环二鸟苷酸(c-di-GMP)对大肠杆菌生物学功能的调控作用及机制
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摘要
环二鸟苷酸(cyclic diguanosine monophosphate, c-di-GMP)是在细菌中发现的第二信使之一,参与大肠杆菌运动性、生物被膜形成及毒力等众多功能的调节。合成与水解c-di-GMP的二鸟苷酸环化酶(diguanylate cyclases, DGCs)和特异性的磷酸二酯酶(phosphodiesterases, PDEs)在大肠杆菌中分布广泛且丰富度较高。同时,DGCs和PDEs的蛋白结构不仅包括与c-di-GMP相关的酶活性中心,而且还具有多种感受环境变化和接收信号分子调节的结构域。鉴于c-di-GMP的调控复杂且值得深入探索,本文综述了c-di-GMP对大肠杆菌生物学特性的调控作用以及c-di-GMP在大肠杆菌中的两种调控模型,并对最新研究进展和应用进行展望。
Cyclic diguanosine monophosphate(c-di-GMP) is one of the second messengers found in bacteria, which is involved in the regulation of many functions in E. coli, such as motility, biofilm formation and virulence. Diguanosine cyclases(DGCs) and specific phosphodiesterases(PDEs) regulate the synthesis and hydrolysis of c-di-GMP, and they are widely distributed and abundant in E. coli. The protein structure of DGCs and PDEs not only includes the c-di-GMP enzymatic activity center, but also has a variety of domains that sense environmental changes and receive regulatory signal molecular. In view of the complexity of c-di-GMP regulation and the worthy of further exploration, the biological functions regulation and two kinds of regulatory models of c-di-GMP in E. coli were reviewed in this paper. We also summarize the latest research progress and application prospect of c-di-GMP in the end.
Cyclic diguanosine monophosphate(c-di-GMP) is one of the second messengers found in bacteria, which is involved in the regulation of many functions in E. coli, such as motility, biofilm formation and virulence. Diguanosine cyclases(DGCs) and specific phosphodiesterases(PDEs) regulate the synthesis and hydrolysis of c-di-GMP, and they are widely distributed and abundant in E. coli. The protein structure of DGCs and PDEs not only includes the c-di-GMP enzymatic activity center, but also has a variety of domains that sense environmental changes and receive regulatory signal molecular. In view of the complexity of c-di-GMP regulation and the worthy of further exploration, the biological functions regulation and two kinds of regulatory models of c-di-GMP in E. coli were reviewed in this paper. We also summarize the latest research progress and application prospect of c-di-GMP in the end.
引文
[1] Hengge R. Principles of c-di-GMP signalling in bacteria.Nat Rev Microbiol, 2009, 7(4):263-273
[2] Ryjenkov DA, Tarutina M, Moskvin OV, et al. Cyclic diguanylate is a ubiquitous signaling molecule in bacteria:insights into biochemistry of the GGDEF protein domain. J Bacteriol, 2005, 187(5):1792-1798
[3] Paul R, Weiser S, Amiot NC, et al. Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev, 2004, 18(6):715-727
[4] Boehm A, Kaiser M, Li H, et al. Second messenger-mediated adjustment of bacterial swimming velocity. Cell,2010, 141(1):107-116
[5] Reinders A, Hee CS, Ozaki S, et al. Expression and genetic activation of cyclic di-GMP-specific phosphodiesterases in Escherichia coli. J Bacteriol, 2016, 198(3):448-462
[6] Tschowri N, Lindenberg S, Hengge R. Molecular function and potential evolution of the biofilm-modulating blue light-signalling pathway of Escherichia coli. Mol Microbiol, 2012, 85(5):893-906
[7] Hengge R, Galperin MY, Ghigo JM, et al. Systematic nomenclature for GGDEF and EAL domain-containing cyclic di-GMP turnover proteins of Escherichia coli. J Bacteriol, 2016, 198(1):7-11
[8] Povolotsky TL, Hengge R. Genome-based comparison of cyclic di-GMP signaling in pathogenic and commensal Escherichia coli strains. J Bacteriol, 2016, 198(1):111-126
[9] Sarenko O, Klauck G, Wilke FM, et al. More than enzymes that make or break cyclic di-GMP-local signaling in the interactome of GGDEF/EAL domain proteins of Escherichia coli. MBio, 2017, 8(5):e01639-17
[10] Tuckerman JR, Gonzalez G, Sousa EH, et al. An oxygen-sensing diguanylate cyclase and phosphodiesterase couple for c-di-GMP control. Biochemistry, 2009,48(41):9764-9774
[11] Hamblin MR, Abrahamse H. Can light-based approaches overcome antimicrobial resistance. Drug Dev Res, 2019,80(1):48-67
[12] Pfiffer V, Sarenko O, Possling A, et al. Genetic dissection of Escherichia coli's master diguanylate cyclase DgcE:role of the N-terminal MASE1 domain and direct signal input from a GTPase partner system. PLoS Genet, 2019,15(4):e1008059
[13] Chatterjee D, Cooley RB, Boyd CD, et al. Mechanistic insight into the conserved allosteric regulation of periplasmic proteolysis by the signaling molecule cyclic-diGMP. Elife, 2014, 3(1):e03650
[14] Herbst S, Lorkowski M, Sarenko O, et al. Transmembrane redox control and proteolysis of PdeC, a novel type of c-di-GMP phosphodiesterase. EMBO J, 2018, 37(8):e97825
[15] da Silva DP, Patel HK, González JF, et al. Studies on synthetic LuxR solo hybrids. Front Cell Infect Mi, 2015,5(52):1-10
[16] Sommerfeldt N, Possling A, Becker G, et al. Gene expression patterns and differential input into curli fimbriae regulation of all GGDEF/EAL domain proteins in Escherichia coli. Microbiology, 2009, 155(Pt 4):1318-1331
[17] Crépin S, Porcheron G, Houle S, et al. Altered regulation of the diguanylate cyclase YaiC reduces production of type1 fimbriae in a pst mutant of uropathogenic Escherichia coli CFT073. J Bacteriol, 2017, 199(24):e00168-17
[18] Weber H, Pesavento C, Possling A, et al. Cyclic-diGMP-mediated signalling within the sigma network of Escherichia coli. Mol Microbiol, 2006, 62(4):1014-1034
[19] Jonas K, Edwards AN, Simm R, et al. The RNA binding protein CsrA controls cyclic di-GMP metabolism by directly regulating the expression of GGDEF proteins. Mol Microbiol, 2008, 70(1):236-257
[20] Lindenberg S, Klauck G, Pesavento C, et al. The EAL domain protein YciR acts as a trigger enzyme in a c-diGMP signalling cascade in E. coli biofilm control.EMBO J, 2013, 32(14):2001-2014
[21] Tagliabue L, Maciag A, Antoniani D, et al. The yddV-dos operon controls biofilm formation through the regulation of genes encoding curli fibers'subunits in aerobically growing Escherichia coli. Fems Immunol Med Microbiol, 2010, 59(3):477-484
[22] Boehm A, Steiner S, Zaehringer F, et al. Second messenger signalling governs Escherichia coli biofilm induction upon ribosomal stress. Mol Microbiol, 2009, 72(6):1500-1516
[23] Zahringer F, Lacanna E, Jenal U, et al. Structure and signaling mechanism of a zinc-sensory diguanylate cyclase.Structure, 2013, 21(7):1149-1157
[24] Sanchez-Torres V, Hu H, Wood TK. GGDEF proteins YeaI, YedQ, and YfiN reduce early biofilm formation and swimming motility in Escherichia coli. Appl Microbiol Biotechnol, 2011, 90(2):651-658
[25] Girgis HS, Liu Y, Ryu WS, et al. A comprehensive genetic characterization of bacterial motility. PLoS Genet,2007, 3(9):1644-1660
[26] Pesavento C, Becker G, Sommerfeldt N, et al. Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli. Genes Dev, 2008, 22(17):2434-2446
[27] Kim HK, Harshey RM. A diguanylate cyclase acts as a cell division inhibitor in a two-step response to reductive and envelope stresses. MBIO J, 2016, 7(4):1-13
[28] Richter AM, Povolotsky TL, Wieler LH, et al. Cyclic-diGMP signalling and biofilm-related properties of the Shiga toxin-producing 2011 German outbreak Escherichia coli O104:H4. EMBO Mol Med, 2014, 6(12):1622-1637
[29] Petersen E, Mills E and Miller SI. Cyclic-di-GMP regulation promotes survival of a slow-replicating subpopulation of intracellular Salmonella Typhimurium. Proc Natl Acad Sci USA, 2019, 116(13):6335-6340
[30] Claret L, Miquel S, Vieille N, et al. The flagellar sigma factor FliA regulates adhesion and invasion of Crohn disease-associated Escherichia coli via a cyclic dimeric GMP-dependent pathway. J Biol Chem, 2007, 282(46):33275-33283
[31] Sundriyal A, Massa C, Samoray D, et al. Inherent regulation of EAL domain-catalyzed hydrolysis of second messenger cyclic di-GMP. J Biol Chem, 2014, 289(10):6978-6990
[32] Zlatkov N and Uhlin BE. Absence of global stress regulation in Escherichia coli promotes pathoadaptation and novel c-di-GMP-dependent metabolic capability. Sci Rep, 2019, 9(1):2600
[33] Cimdins A, Simm R, Li F, et al. Alterations of c-di-GMP turnover proteins modulate semi-constitutive rdar biofilm formation in commensal and uropathogenic Escherichia coli. Microbiologyopen, 2017, 6(5):doi:10.1002/mbo3.508
[34] Lacey MM, Partridge JD, Green J. Escherichia coli K-12YfgF is an anaerobic cyclic di-GMP phosphodiesterase with roles in cell surface remodelling and the oxidative stress response. Microbiology, 2010, 156(Pt 9):2873-2886
[35] Huang CJ, Wang ZC, Huang HY, et al. YjcC, a c-di-GMP phosphodiesterase protein, regulates the oxidative stress response and virulence of Klebsiella pneumoniae CG43.PLoS One, 2013, 8(7):e66740
[36] Brombacher E, Baratto A, Dorel C, et al. Gene expression regulation by the Curli activator CsgD protein:modulation of cellulose biosynthesis and control of negative determinants for microbial adhesion. J Bacteriol, 2006,188(6):2027-2037
[37] Jonas K, Tomenius H, Romling U, et al. Identification of YhdA as a regulator of the Escherichia coli carbon storage regulation system. Fems Microbiol Lett, 2006,264(2):232-237
[38] Wang F, Burrage AM, Postel S, et al. A structural model of flagellar filament switching across multiple bacterial species. Nat Commun, 2017, 8(1):960
[39] Imada K. Bacterial flagellar axial structure and its construction. Biophys Rev, 2018, 10(2):559-570
[40] Flemming HC, Wingender J. The biofilm matrix. Nat Rev Microbiol, 2010, 8(9):623-633
[41] Bowen WH, Burne RA, Wu H, et al. Oral biofilms:pathogens, matrix, and polymicrobial interactions in microenvironments. Trends Microbiol, 2018, 26(3):229-242
[42] Itoh Y, Rice JD, Goller C, et al. Roles of pgaABCD genes in synthesis, modification, and export of the Escherichia coli biofilm adhesin poly-beta-1,6-N-acetyl-Dglucosamine. J Bacteriol, 2008, 190(10):3670-3680
[43] Cheang QW, Xin L, Chea RYF, et al. Emerging paradigms for PilZ domain-mediated C-di-GMP signaling.Biochem Soc Trans, 2019, 47(1):381-388
[44] Agladze K, Wang X, Romeo T. Spatial periodicity of Escherichia coli K-12 biofilm microstructure initiates during a reversible, polar attachment phase of development and requires the polysaccharide adhesin PGA. J Bacteriol, 2005, 187(24):8237-8246
[45] Wang X, Preston JF, Romeo T. The pgaABCD Locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J Bacteriol,2004, 186(9):2724-2734
[46] Steiner S, Lori C, Boehm A, et al. Allosteric activation of exopolysaccharide synthesis through cyclic di-GMP-stimulated protein-protein interaction. EMBO J,2013, 32(3):354-368
[47] Czaja W, Krystynowicz A, Bielecki S, et al. Microbial cellulose--the natural power to heal wounds. Biomaterials, 2006, 27(2):145-151
[48] Beloin C, Ghigo JM. Finding gene-expression patterns in bacterial biofilms. Trends Microbiol, 2005, 13(1):16-19
[49] Serra DO, Richter AM, Hengge R. Cellulose as an architectural element in spatially structured Escherichia coli biofilms. J Bacteriol, 2013, 195(24):5540-5554
[50] Hu L, Grim CJ, Franco AA, et al. Analysis of the cellulose synthase operon genes, bcsA, bcsB, and bcsC in cronobacter species:prevalence among species and their roles in biofilm formation and cell-cell aggregation. Food Microbiol, 2015, 52(1):97-105
[51] Morgan JL, Strumillo J, Zimmer J. Crystallographic snapshot of cellulose synthesis and membrane translocation. Nature, 2013, 493(7431):181-186
[52] Fang X, Ahmad I, Blanka A, et al. GIL, a new c-di-GMPbinding protein domain involved in regulation of cellulose synthesis in enterobacteria. Mol Microbiol, 2014,93(3):439-452
[53] Tursi SA, Tükel?. Curli-containing enteric biofilms inside and out:matrix composition, immune recognition,and disease implications. Microbiol Mol Biol R, 2018,82(4):1-16
[54] Schiebel J, B?hm A, Nitschke J, et al. Genotypic and phenotypic characteristics associated with biofilm formation by human clinical Escherichia coli isolates of different pathotypes. Appl Environ Microbiol, 2017, 83(24):1-15
[55] Taylor BL, Zhulin IB. PAS domains:internal sensors of oxygen, redox potential, and light. Microbiology and molecular biology reviews:Mmbr, 1999, 63(2):479-506
[56] Mao X, Li K, Liu M, et al. Directing curli polymerization with DNA origami nucleators. Nat Commun, 2019,10(1):1-10
[57] Uhlich GA, Chen CY, Cottrell BJ, et al. Growth media and temperature effects on biofilm formation by serotype O157:H7 and non-O157 Shiga toxin-producing Escherichia coli. Fems Microbiol Lett, 2014, 354(2):133-141
[58] Gualdi L, Tagliabue L, Bertagnoli S, et al. Cellulose modulates biofilm formation by counteracting curli-mediated colonization of solid surfaces in Escherichia coli.Microbiology, 2008, 154(Pt 7):2017-2024
[59] Zhou M, Yang Y, Chen P, et al. More than a locomotive organelle:flagella in Escherichia coli. Appl Microbiol Biotechnol, 2015, 99(21):8883-8890
[60] Yuan X, Khokhani D, Wu X, et al. Cross-talk between a regulatory small RNA, cyclic-di-GMP signalling and flagellar regulator FlhDC for virulence and bacterial behaviours. Environ Microbiol, 2015, 17(11):4745-4763
[61] Santos-Zavaleta A, Perez-Rueda E, Sanchez-Perez M,et al. Tracing the phylogenetic history of the Crl regulon through the bacteria and archaea genomes. BMC Genomics, 2019, 20(1):299
[62] Kalir S, McClure J, Pabbaraju K, et al. Ordering genes in a flagella pathway by analysis of expression kinetics from living bacteria. Science, 2001, 292(5524):2080-2083
[63] Guttenplan SB, Kearns DB. Regulation of flagellar motility during biofilm formation. Fems Microbiol Rev, 2013,37(6):849-871
[64] R?mling U, Rohde M, Olsén A, et al. AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol, 2000, 36(1):10-23
[65] Makinoshima H, Aizawa SI, Hayashi H, et al. Growth phase-coupled alterations in cell structure and function of Escherichia coli. J Bacteriol, 2003, 185(4):1338-1345
[66] Shimada T, Yamazaki Y, Tanaka K, et al. The whole set of constitutive promoters recognized by RNA polymerase RpoD holoenzyme of Escherichia coli. PLoS One, 2014,9(3):e90447
[2] Ryjenkov DA, Tarutina M, Moskvin OV, et al. Cyclic diguanylate is a ubiquitous signaling molecule in bacteria:insights into biochemistry of the GGDEF protein domain. J Bacteriol, 2005, 187(5):1792-1798
[3] Paul R, Weiser S, Amiot NC, et al. Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain. Genes Dev, 2004, 18(6):715-727
[4] Boehm A, Kaiser M, Li H, et al. Second messenger-mediated adjustment of bacterial swimming velocity. Cell,2010, 141(1):107-116
[5] Reinders A, Hee CS, Ozaki S, et al. Expression and genetic activation of cyclic di-GMP-specific phosphodiesterases in Escherichia coli. J Bacteriol, 2016, 198(3):448-462
[6] Tschowri N, Lindenberg S, Hengge R. Molecular function and potential evolution of the biofilm-modulating blue light-signalling pathway of Escherichia coli. Mol Microbiol, 2012, 85(5):893-906
[7] Hengge R, Galperin MY, Ghigo JM, et al. Systematic nomenclature for GGDEF and EAL domain-containing cyclic di-GMP turnover proteins of Escherichia coli. J Bacteriol, 2016, 198(1):7-11
[8] Povolotsky TL, Hengge R. Genome-based comparison of cyclic di-GMP signaling in pathogenic and commensal Escherichia coli strains. J Bacteriol, 2016, 198(1):111-126
[9] Sarenko O, Klauck G, Wilke FM, et al. More than enzymes that make or break cyclic di-GMP-local signaling in the interactome of GGDEF/EAL domain proteins of Escherichia coli. MBio, 2017, 8(5):e01639-17
[10] Tuckerman JR, Gonzalez G, Sousa EH, et al. An oxygen-sensing diguanylate cyclase and phosphodiesterase couple for c-di-GMP control. Biochemistry, 2009,48(41):9764-9774
[11] Hamblin MR, Abrahamse H. Can light-based approaches overcome antimicrobial resistance. Drug Dev Res, 2019,80(1):48-67
[12] Pfiffer V, Sarenko O, Possling A, et al. Genetic dissection of Escherichia coli's master diguanylate cyclase DgcE:role of the N-terminal MASE1 domain and direct signal input from a GTPase partner system. PLoS Genet, 2019,15(4):e1008059
[13] Chatterjee D, Cooley RB, Boyd CD, et al. Mechanistic insight into the conserved allosteric regulation of periplasmic proteolysis by the signaling molecule cyclic-diGMP. Elife, 2014, 3(1):e03650
[14] Herbst S, Lorkowski M, Sarenko O, et al. Transmembrane redox control and proteolysis of PdeC, a novel type of c-di-GMP phosphodiesterase. EMBO J, 2018, 37(8):e97825
[15] da Silva DP, Patel HK, González JF, et al. Studies on synthetic LuxR solo hybrids. Front Cell Infect Mi, 2015,5(52):1-10
[16] Sommerfeldt N, Possling A, Becker G, et al. Gene expression patterns and differential input into curli fimbriae regulation of all GGDEF/EAL domain proteins in Escherichia coli. Microbiology, 2009, 155(Pt 4):1318-1331
[17] Crépin S, Porcheron G, Houle S, et al. Altered regulation of the diguanylate cyclase YaiC reduces production of type1 fimbriae in a pst mutant of uropathogenic Escherichia coli CFT073. J Bacteriol, 2017, 199(24):e00168-17
[18] Weber H, Pesavento C, Possling A, et al. Cyclic-diGMP-mediated signalling within the sigma network of Escherichia coli. Mol Microbiol, 2006, 62(4):1014-1034
[19] Jonas K, Edwards AN, Simm R, et al. The RNA binding protein CsrA controls cyclic di-GMP metabolism by directly regulating the expression of GGDEF proteins. Mol Microbiol, 2008, 70(1):236-257
[20] Lindenberg S, Klauck G, Pesavento C, et al. The EAL domain protein YciR acts as a trigger enzyme in a c-diGMP signalling cascade in E. coli biofilm control.EMBO J, 2013, 32(14):2001-2014
[21] Tagliabue L, Maciag A, Antoniani D, et al. The yddV-dos operon controls biofilm formation through the regulation of genes encoding curli fibers'subunits in aerobically growing Escherichia coli. Fems Immunol Med Microbiol, 2010, 59(3):477-484
[22] Boehm A, Steiner S, Zaehringer F, et al. Second messenger signalling governs Escherichia coli biofilm induction upon ribosomal stress. Mol Microbiol, 2009, 72(6):1500-1516
[23] Zahringer F, Lacanna E, Jenal U, et al. Structure and signaling mechanism of a zinc-sensory diguanylate cyclase.Structure, 2013, 21(7):1149-1157
[24] Sanchez-Torres V, Hu H, Wood TK. GGDEF proteins YeaI, YedQ, and YfiN reduce early biofilm formation and swimming motility in Escherichia coli. Appl Microbiol Biotechnol, 2011, 90(2):651-658
[25] Girgis HS, Liu Y, Ryu WS, et al. A comprehensive genetic characterization of bacterial motility. PLoS Genet,2007, 3(9):1644-1660
[26] Pesavento C, Becker G, Sommerfeldt N, et al. Inverse regulatory coordination of motility and curli-mediated adhesion in Escherichia coli. Genes Dev, 2008, 22(17):2434-2446
[27] Kim HK, Harshey RM. A diguanylate cyclase acts as a cell division inhibitor in a two-step response to reductive and envelope stresses. MBIO J, 2016, 7(4):1-13
[28] Richter AM, Povolotsky TL, Wieler LH, et al. Cyclic-diGMP signalling and biofilm-related properties of the Shiga toxin-producing 2011 German outbreak Escherichia coli O104:H4. EMBO Mol Med, 2014, 6(12):1622-1637
[29] Petersen E, Mills E and Miller SI. Cyclic-di-GMP regulation promotes survival of a slow-replicating subpopulation of intracellular Salmonella Typhimurium. Proc Natl Acad Sci USA, 2019, 116(13):6335-6340
[30] Claret L, Miquel S, Vieille N, et al. The flagellar sigma factor FliA regulates adhesion and invasion of Crohn disease-associated Escherichia coli via a cyclic dimeric GMP-dependent pathway. J Biol Chem, 2007, 282(46):33275-33283
[31] Sundriyal A, Massa C, Samoray D, et al. Inherent regulation of EAL domain-catalyzed hydrolysis of second messenger cyclic di-GMP. J Biol Chem, 2014, 289(10):6978-6990
[32] Zlatkov N and Uhlin BE. Absence of global stress regulation in Escherichia coli promotes pathoadaptation and novel c-di-GMP-dependent metabolic capability. Sci Rep, 2019, 9(1):2600
[33] Cimdins A, Simm R, Li F, et al. Alterations of c-di-GMP turnover proteins modulate semi-constitutive rdar biofilm formation in commensal and uropathogenic Escherichia coli. Microbiologyopen, 2017, 6(5):doi:10.1002/mbo3.508
[34] Lacey MM, Partridge JD, Green J. Escherichia coli K-12YfgF is an anaerobic cyclic di-GMP phosphodiesterase with roles in cell surface remodelling and the oxidative stress response. Microbiology, 2010, 156(Pt 9):2873-2886
[35] Huang CJ, Wang ZC, Huang HY, et al. YjcC, a c-di-GMP phosphodiesterase protein, regulates the oxidative stress response and virulence of Klebsiella pneumoniae CG43.PLoS One, 2013, 8(7):e66740
[36] Brombacher E, Baratto A, Dorel C, et al. Gene expression regulation by the Curli activator CsgD protein:modulation of cellulose biosynthesis and control of negative determinants for microbial adhesion. J Bacteriol, 2006,188(6):2027-2037
[37] Jonas K, Tomenius H, Romling U, et al. Identification of YhdA as a regulator of the Escherichia coli carbon storage regulation system. Fems Microbiol Lett, 2006,264(2):232-237
[38] Wang F, Burrage AM, Postel S, et al. A structural model of flagellar filament switching across multiple bacterial species. Nat Commun, 2017, 8(1):960
[39] Imada K. Bacterial flagellar axial structure and its construction. Biophys Rev, 2018, 10(2):559-570
[40] Flemming HC, Wingender J. The biofilm matrix. Nat Rev Microbiol, 2010, 8(9):623-633
[41] Bowen WH, Burne RA, Wu H, et al. Oral biofilms:pathogens, matrix, and polymicrobial interactions in microenvironments. Trends Microbiol, 2018, 26(3):229-242
[42] Itoh Y, Rice JD, Goller C, et al. Roles of pgaABCD genes in synthesis, modification, and export of the Escherichia coli biofilm adhesin poly-beta-1,6-N-acetyl-Dglucosamine. J Bacteriol, 2008, 190(10):3670-3680
[43] Cheang QW, Xin L, Chea RYF, et al. Emerging paradigms for PilZ domain-mediated C-di-GMP signaling.Biochem Soc Trans, 2019, 47(1):381-388
[44] Agladze K, Wang X, Romeo T. Spatial periodicity of Escherichia coli K-12 biofilm microstructure initiates during a reversible, polar attachment phase of development and requires the polysaccharide adhesin PGA. J Bacteriol, 2005, 187(24):8237-8246
[45] Wang X, Preston JF, Romeo T. The pgaABCD Locus of Escherichia coli promotes the synthesis of a polysaccharide adhesin required for biofilm formation. J Bacteriol,2004, 186(9):2724-2734
[46] Steiner S, Lori C, Boehm A, et al. Allosteric activation of exopolysaccharide synthesis through cyclic di-GMP-stimulated protein-protein interaction. EMBO J,2013, 32(3):354-368
[47] Czaja W, Krystynowicz A, Bielecki S, et al. Microbial cellulose--the natural power to heal wounds. Biomaterials, 2006, 27(2):145-151
[48] Beloin C, Ghigo JM. Finding gene-expression patterns in bacterial biofilms. Trends Microbiol, 2005, 13(1):16-19
[49] Serra DO, Richter AM, Hengge R. Cellulose as an architectural element in spatially structured Escherichia coli biofilms. J Bacteriol, 2013, 195(24):5540-5554
[50] Hu L, Grim CJ, Franco AA, et al. Analysis of the cellulose synthase operon genes, bcsA, bcsB, and bcsC in cronobacter species:prevalence among species and their roles in biofilm formation and cell-cell aggregation. Food Microbiol, 2015, 52(1):97-105
[51] Morgan JL, Strumillo J, Zimmer J. Crystallographic snapshot of cellulose synthesis and membrane translocation. Nature, 2013, 493(7431):181-186
[52] Fang X, Ahmad I, Blanka A, et al. GIL, a new c-di-GMPbinding protein domain involved in regulation of cellulose synthesis in enterobacteria. Mol Microbiol, 2014,93(3):439-452
[53] Tursi SA, Tükel?. Curli-containing enteric biofilms inside and out:matrix composition, immune recognition,and disease implications. Microbiol Mol Biol R, 2018,82(4):1-16
[54] Schiebel J, B?hm A, Nitschke J, et al. Genotypic and phenotypic characteristics associated with biofilm formation by human clinical Escherichia coli isolates of different pathotypes. Appl Environ Microbiol, 2017, 83(24):1-15
[55] Taylor BL, Zhulin IB. PAS domains:internal sensors of oxygen, redox potential, and light. Microbiology and molecular biology reviews:Mmbr, 1999, 63(2):479-506
[56] Mao X, Li K, Liu M, et al. Directing curli polymerization with DNA origami nucleators. Nat Commun, 2019,10(1):1-10
[57] Uhlich GA, Chen CY, Cottrell BJ, et al. Growth media and temperature effects on biofilm formation by serotype O157:H7 and non-O157 Shiga toxin-producing Escherichia coli. Fems Microbiol Lett, 2014, 354(2):133-141
[58] Gualdi L, Tagliabue L, Bertagnoli S, et al. Cellulose modulates biofilm formation by counteracting curli-mediated colonization of solid surfaces in Escherichia coli.Microbiology, 2008, 154(Pt 7):2017-2024
[59] Zhou M, Yang Y, Chen P, et al. More than a locomotive organelle:flagella in Escherichia coli. Appl Microbiol Biotechnol, 2015, 99(21):8883-8890
[60] Yuan X, Khokhani D, Wu X, et al. Cross-talk between a regulatory small RNA, cyclic-di-GMP signalling and flagellar regulator FlhDC for virulence and bacterial behaviours. Environ Microbiol, 2015, 17(11):4745-4763
[61] Santos-Zavaleta A, Perez-Rueda E, Sanchez-Perez M,et al. Tracing the phylogenetic history of the Crl regulon through the bacteria and archaea genomes. BMC Genomics, 2019, 20(1):299
[62] Kalir S, McClure J, Pabbaraju K, et al. Ordering genes in a flagella pathway by analysis of expression kinetics from living bacteria. Science, 2001, 292(5524):2080-2083
[63] Guttenplan SB, Kearns DB. Regulation of flagellar motility during biofilm formation. Fems Microbiol Rev, 2013,37(6):849-871
[64] R?mling U, Rohde M, Olsén A, et al. AgfD, the checkpoint of multicellular and aggregative behaviour in Salmonella typhimurium regulates at least two independent pathways. Mol Microbiol, 2000, 36(1):10-23
[65] Makinoshima H, Aizawa SI, Hayashi H, et al. Growth phase-coupled alterations in cell structure and function of Escherichia coli. J Bacteriol, 2003, 185(4):1338-1345
[66] Shimada T, Yamazaki Y, Tanaka K, et al. The whole set of constitutive promoters recognized by RNA polymerase RpoD holoenzyme of Escherichia coli. PLoS One, 2014,9(3):e90447