Clp is a “busy” transcription factor in the bacterial warrior, Lysobacter enzymogenes

Zheng, 2004, Identification of the CRP regulon using in vitro and in vivo transcriptional profiling, Nucleic Acids Res, 32, 5874, 10.1093/nar/gkh908 Serate, 2011, Ligand responses of Vfr, the virulence factor regulator from Pseudomonas aeruginosa, J Bacteriol, 193, 4859, 10.1128/JB.00352-11 Gunasekera, 1992, DNA sequence determinants for binding of the Escherichia coli catabolite gene activator protein, J Biol Chem, 267, 14713, 10.1016/S0021-9258(18)42099-6 Gosset, 2004, Transcriptome analysis of Crp-dependent catabolite control of gene expression in Escherichia coli, J Bacteriol, 186, 3516, 10.1128/JB.186.11.3516-3524.2004 Fuchs, 2010, The Pseudomonas aeruginosa Vfr regulator controls global virulence factor expression through cyclic AMP-dependent and -independent mechanisms, J Bacteriol, 192, 3553, 10.1128/JB.00363-10 Beatson, 2002, Differential regulation of twitching motility and elastase production by Vfr in Pseudomonas aeruginosa, J Bacteriol, 184, 3605, 10.1128/JB.184.13.3605-3613.2002 Dasgupta, 2002, fleQ, the gene encoding the major flagellar regulator of Pseudomonas aeruginosa, is sigma70 dependent and is downregulated by Vfr, a homolog of Escherichia coli cyclic AMP receptor protein, J Bacteriol, 184, 5240, 10.1128/JB.184.19.5240-5250.2002 Zhang, 2016, Role of Vfr in the regulation of antifungal compound production by Pseudomonas fluorescens FD6, Microbiol Res, 188-189, 106, 10.1016/j.micres.2016.04.013 Zhang, 2019, Glutathione activates type III secretion system through Vfr in Pseudomonas aeruginosa, Front Cell Infect Microbiol, 9, 10.3389/fcimb.2019.00164 Albus, 1997, Vfr controls quorum sensing in Pseudomonas aeruginosa, J Bacteriol, 179, 3928, 10.1128/jb.179.12.3928-3935.1997 He YW, Ng AY, Xu M, Lin K, Wang LH, et al. Xanthomonas campestris cell-cell communication involves a putative nucleotide receptor protein Clp and a hierarchical signalling network. Mol Microbiol 2007;64:281–92. Chin, 2010, The cAMP receptor-like protein Clp is a novel c-di-GMP receptor linking cell-cell signaling to virulence gene expression in Xanthomonas campestris, J Mol Biol, 396, 646, 10.1016/j.jmb.2009.11.076 Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M, et al. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol Plant Pathol 2012;13:614–29. Leduc, 2009, Cyclic di-GMP allosterically inhibits the CRP-like protein (Clp) of Xanthomonas axonopodis pv. citri, J Bacteriol, 191, 7121, 10.1128/JB.00845-09 Tao, 2010, The cyclic nucleotide monophosphate domain of Xanthomonas campestris global regulator Clp defines a new class of cyclic di-GMP effectors, J Bacteriol, 192, 1020, 10.1128/JB.01253-09 Ross, 1987, Regulation of cellulose synthesis in Acetobacter xylinum by cyclic diguanylic acid, Nature, 325, 279, 10.1038/325279a0 Römling, 2013, Cyclic di-GMP: the first 25 years of a universal bacterial second messenger, Microbiol Mol Biol Rev, 77, 1, 10.1128/MMBR.00043-12 Chou, 2016, Diversity of cyclic di-GMP-binding proteins and mechanisms, J Bacteriol, 198, 32, 10.1128/JB.00333-15 Jain R, Sliusarenko O, Kazmierczak BI. Interaction of the cyclic-di-GMP binding protein FimX and the Type 4 pilus assembly ATPase promotes pilus assembly. PLoS Pathog 2017;13:e1006594. Paul, 2004, Cell cycle-dependent dynamic localization of a bacterial response regulator with a novel di-guanylate cyclase output domain, Genes Dev, 18, 715, 10.1101/gad.289504 Ryjenkov, 2005, Cyclic diguanylate is a ubiquitous signaling molecule in bacteria: insights into biochemistry of the GGDEF protein domain, J Bacteriol, 187, 1792, 10.1128/JB.187.5.1792-1798.2005 Schmidt, 2005, The ubiquitous protein domain EAL is a cyclic diguanylate-specific phosphodiesterase: enzymatically active and inactive EAL domains, J Bacteriol, 187, 4774, 10.1128/JB.187.14.4774-4781.2005 Christen, 2005, Identification and characterization of a cyclic di-GMP-specific phosphodiesterase and its allosteric control by GTP, J Biol Chem, 280, 30829, 10.1074/jbc.M504429200 Bellini, 2014, Crystal structure of an HD-GYP domain cyclic-di-GMP phosphodiesterase reveals an enzyme with a novel trinuclear catalytic iron centre, Mol Microbiol, 91, 26, 10.1111/mmi.12447 He YW, Xu M, Lin K, Ng YJ, Wen CM, et al. Genome scale analysis of diffusible signal factor regulon in Xanthomonas campestris pv. campestris: identification of novel cell-cell communication-dependent genes and functions. Mol Microbiol 2006;59:610–22. Barber, 1997, A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule, Mol Microbiol, 24, 555, 10.1046/j.1365-2958.1997.3721736.x He, 2008, Quorum sensing and virulence regulation in Xanthomonas campestris, FEMS Microbiol Rev, 32, 842, 10.1111/j.1574-6976.2008.00120.x Slater, 2000, A two-component system involving an HD-GYP domain protein links cell-cell signalling to pathogenicity gene expression in Xanthomonas campestris, Mol Microbiol, 38, 986, 10.1046/j.1365-2958.2000.02196.x Cai, 2017, Fatty acid DSF binds and allosterically activates histidine kinase RpfC of phytopathogenic bacterium Xanthomonas campestris pv. campestris to regulate quorum-sensing and virulence, PLoS Pathog, 13, e1006304, 10.1371/journal.ppat.1006304 Christensen, 1978, Lysobacter, a new genus of nonfruiting, gliding bacteria with a high base ratio, Int J Syst Evol Microbiol, 28, 367 Puopolo, 2018, The impact of the omics era on the knowledge and use of Lysobacter species to control phytopathogenic micro-organisms, J Appl Microbiol, 124, 15, 10.1111/jam.13607 Panthee, 2016, Lysobacter species: a potential source of novel antibiotics, Arch Microbiol, 198, 839, 10.1007/s00203-016-1278-5 de Bruijn, 2015, Comparative genomics and metabolic profiling of the genus Lysobacter, BMC Genom, 16, 10.1186/s12864-015-2191-z Zhao, 2016, Heterocyclic aromatic N-oxidation in the biosynthesis of phenazine antibiotics from Lysobacter antibioticus, Org Lett, 18, 2495, 10.1021/acs.orglett.6b01089 Ling, 2019, LbDSF, the Lysobacter brunescens quorum-sensing system diffusible signaling factor, regulates anti- Xanthomonas XSAC biosynthesis, colony morphology, and surface motility, Front Microbiol, 10, 10.3389/fmicb.2019.01230 Puopolo, 2014, Lysobacter capsici AZ78 produces cyclo(L-Pro-L-Tyr), a 2,5-diketopiperazine with toxic activity against sporangia of Phytophthora infestans and Plasmopara viticola, J Appl Microbiol, 117, 1168, 10.1111/jam.12611 Laborda, 2018, ACC deaminase from Lysobacter gummosus OH17 can promote root growth in Oryza sativa nipponbare plants, J Agric Food Chem, 66, 3675, 10.1021/acs.jafc.8b00063 Xie, 2012, Bioactive natural products from Lysobacter, Nat Prod Rep, 29, 1277, 10.1039/c2np20064c Qian, 2009, Identification and characterization of Lysobacter enzymogenes as a biological control agent against some fungal pathogens, Agr Sci China, 8, 68, 10.1016/S1671-2927(09)60010-9 Qian, 2012, Selection of available suicide vectors for gene mutagenesis using chiA (a chitinase encoding gene) as a new reporter and primary functional analysis of chiA in Lysobacter enzymogenes strain OH11, World J Microbiol Biotechnol, 28, 549, 10.1007/s11274-011-0846-8 Fulano, 2020, The homologous components of flagellar type III protein apparatus have acquired a novel function to control twitching motility in a non-flagellated biocontrol bacterium, Biomolecules, 10, 733, 10.3390/biom10050733 Fulano, 2020, Functional divergence of flagellar type III secretion system: a case study in a non-flagellated, predatory bacterium, Comput Struct Biotechnol J, 18, 3368, 10.1016/j.csbj.2020.10.029 Xia, 2018, Type IV pilus biogenesis genes and their roles in biofilm formation in the biological control agent Lysobacter enzymogenes OH11, Appl Microbiol Biotechnol, 102, 833, 10.1007/s00253-017-8619-4 Lin, 2020, A non-flagellated biocontrol bacterium employs a PilZ-PilB complex to provoke twitching motility associated with its predation behavior, Phytopathol Res, 2, 10.1186/s42483-020-00054-x Kobayashi, 2005, A clp gene homologue belonging to the Crp gene family globally regulates lytic enzyme production, antimicrobial activity, and biological control activity expressed by Lysobacter enzymogenes strain C3, Appl Environ Microbiol, 71, 261, 10.1128/AEM.71.1.261-269.2005 Li, 2006, Distinct ceramide synthases regulate polarized growth in the filamentous fungus Aspergillus nidulans, Mol Biol Cell, 17, 1218, 10.1091/mbc.e05-06-0533 Yu, 2007, Structure and biosynthesis of heat-stable antifungal factor (HSAF), a broad-spectrum antimycotic with a novel mode of action, Antimicrob Agents Chemother, 51, 64, 10.1128/AAC.00931-06 Qian, 2013, Lysobacter enzymogenes uses two distinct cell-cell signaling systems for differential regulation of secondary-metabolite biosynthesis and colony morphology, Appl Environ Microb, 79, 6604, 10.1128/AEM.01841-13 Kobayashi, 2005, The role of clp-regulated factors in antagonism against Magnaporthe poae and biological control of summer patch disease of Kentucky bluegrass by Lysobacter enzymogenes C3, Can J Microbiol, 51, 719, 10.1139/w05-056 Zhao, 2017, Transcriptional and antagonistic responses of biocontrol strain Lysobacter enzymogenes OH11 to the plant pathogenic oomycete Pythium aphanidermatum, Front Microbiol, 8, 1025, 10.3389/fmicb.2017.01025 Wang, 2014, Transcriptomic analysis reveals new regulatory roles of Clp signaling in secondary metabolite biosynthesis and surface motility in Lysobacter enzymogenes OH11, Appl Microbiol Biotechnol, 98, 9009, 10.1007/s00253-014-6072-1 Wang, 2017, LetR is a TetR family transcription factor from Lysobacter controlling antifungal antibiotic biosynthesis, Appl Microbiol Biotechnol, 101, 3273, 10.1007/s00253-017-8117-8 Chen, 2018, Two direct gene targets contribute to Clp-dependent regulation of type IV pilus-mediated twitching motility in Lysobacter enzymogenes OH11, Appl Microbiol Biotechnol, 102, 7509, 10.1007/s00253-018-9196-x Xu GG, Han S, Huo CM, Chin KH, Chou SH, et al. Signaling specificity in the c-di-GMP-dependent network regulating antibiotic synthesis in Lysobacter. Nucleic Acids Res 2018;46:9276–88. Xu, 2016, Direct regulation of extracellular chitinase production by the transcription factor Le Clp in Lysobacter enzymogenes OH11, Phytopathology, 106, 971, 10.1094/PHYTO-01-16-0001-R Ren, 2020, Knockout of diguanylate cyclase genes in Lysobacter enzymogenes to improve production of antifungal factor and increase its application in seed coating, Curr Microbiol, 77, 1006, 10.1007/s00284-020-01902-x Han, 2015, Identification of a small molecule signaling factor that regulates the biosynthesis of the antifungal polycyclic tetramate macrolactam HSAF in Lysobacter enzymogenes, Appl Microbiol Biotechnol, 99, 801, 10.1007/s00253-014-6120-x Ryan, 2011, Communication with a growing family: diffusible signal factor (DSF) signaling in bacteria, Trends Microbiol, 19, 145, 10.1016/j.tim.2010.12.003 Gevrekci, 2017, The roles of polyamines in microorganisms, World J Microbiol Biotechnol, 33, 204, 10.1007/s11274-017-2370-y Zhao, 2019, Spermidine plays a significant role in stabilizing a master transcription factor Clp to promote antifungal activity in Lysobacter enzymogenes, Appl Microbiol Biotechnol, 103, 1811, 10.1007/s00253-018-09596-9 Hobley, 2017, Spermidine promotes Bacillus subtilis biofilm formation by activating expression of the matrix regulator slrR, J Biol Chem, 292, 12041, 10.1074/jbc.M117.789644 Xu K, Shen D, Yang N, Chou SH, Gomelsky M, et al. (2021) Coordinated control of the type IV pili and c-di-GMP-dependent antifungal antibiotic production in Lysobacter by the response regulator PilR. Mol Plant Pathol. In press. Mougous, 2006, A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus, Science, 312, 1526, 10.1126/science.1128393 Hachani, 2016, Type VI secretion and anti-host effectors, Curr Opin Microbiol, 29, 81, 10.1016/j.mib.2015.11.006 Galán, 2018, Protein-injection machines in bacteria, Cell, 172, 1306, 10.1016/j.cell.2018.01.034 Hernandez, 2020, Type VI secretion system effector proteins: effective weapons for bacterial competitiveness, Cell Microbiol, 22, e13241, 10.1111/cmi.13241 Liang, 2019, An onboard checking mechanism ensures effector delivery of the type VI secretion system in Vibrio cholerae, Proc Natl Acad Sci U S A, 116, 23292, 10.1073/pnas.1914202116 Yang, 2020, An intrinsic mechanism for coordinated production of the contact-dependent and contact-independent weapon systems in a soil bacterium, PLoS Pathog, 16, e1008967, 10.1371/journal.ppat.1008967