287
Views
2
CrossRef citations to date
0
Altmetric
REVIEW

The Biological and Regulatory Role of Type VI Secretion System of Klebsiella pneumoniae

, , , , , ORCID Icon & show all
Pages 6911-6922 | Received 27 Jun 2023, Accepted 30 Sep 2023, Published online: 30 Oct 2023

References

  • Yu KW, Xue P, Fu Y, Yang L. T6SS mediated stress responses for bacterial environmental survival and host adaptation. Int J Mol Sci. 2021;22(2). doi:10.3390/ijms22020478
  • Le NH, Pinedo V, Lopez J, Cava F, Feldman MF. Killing of Gram-negative and Gram-positive bacteria by a bifunctional cell wall-targeting T6SS effector. Proc Natl Acad Sci USA. 2021;118(40). doi:10.1073/pnas.2106555118
  • Yang M, Zhou X, Bao Y, et al. Comprehensive genomic analysis reveals extensive diversity of type I and type IV secretion systems in Klebsiella pneumoniae. Curr Microbiol. 2023;80(8):270. doi:10.1007/s00284-023-03362-5
  • Pukatzki S, Ma AT, Sturtevant D, et al. Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci USA. 2006;103(5):1528–1533. doi:10.1073/pnas.0510322103
  • Broms JE, Meyer L, Lavander M, Larsson P, Sjostedt A. DotU and VgrG, core components of type VI secretion systems, are essential for Francisella LVS pathogenicity. PLoS One. 2012;7(4):e34639. doi:10.1371/journal.pone.0034639
  • Blondel CJ, Amaya FA, Bustamante P, Santiviago CA, Pezoa D. Identification and distribution of new candidate T6SS effectors encoded in salmonella pathogenicity Island 6. Front Microbiol. 2023;14:1252344. doi:10.3389/fmicb.2023.1252344
  • Trunk K, Peltier J, Liu YC, et al. The type VI secretion system deploys antifungal effectors against microbial competitors. Nat Microbiol. 2018;3(8):920–931. doi:10.1038/s41564-018-0191-x
  • Fridman CM, Keppel K, Gerlic M, Bosis E, Salomon D. A comparative genomics methodology reveals a widespread family of membrane-disrupting T6SS effectors. Nat Commun. 2020;11(1):1085. doi:10.1038/s41467-020-14951-4
  • Lu W, Lu H, Wang C, Wang G, Dong W, Tan C. Effectors of the type VI secretion system have the potential to be modified into antimicrobial peptides. Microbiol Spectr. 2023;11(4):e0030823. doi:10.1128/spectrum.00308-23
  • Decoin V, Barbey C, Bergeau D, et al. A type VI secretion system is involved in Pseudomonas fluorescens bacterial competition. PLoS One. 2014;9(2):e89411. doi:10.1371/journal.pone.0089411
  • Jani AJ, Cotter PA. Type VI secretion: not just for pathogenesis anymore. Cell Host Microbe. 2010;8(1):2–6. doi:10.1016/j.chom.2010.06.012
  • Tashiro Y, Yawata Y, Toyofuku M, Uchiyama H, Nomura N. Interspecies interaction between Pseudomonas aeruginosa and other microorganisms. Microbes Environ. 2013;28(1):13–24. doi:10.1264/jsme2.ME12167
  • Yang X, Liu H, Zhang Y, Shen X. Roles of type VI secretion system in transport of metal ions. Front Microbiol. 2021;12:756136. doi:10.3389/fmicb.2021.756136
  • Kanarek K, Fridman CM, Bosis E, Salomon D. The RIX domain defines a class of polymorphic T6SS effectors and secreted adaptors. Nat Commun. 2023;14(1):4983. doi:10.1038/s41467-023-40659-2
  • Paczosa MK, Mecsas J. Klebsiella pneumoniae: going on the offense with a strong defense. Microbiol Mol Biol Rev. 2016;80(3):629–661. doi:10.1128/MMBR.00078-15
  • Ahmadi M, Ranjbar R, Behzadi P, Mohammadian T. Virulence factors, antibiotic resistance patterns, and molecular types of clinical isolates of Klebsiella Pneumoniae. Expert Rev Anti Infect Ther. 2022;20(3):463–472. doi:10.1080/14787210.2022.1990040
  • Holt KE, Wertheim H, Zadoks RN, et al. Genomic analysis of diversity, population structure, virulence, and antimicrobial resistance in Klebsiella pneumoniae, an urgent threat to public health. Proc Natl Acad Sci USA. 2015;112(27):E3574–3581. doi:10.1073/pnas.1501049112
  • Karampatakis T, Tsergouli K, Behzadi P. Carbapenem-resistant Klebsiella pneumoniae: virulence factors, molecular epidemiology and latest updates in treatment options. Antibiotics. 2023;12:2.
  • Hsieh PF, Lu YR, Lin TL, Lai LY, Wang JT. Klebsiella pneumoniae type VI secretion system contributes to bacterial competition, cell invasion, type-1 fimbriae expression, and in vivo colonization. J Infect Dis. 2019;219(4):637–647. doi:10.1093/infdis/jiy534
  • Liu L, Ye M, Li X, et al. Identification and characterization of an antibacterial type VI secretion system in the carbapenem-resistant strain Klebsiella pneumoniae HS11286. Front Cell Infect Microbiol. 2017;7:442. doi:10.3389/fcimb.2017.00442
  • Zhang Y, Xu Y, Huang Y. Virulence genotype and correlation of clinical severeness with presence of the type VI secretion system in Klebsiella pneumoniae isolates causing bloodstream infections. Infect Drug Resist. 2022;15:1487–1497. doi:10.2147/IDR.S353858
  • Boyer F, Fichant G, Berthod J, Vandenbrouck Y, Attree I. Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources? BMC Genomics. 2009;10:104. doi:10.1186/1471-2164-10-104
  • Zheng J, Leung KY. Dissection of a type VI secretion system in Edwardsiella tarda. Mol Microbiol. 2007;66(5):1192–1206. doi:10.1111/j.1365-2958.2007.05993.x
  • Singh RP, Kumari K. Bacterial type VI secretion system (T6SS): an evolved molecular weapon with diverse functionality. Biotechnol Lett. 2023;45(3):309–331. doi:10.1007/s10529-023-03354-2
  • Li W, Liu X, Tsui W, et al. Identification and comparative genomic analysis of type VI secretion systems and effectors in Klebsiella pneumoniae. Front Microbiol. 2022;13:853744. doi:10.3389/fmicb.2022.853744
  • Cascales E, Cambillau C. Structural biology of type VI secretion systems. Philos Trans R Soc Lond B Biol Sci. 2012;367(1592):1102–1111. doi:10.1098/rstb.2011.0209
  • Navarro-Garcia F, Ruiz-Perez F, Cataldi A, Larzabal M. Type VI secretion system in pathogenic Escherichia coli: structure, role in virulence, and acquisition. Front Microbiol. 2019;10:1965. doi:10.3389/fmicb.2019.01965
  • Hespanhol JT, Nobrega-Silva L, Bayer-Santos E. Regulation of type VI secretion systems at the transcriptional, posttranscriptional and posttranslational level. Microbiology. 2023;169(8). doi:10.1099/mic.0.001376
  • Nguyen VS, Douzi B, Durand E, Roussel A, Cascales E, Cambillau C. Towards a complete structural deciphering of Type VI secretion system. Curr Opin Struct Biol. 2018;49:77–84. doi:10.1016/j.sbi.2018.01.007
  • Cianfanelli FR, Alcoforado Diniz J, Guo M, De Cesare V, Trost M, Coulthurst SJ. VgrG and PAAR proteins define distinct versions of a functional type VI secretion system. PLoS Pathog. 2016;12(6):e1005735. doi:10.1371/journal.ppat.1005735
  • Weber BS, Kinsella RL, Harding CM, Feldman MF. The secrets of Acinetobacter secretion. Trends Microbiol. 2017;25(7):532–545. doi:10.1016/j.tim.2017.01.005
  • Leiman PG, Basler M, Ramagopal UA, et al. Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc Natl Acad Sci USA. 2009;106(11):4154–4159. doi:10.1073/pnas.0813360106
  • Douzi B, Logger L, Spinelli S, Blangy S, Cambillau C, Cascales E. Structure-function analysis of the C-terminal domain of the type VI secretion TssB tail sheath subunit. J Mol Biol. 2018;430(3):297–309. doi:10.1016/j.jmb.2017.11.015
  • Do Nascimento Soares T, Silva Valadares V, Cardoso Amorim G, et al. The C-terminal extension of VgrG4 from Klebsiella pneumoniae remodels host cell microfilaments. Proteins. 2022;90(9):1655–1668. doi:10.1002/prot.26344
  • Shneider MM, Buth SA, Ho BT, Basler M, Mekalanos JJ, Leiman PG. PAAR-repeat proteins sharpen and diversify the type VI secretion system spike. Nature. 2013;500(7462):350–353. doi:10.1038/nature12453
  • Basler M, Pilhofer M, Henderson GP, Jensen GJ, Mekalanos JJ. Type VI secretion requires a dynamic contractile phage tail-like structure. Nature. 2012;483(7388):182–186. doi:10.1038/nature10846
  • Howard SA, Furniss RCD, Bonini D, et al. The breadth and molecular basis of hcp-driven type VI Secretion system effector delivery. mBio. 2021;12(3):e0026221. doi:10.1128/mBio.00262-21
  • Durand E, Cambillau C, Cascales E, Journet L. VgrG, Tae, Tle, and beyond: the versatile arsenal of Type VI secretion effectors. Trends Microbiol. 2014;22(9):498–507. doi:10.1016/j.tim.2014.06.004
  • Liang X, Zheng HY, Zhao YJ, et al. VgrG Spike Dictates PAAR Requirement for the assembly of the type VI secretion system. J Bacteriol. 2023;205(2):e0035622. doi:10.1128/jb.00356-22
  • Alcoforado Diniz J, Liu YC, Coulthurst SJ. Molecular weaponry: diverse effectors delivered by the Type VI secretion system. Cell Microbiol. 2015;17(12):1742–1751. doi:10.1111/cmi.12532
  • Chen L, Zou Y, She P, Wu Y. Composition, function, and regulation of T6SS in Pseudomonas aeruginosa. Microbiol Res. 2015;172:19–25. doi:10.1016/j.micres.2015.01.004
  • Cherrak Y, Rapisarda C, Pellarin R, et al. Biogenesis and structure of a type VI secretion baseplate. Nat Microbiol. 2018;3(12):1404–1416. doi:10.1038/s41564-018-0260-1
  • Nguyen VS, Logger L, Spinelli S, et al. Type VI secretion TssK baseplate protein exhibits structural similarity with phage receptor-binding proteins and evolved to bind the membrane complex. Nat Microbiol. 2017;2:17103. doi:10.1038/nmicrobiol.2017.103
  • Cherrak Y, Filella-Merce I, Schmidt V, et al. Inhibiting type VI secretion system activity with a biomimetic peptide designed to target the baseplate wedge complex. mBio. 2021;12(4):e0134821. doi:10.1128/mBio.01348-21
  • Rapisarda C, Cherrak Y, Kooger R, et al. In situ and high-resolution cryo-EM structure of a bacterial type VI secretion system membrane complex. EMBO J. 2019;38(10). doi:10.15252/embj.2018100886
  • Yin M, Yan Z, Li X. Architecture of type VI secretion system membrane core complex. Cell Res. 2019;29(3):251–253. doi:10.1038/s41422-018-0130-7
  • Cherrak Y, Flaugnatti N, Durand E, Journet L, Cascales E. Structure and activity of the type VI secretion system. Microbiol Spectr. 2019;7(4). doi:10.1128/microbiolspec.PSIB-0031-2019
  • Bonemann G, Pietrosiuk A, Diemand A, Zentgraf H, Mogk A. Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO J. 2009;28(4):315–325. doi:10.1038/emboj.2008.269
  • Schlieker C, Zentgraf H, Dersch P, Mogk A. ClpV, a unique Hsp100/Clp member of pathogenic proteobacteria. Biol Chem. 2005;386(11):1115–1127. doi:10.1515/BC.2005.128
  • Kapitein N, Bonemann G, Pietrosiuk A, et al. ClpV recycles VipA/VipB tubules and prevents non-productive tubule formation to ensure efficient type VI protein secretion. Mol Microbiol. 2013;87(5):1013–1028. doi:10.1111/mmi.12147
  • Dix SR, Owen HJ, Sun R, et al. Structural insights into the function of type VI secretion system TssA subunits. Nat Commun. 2018;9(1):4765. doi:10.1038/s41467-018-07247-1
  • Santin YG, Doan T, Lebrun R, Espinosa L, Journet L, Cascales E. In vivo TssA proximity labelling during type VI secretion biogenesis reveals TagA as a protein that stops and holds the sheath. Nat Microbiol. 2018;3(11):1304–1313. doi:10.1038/s41564-018-0234-3
  • Zoued A, Durand E, Santin YG, et al. TssA: the cap protein of the Type VI secretion system tail. Bioessays. 2017;39(10). doi:10.1002/bies.201600262
  • Planamente S, Salih O, Manoli E, Albesa-Jove D, Freemont PS, Filloux A. TssA forms a gp6-like ring attached to the type VI secretion sheath. EMBO J. 2016;35(15):1613–1627. doi:10.15252/embj.201694024
  • Stietz MS, Liang X, Li H, Zhang X, Dong TG. TssA-TssM-TagA interaction modulates type VI secretion system sheath-tube assembly in Vibrio cholerae. Nat Commun. 2020;11(1):5065. doi:10.1038/s41467-020-18807-9
  • Pira H, Risdian C, Musken M, Schupp PJ, Wink J. Photobacterium arenosum WH24, isolated from the gill of pacific oyster Crassostrea gigas from the North Sea of Germany: co-cultivation and prediction of virulence. Curr Microbiol. 2022;79(8):219. doi:10.1007/s00284-022-02909-2
  • Brunet YR, Zoued A, Boyer F, Douzi B, Cascales E. The Type VI Secretion TssEFGK-VgrG phage-like baseplate is recruited to the TssJLM membrane complex via multiple contacts and serves as assembly platform for tail tube/sheath polymerization. PLoS Genet. 2015;11(10):e1005545. doi:10.1371/journal.pgen.1005545
  • Liebl D, Robert-Genthon M, Job V, Cogoni V, Attree I. Baseplate component TssK and spatio-temporal assembly of T6SS in pseudomonas aeruginosa. Front Microbiol. 2019;10:1615. doi:10.3389/fmicb.2019.01615
  • Zoued A, Cassaro CJ, Durand E, et al. Structure-function analysis of the TssL cytoplasmic domain reveals a new interaction between the type VI secretion baseplate and membrane complexes. J Mol Biol. 2016;428(22):4413–4423. doi:10.1016/j.jmb.2016.08.030
  • Zheng HY, Yang L, Dong T. More than just a spearhead: diverse functions of PAAR for assembly and delivery of toxins of the contractile injection systems. mSystems. 2021;6(6):e0138621. doi:10.1128/msystems.01386-21
  • Y G, J L, W H. Advances in Klebsiella pneumoniae and Acinetobacter baumannii type VI secretion systems. Chin J Microbiol Immunol. 2021;41(08):640–644.
  • Lawlor MS, Hsu J, Rick PD, Miller VL. Identification of Klebsiella pneumoniae virulence determinants using an intranasal infection model. Mol Microbiol. 2005;58(4):1054–1073. doi:10.1111/j.1365-2958.2005.04918.x
  • Sarris PF, Zoumadakis C, Panopoulos NJ, Scoulica EV. Distribution of the putative type VI secretion system core genes in Klebsiella spp. Infect Genet Evol. 2011;11(1):157–166. doi:10.1016/j.meegid.2010.09.006
  • Barret M, Egan F, Fargier E, Morrissey JP, O’Gara F. Genomic analysis of the type VI secretion systems in Pseudomonas spp.: novel clusters and putative effectors uncovered. Microbiology. 2011;157(Pt 6):1726–1739. doi:10.1099/mic.0.048645-0
  • Barret M, Egan F, O’Gara F. Distribution and diversity of bacterial secretion systems across metagenomic datasets. Environ Microbiol Rep. 2013;5(1):117–126. doi:10.1111/j.1758-2229.2012.00394.x
  • Russell AB, Wexler AG, Harding BN, et al. A type VI secretion-related pathway in Bacteroidetes mediates interbacterial antagonism. Cell Host Microbe. 2014;16(2):227–236. doi:10.1016/j.chom.2014.07.007
  • Zhang J, Guan J, Wang M, et al. SecReT6 update: a comprehensive resource of bacterial Type VI Secretion Systems. Sci China Life Sci. 2023;66(3):626–634. doi:10.1007/s11427-022-2172-x
  • Bock D, Medeiros JM, Tsao HF, et al. In situ architecture, function, and evolution of a contractile injection system. Science. 2017;357(6352):713–717. doi:10.1126/science.aan7904
  • Lery LM, Frangeul L, Tomas A, et al. Comparative analysis of Klebsiella pneumoniae genomes identifies a phospholipase D family protein as a novel virulence factor. BMC Biol. 2014;12:41. doi:10.1186/1741-7007-12-41
  • Barbosa VAA, Lery LMS. Insights into Klebsiella pneumoniae type VI secretion system transcriptional regulation. BMC Genomics. 2019;20(1):506. doi:10.1186/s12864-019-5885-9
  • Storey D, McNally A, Astrand M, et al. Klebsiella pneumoniae type VI secretion system-mediated microbial competition is PhoPQ controlled and reactive oxygen species dependent. PLoS Pathog. 2020;16(3):e1007969. doi:10.1371/journal.ppat.1007969
  • Fitzsimons TC, Lewis JM, Wright A, et al. Identification of novel Acinetobacter baumannii type VI Secretion system antibacterial effector and immunity pairs. Infect Immun. 2018;86(8). doi:10.1128/IAI.00297-18
  • Sa-Pessoa J, Lopez-Montesino S, Przybyszewska K, et al. A trans-kingdom T6SS effector induces the fragmentation of the mitochondrial network and activates innate immune receptor NLRX1 to promote infection. Nat Commun. 2023;14(1):871. doi:10.1038/s41467-023-36629-3
  • Merciecca T, Bornes S, Nakusi L, et al. Role of Klebsiella pneumoniae Type VI secretion system (T6SS) in long-term gastrointestinal colonization. Sci Rep. 2022;12(1):16968. doi:10.1038/s41598-022-21396-w
  • Liao W, Huang HH, Huang QS, et al. Distribution of type VI secretion system (T6SS) in clinical Klebsiella pneumoniae strains from a Chinese hospital and its potential relationship with virulence and drug resistance. Microb Pathog. 2022;162:105085. doi:10.1016/j.micpath.2021.105085
  • Thomas J, Watve SS, Ratcliff WC, Hammer BK. Horizontal gene transfer of functional type VI killing genes by natural transformation. mBio. 2017;8(4). doi:10.1128/mBio.00654-17
  • Chen F, Zhang W, Schwarz S, et al. Genetic characterization of an MDR/virulence genomic element carrying two T6SS gene clusters in a clinical Klebsiella pneumoniae isolate of swine origin. J Antimicrob Chemother. 2019;74(6):1539–1544. doi:10.1093/jac/dkz093
  • Liu P, Yang A, Tang B, et al. Molecular epidemiology and clinical characteristics of the type VI secretion system in Klebsiella pneumoniae causing abscesses. Front Microbiol. 2023;14:1181701. doi:10.3389/fmicb.2023.1181701
  • Kapitein N, Mogk A. Deadly syringes: type VI secretion system activities in pathogenicity and interbacterial competition. Curr Opin Microbiol. 2013;16(1):52–58. doi:10.1016/j.mib.2012.11.009
  • Dey S, Gaur M, Sykes EME, et al. Unravelling the evolutionary dynamics of high-risk Klebsiella pneumoniae ST147 clones: insights from comparative pangenome analysis. Genes. 2023;14(5):1037. doi:10.3390/genes14051037
  • Zhou M, Lan Y, Wang S, et al. Epidemiology and molecular characteristics of the type VI secretion system in Klebsiella pneumoniae isolated from bloodstream infections. J Clin Lab Anal. 2020;34(11):e23459. doi:10.1002/jcla.23459
  • Wang H, Guo Y, Liu Z, Chang Z. The type VI secretion system contributes to the invasiveness of liver abscess caused by Klebsiella pneumoniae. J Infect Dis. 2023;228:1127–1136. doi:10.1093/infdis/jiad166
  • Silverman JM, Brunet YR, Cascales E, Mougous JD. Structure and regulation of the type VI secretion system. Annu Rev Microbiol. 2012;66:453–472. doi:10.1146/annurev-micro-121809-151619
  • Miyata ST, Bachmann V, Pukatzki S. Type VI secretion system regulation as a consequence of evolutionary pressure. J Med Microbiol. 2013;62(Pt 5):663–676. doi:10.1099/jmm.0.053983-0
  • Ali SS, Xia B, Liu J, Navarre WW. Silencing of foreign DNA in bacteria. Curr Opin Microbiol. 2012;15(2):175–181. doi:10.1016/j.mib.2011.12.014
  • Ares MA, Fernandez-Vazquez JL, Rosales-Reyes R, et al. H-NS nucleoid protein controls virulence features of Klebsiella pneumoniae by regulating the expression of type 3 Pili and the capsule polysaccharide. Front Cell Infect Microbiol. 2016;6:13. doi:10.3389/fcimb.2016.00013
  • Ares MA, Fernandez-Vazquez JL, Pacheco S, et al. Additional regulatory activities of MrkH for the transcriptional expression of the Klebsiella pneumoniae mrk genes: antagonist of H-NS and repressor. PLoS One. 2017;12(3):e0173285. doi:10.1371/journal.pone.0173285
  • Bent ZW, Poorey K, LaBauve AE, Hamblin R, Williams KP, Meagher RJ. A rapid spin column-based method to enrich pathogen transcripts from eukaryotic host cells prior to sequencing. PLoS One. 2016;11(12):e0168788. doi:10.1371/journal.pone.0168788
  • Gueguen E, Durand E, Zhang XY, d’Amalric Q, Journet L, Cascales E. Expression of a Yersinia pseudotuberculosis type VI secretion system is responsive to envelope stresses through the OmpR transcriptional activator. PLoS One. 2013;8(6):e66615. doi:10.1371/journal.pone.0066615
  • Zhang W, Wang Y, Song Y, et al. A type VI secretion system regulated by OmpR in Yersinia pseudotuberculosis functions to maintain intracellular pH homeostasis. Environ Microbiol. 2013;15(2):557–569. doi:10.1111/1462-2920.12005
  • Lin TH, Chen Y, Kuo JT, et al. Phosphorylated OmpR is required for type 3 fimbriae expression in Klebsiella pneumoniae under hypertonic conditions. Front Microbiol. 2018;9:2405. doi:10.3389/fmicb.2018.02405
  • Wong Fok Lung T, Charytonowicz D, Beaumont KG, et al. Klebsiella pneumoniae induces host metabolic stress that promotes tolerance to pulmonary infection. Cell Metab. 2022;34(5):761–774 e769. doi:10.1016/j.cmet.2022.03.009
  • Hennequin C, Forestier C. oxyR, a LysR-type regulator involved in Klebsiella pneumoniae mucosal and abiotic colonization. Infect Immun. 2009;77(12):5449–5457. doi:10.1128/IAI.00837-09
  • Srinivasan VB, Mondal A, Venkataramaiah M, Chauhan NK, Rajamohan G. Role of oxyRKP, a novel LysR-family transcriptional regulator, in antimicrobial resistance and virulence in Klebsiella pneumoniae. Microbiology. 2013;159(Pt 7):1301–1314. doi:10.1099/mic.0.065052-0
  • Peng D, Li X, Liu P, et al. Transcriptional regulation of galF by RcsAB affects capsular polysaccharide formation in Klebsiella pneumoniae NTUH-K2044. Microbiol Res. 2018;216:70–78. doi:10.1016/j.micres.2018.08.010
  • Su K, Zhou X, Luo M, et al. Genome-wide identification of genes regulated by RcsA, RcsB, and RcsAB phosphorelay regulators in Klebsiella pneumoniae NTUH-K2044. Microb Pathog. 2018;123:36–41. doi:10.1016/j.micpath.2018.06.036
  • Brown MJ, Russo BC, O’Dee DM, Schmitt DM, Nau GJ. The contribution of the glycine cleavage system to the pathogenesis of Francisella tularensis. Microbes Infect. 2014;16(4):300–309. doi:10.1016/j.micinf.2013.12.003
  • Mallik P, Pratt TS, Beach MB, Bradley MD, Undamatla J, Osuna R. Growth phase-dependent regulation and stringent control of fis are conserved processes in enteric bacteria and involve a single promoter (fis P) in Escherichia coli. J Bacteriol. 2004;186(1):122–135. doi:10.1128/JB.186.1.122-135.2004
  • Li L, Ma J, Cheng P, et al. Roles of two-component regulatory systems in Klebsiella pneumoniae: regulation of virulence, antibiotic resistance, and stress responses. Microbiol Res. 2023;272:127374. doi:10.1016/j.micres.2023.127374
  • Zhang F, Yan X, Bai J, et al. Identification of the BolA protein reveals a novel virulence factor in K. pneumoniae that contributes to survival in host. Microbiol Spectr. 2022;10(5):e0037822. doi:10.1128/spectrum.00378-22