hames C, Halbedel S, Hoppert M, et al. Glycerol metabolism is important for cytotoxicity of Mycoplasma pneumoniae. J Bacteriol. 2009;191:747–753. doi:10.1128/JB.01103-08.
  • Großhennig S, Schmidl SR, Schmeisky G, et al. Implication of glycerol and phospholipid transporters in Mycoplasma pneumoniae growth and virulence. Infect Immun. 2013;81:896–904. doi:10.1128/iai.01212-12.
  • Liang W, Ouyang S, Shaw N, et al. Conversion of d -ribulose 5-phosphate to d -xylulose 5-phosphate: new insights from structural and biochemical studies on human RPE. FASEB J. 2010;25:497–504. doi:10.1096/fj.10-171207.
  • Glass JI, Assad-Garcia N, Alperovich N, et al. Essential genes of a minimal bacterium. Proc Natl Acad Sci. 2006;103:425–430. doi:10.1073/pnas.0510013103.
  • Zhang W, Baseman JB. Transcriptional regulation of MG_149, an osmoinducible lipoprotein gene from Mycoplasma genitalium. Mol Microbiol. 2011;81:327–339. doi:10.1111/j.1365-2958.2011.07717.x.
  • Gancz H, Merrell DS. The Helicobacter pylori ferric uptake regulator (Fur) is essential for growth under sodium chloride stress. J Microbiol. 2011;49:294–298. doi:10.1007/s12275-011-0396-7.
  • Gancz H, Jones KR, Merrell DS. Sodium chloride affects Helicobacter pylori growth and gene expression. J Bacteriol. 2008;190:4100–4105. doi:10.1128/JB.01728-07.
  • De Lorenzo V, Wee S, Herrero M, et al. Operator sequences of the aerobactin operon of plasmid colV–K30 binding the ferric uptake regulation (fur) repressor. J Bacteriol. 1987;169:2624–2630. doi:10.1128/jb.169.6.2624-2630.1987.
  • Escolar L, Pérez-Martín J, De Lorenzo V. Binding of the Fur (ferric uptake regulator) repressor of Escherichia coli to arrays of the GATAAT sequence. J Mol Biol. 1998;283:537–547. doi:10.1006/jmbi.1998.2119.
  • Milano A, Forti F, Sala C, et al. Transcriptional regulation of furA and katG upon oxidative stress in Mycobacterium smegmatis. J Bacteriol. 2001;183:6801–6806. doi:10.1128/JB.183.23.6801-6806.2001.
  • Güell M, Van Noort V, Yus E, et al. Transcriptome complexity in a genome-reduced bacterium. Science. 2009;326:1268–1271. doi:10.1126/science.1176951.
  • Zhao S, Cao S, Luo L, et al. A preliminary investigation of metal element profiles in the serum of patients with bloodstream infections using inductively-coupled plasma mass spectrometry (ICP-MS). Clin Chim Acta. 2018;485:323–332. doi:10.1016/j.cca.2018.07.013.
  • Pohl E, Haller JC, Mijovilovich A, et al. Architecture of a protein central to iron homeostasis: crystal structure and spectroscopic analysis of the ferric uptake regulator. Mol Microbiol. 2003;47:903–915. doi:10.1046/j.1365-2958.2003.03337.x.
  • Jacquamet L, Aberdam D, Adrait A, et al. X-ray absorption spectroscopy of a new zinc site in the Fur protein from Escherichia coli. Biochemistry. 1998;37:2564–2571. doi:10.1021/bi9721344.
  • Sheikh MA, Taylor GL. Crystal structure of the Vibrio cholerae ferric uptake regulator (Fur) reveals insights into metal co-ordination. Mol Microbiol. 2009;72:1208–1220. doi:10.1111/j.1365-2958.2009.06718.x.
  • D’Autréaux B, Pecqueur L, De Peredo AG, et al. Reversible redox- and zinc-dependent dimerization of the Escherichia coli fur protein. Biochemistry. 2007;46:1329–1342. doi:10.1021/bi061636r.
  • Lauinger L, Li J, Shostak A, et al. Thiolutin is a zinc chelator that inhibits the Rpn11 and other JAMM metalloproteases. Nat Chem Biol. 2017;13:709–714. doi:10.1038/nchembio.2370.
  • Rodrigue A, Effantin G, Mandrand-Berthelot M-A. Identification of rcnA (yohM), a nickel and cobalt resistance gene in Escherichia coli. J Bacteriol. 2005;187:2912–2916. doi:10.1128/JB.187.8.2912-2916.2005.
  • Rodionov DA, Hebbeln P, Gelfand MS, et al. Comparative and functional genomic analysis of prokaryotic nickel and cobalt uptake transporters: evidence for a novel group of ATP-binding cassette transporters. J Bacteriol. 2006;188:317–327. doi:10.1128/JB.188.1.317-327.2006.
  • Bousis S, Setyawati I, Diamanti E, et al. Energy-coupling factor transporters as novel antimicrobial targets. Adv Ther. 2018;2:1800066. doi:10.1002/adtp.201800066.
  • Shimizu T, Kida Y, Kuwano K. Triacylated lipoproteins derived from Mycoplasma pneumoniae activate nuclear factor-κB through toll-like receptors 1 and 2. Immunology. 2007;121:473–483. doi:10.1111/j.1365-2567.2007.02594.x.
  • Mathieu S, Cissé C, Vitale S, et al. From peptide aptamers to inhibitors of FUR, bacterial transcriptional regulator of iron homeostasis and virulence. ACS Chem Biol. 2016;11:2519–2528. doi:10.1021/acschembio.6b00360.
  • Sarvan S, Charih F, Askoura M, et al. Functional insights into the interplay between DNA interaction and metal coordination in ferric uptake regulators. Sci Rep. 2018;8. doi:10.1038/s41598-018-25157-6.