Research Progress on Microbial Quorum Quenching Enzymes and Their Control of Plant Diseases

doi:10.13560/j.cnki.biotech.bull.1985.2017-0223

Abstract

Abstract: The phenomenon of information exchanging through signal molecules between microbial cells is the Quorum Sensing（QS）. QS is widely present in microorganisms，and can modulate the expression of specific genes，especially virulence factors in pathogenic microorganisms. Quorum Quenching（QQ）is a new therapeutic strategy of plant diseases based on QS. QQ can be achieved by interfering QS from inhibiting the synthesis or detection of the signal molecules，or by enzyme-catalyzed degradation or modification of the signal molecules. Degrading signal molecules by using QQ enzymes is one of the most effective and nontoxic ways of QQ. So far，QQ enzymes of various microbial signaling molecules have been reported，especially N-acyl homoserine lactones（AHLs）and cis-11-methyl-2-dodecenoic acid were deeply investigated. In this review，we summarize and analyze the research status，deficiencies and the future development of QQ enzymes and their control of plant diseases，for laying a solid foundation for developing new，green and safe measures of disease control.

Key words: quorum sensing, quorum quenching enzymes, N-acyl homoserine lactones, cis-11-methyl-2-dodecenoic acid

FAN Xing-hui, WANG Hui-shan HE, Jie-hua YE, Tian YANG, Fang CHEN Shao-hua. Research Progress on Microbial Quorum Quenching Enzymes and Their Control of Plant Diseases[J]. Biotechnology Bulletin, 2017, 33(10): 80-87.

References

[1]Nealson KH. Autoinduction of bacterial luciferase. Occurrence, mechanism and significance[J]. Archives of Microbiology, 1977, 112(1)：73-79.
[2]Nealson KH, Platt T, Hastings JW. Cellular control of the synthesis and activity of the bacterial luminescent system[J]. Journal of Bacteriology, 1970, 104(1)：313-322.
[3]Davies DG, Parsek MR, Pearson JP, et al. The involvement of cell-to-cell signals in the development of a bacterial biofilm[J]. Science, 1998, 280(5361)：295-298.
[4]Fuqua WC, Winans SC, Greenberg EP. Quorum sensing in bacteria：the LuxR-LuxI family of cell density-responsive transcriptional regulators[J]. Journal of Bacteriology, 1994, 176(2)：269-275.
[5]Brameyer S, Kresovic D, Bode HB, et al. Dialkylresorcinols as bacterial signaling molecules[J]. Proc Natl Acad Sci USA, 2015, 112(2)：572-577.
[6]Brameyer S, Bode HB, Heermann R. Languages and dialects：bacterial communication beyond homoserine lactones[J]. Trends in Microbiology, 2015, 23(9)：521-523.
[7]Yates EA, Philipp B, Buckley C, et al. N-acylhomoserine lactones undergo lactonolysis in a pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa[J]. Infection and Immunity, 2002, 70(10)：5635-5646.
[8]Park SY, Lee SJ, Oh TK, et al. AhlD, an N-acylhomoserine lactonase in Arthrobacter sp. , and predicted homologues in other bacteria[J]. Microbiology-Sgm, 2003, 149(6)：1541-1550.
[9]邱健, 贾振华, 马宏, 等. 一株降解N-酰基高丝氨酸内酯酵母菌菌株的分离鉴定及其降解特性[J]. 微生物学报, 2007, 2：355-358.
[10]罗利龙. 红冬孢酵母中Ahl降解酶的分离纯化[D]. 天津：河北工业大学, 2010.
[11]Bar-Rogovsky H, Hugenmatter A, Tawfik DS. The evolutionary origins of detoxifying enzymes：the mammalian serum paraoxonases(PONs)relate to bacterial homoserine lactonases[J]. Journal of Biological Chemistry, 2013, 288(33)：23914-23927.
[12]Eberhard A, Burlingame AL, Eberhard C, et al. Structural identification of autoinducer of Photobacterium fischeri luciferase[J]. Biochemistry, 1981, 20(9)：2444-2449.
[13]Zhang G, Zhang F, Ding G, et al. Acyl homoserine lactone-based quorum sensing in a Methanogenic archaeon[J]. ISME Journal, 2012, 6(7)：1336-1344.
[14]Ahlgren NA, Harwood CS, Schaefer AL, et al. Aryl-homoserine lactone quorum sensing in stem-nodulating photosynthetic bradyrhizobia[J]. Proc Natl Acad Sci USA, 2011, 108(17)：7183-7188.
[15]Lindemann A, Pessi G, Schaefer AL, et al. Isovaleryl-homoserine lactone, an unusual branched-chain quorum-sensing signal from the soybean symbiont Bradyrhizobium japonicum[J]. Proc Natl Acad Sci USA, 2011, 108(40)：16765-16770.
[16]Schaefer AL, Greenberg EP, Oliver CM, et al. A new class of homoserine lactone quorum-sensing signals[J]. Nature, 2008, 454(7204)：595-596.
[17]Dong Y, Xu J, Li X, et al. AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia Carotovora[J]. Proc Natl Acad Sci USA, 2000, 97(7)：3526-3531.
[18]Leadbetter JR, Greenberg EP. Metabolism of acyl-homoserine lactone quorum-sensing signals by Variovorax Paradoxus[J]. Journal of Bacteriology, 2000, 182(24)：6921-6926.
[19]Xue B, Chow JY, Baldansuren A, et al. Structural evidence of a productive active site architecture for an evolved quorum-quenching GKL lactonase[J]. Biochemistry, 2013, 52(13)：2359-2370.
[20] See-Too WS, Ee R, Lim Y, et al. AidP, a novel N-acyl homoserine lactonase gene from antarctic Planococcus sp[J]. Scientific Reports, 2017, 7：42968.
[21] Zhang HB, Wang LH, Zhang LH. Genetic control of quorum-sensing signal turnover in Agrobacterium tumefaciens[J]. Proc Natl Acad Sci USA, 2002, 99(7)：4638-4643.
[22] Tang K, Su Y, Brackman G, et al. MomL, a novel marine-derived N-acyl homoserine lactonase from Muricauda Olearia[J]. Appl Environ Microbiol, 2015, 81(2)：774-782.
[23] Wang W, Morohoshi T, Someya N, et al. AidC, a novel N-acylhomoserine lactonase from the potato root-associated cytophaga-flavobacteria-bacteroides(CFB)group bacterium Chryseobacterium sp. strain StRB126[J]. Appl Environ Microbiol, 2012, 78(22)：7985-7992.
[24]Morohoshi T, Tominaga Y, Someya N, et al. Complete genome sequence and characterization of the N-acylhomoserine lactone-degrading gene of the potato leaf-associated Solibacillus silvestris[J]. Journal of Bioscience and Bioengineering, 2012, 113(1)：20-25.
[25]Krysciak D, Schmeisser C, Preuss S, et al. Involvement of multiple loci in quorum quenching of autoinducer l molecules in the nitrogen-fixing symbiont Rhizobium(Sinorhizobium)sp. strain NGR234[J]. Appl Environ Microbiol, 2011, 77(15)：5089-5099.
[26]Riaz K, Elmerich C, Raffoux A, et al. Metagenomics revealed a quorum quenching lactonase QlcA from yet unculturable soil bacteria[J]. Communications in Agricultural and Applied Biological Sciences, 2008, 73(2)：3-6.
[27]Chow JY, Wu L, Yew WS. Directed evolution of a quorum-quenching lactonase from Mycobacterium avium subsp. paratuberculosis K-10 in the amidohydrolase superfamily[J]. Biochemistry, 2009, 48(20)：4344-4353.
[28]Hong K, Koh C, Sam C, et al. Quorum quenching revisited-from signal decays to signalling confusion[J]. Sensors, 2012, 12(4)：4661-4696.
[29]Afriat L, Roodveldt C, Manco G, et al. The latent promiscuity of newly identified microbial lactonases is linked to a recently diverged phosphotriesterase[J]. Biochemistry, 2006, 45(46)：13677-13686.
[30]Hiblot J, Gotthard G, Chabriere E, et al. Structural and enzymatic characterization of the lactonase SisLac from Sulfolobus islandicus[J]. PLoS One, 2012, 7：e4702810.
[31]Park SY, Hwang BJ, Shin MH, et al. N-acylhomoserine lactonase producing Rhodococcus spp. with different AHL-degrading activities[J]. FEMS Microbiology Letters, 2006, 261(1)：102-108.
[32]Wang W, Morohoshi T, Ikenoya M, et al. AiiM, a novel class of N-acylhomoserine lactonase from the leaf-associated bacterium Microbacterium testaceum[J]. Appl Environ Microbiol, 2010, 76(8)：2524-2530.
[33]Mei G, Yan X, Turak A, et al. AidH, an alpha/beta-hydrolase fold family member from an Ochrobactrum sp. strain, is a novel N-acylhomoserine lactonase[J]. Appl Environ Microbiol, 2010, 76(15)：4933-4942.
[34]Schipper C, Hornung C, Bijtenhoorn P, et al. Metagenome-derived clones encoding two novel lactonase family proteins involved in biofilm inhibition in Pseudomonas aeruginosa[J]. Appl Environ Microbiol, 2009, 75(1)：224-233.
[35]Garge SS, Nerurkar AS. Attenuation of quorum sensing regulated virulence of Pectobacterium carotovorum subsp. carotovorum through an AHL lactonase produced by Lysinibacillus sp. Gs50[J]. PLoS One, 2016, 11：e016734412.
[36]Harel M, Aharoni A, Gaidukov L, et al. Structure and evolution of the serum paraoxonase family of detoxifying and anti-atheroscleroticenzymes[J]. Nature Structural & Molecular Biology, 2004, 11(12)：1253.
[37]Park SY, Kang HO, Jang HS, et al. Identification of extracellular N-acylhomoserine lactone acylase from a Streptomyces sp. and its application to quorum quenching[J]. Appl Environ Microbiol, 2005, 71(5)：2632-2641.
[38]Romero M, Diggle SP, Heeb S, et al. Quorum quenching activity in Anabaena sp. PCC 7120：Identification of AiiC, a novel AHL-acylase[J]. FEMS Microbiology Letters, 2008, 280(1)：73-80.
[39]Lin YH, Xu JL, Hu JY, et al. Acyl-homoserine lactone acylase from Ralstonia strain XJ12B represents a novel and potent class of quorum-quenching enzymes[J]. Molecular Microbiology, 2003, 47(3)：849-860.
[40]Huang JJ, Han JI, Zhang LH, et al. Utilization of acyl-homoserine lactone quorum signals for growth by a soil pseudomonad and Pseudomonas aeruginosa PAO1[J]. Appl Environ Microbiol, 2003, 69(10)：5941-5949.
[41]Morohoshi T, Nakazawa S, Ebata A, et al. Identification and characterization of N-acylhomoserine lactone-acylase from the fish intestinal Shewanella sp. strain MIB015[J]. Bioscience Biotechnology and Biochemistry, 2008, 72(7)：1887-1893.
[42]Chen C, Chen C, Liao C, et al. A probable aculeacin a acylase from the Ralstonia solanacearum GMI1000 is N-acyl-homoserine lactone acylase with quorum-quenching activity[J]. BMC Microbiology, 2009, 9：89.
[43]Huang JJ, Petersen A, Whiteley M, et al. Identification of QuiP, the product of gene PA1032, as the second acyl-homoserine lactone acylase of Pseudomonas aeruginosa PAO1[J]. Appl Environ Microbiol, 2006, 72(2)：1190-1197.
[44]Shepherd RW, Lindow SE. Two dissimilar N-acyl-homoserine lactone acylases of Pseudomonas syringae influence colony and biofilm morphology[J]. Appl Environ Microbiol, 2009, 75(1)：45-53.
[45]Terwagne M, Mirabella A, Lemaire J, et al. Quorum sensing and self-quorum quenching in the intracellular pathogen Brucellamelitensis[J]. PLoS One, 2013, 8：e8251412.
[46]Czajkowski R, Krzyzanowska D, Karczewska J, et al. Inactivation of AHLs by Ochrobactrum sp. A44 depends on the activity of a novel class of AHL acylase[J]. Environ Microbiol Reports, 2011, 3(1)：59-68.
[47]Maisuria VB, Nerurkar AS. Interference of quorum sensing by Delftia sp. VM4 depends on the activity of a novel N-acylhomoserine lactone-acylase[J]. PLoS One, 2015, 10(9)：e138034.
[48]Nasuno E, Suzuki T, Suzuki R, et al. Novel quorum quenching enzymes identified from draft genome of Roseomonas sp. TAS13[J]. Genomics Data, 2017, 12：22-23.
[49]Sunder AV, Utari PD, Ramasamy S, et al. Penicillin V acylases from gram-negative bacteria degrade N-acylhomoserine lactones and attenuate virulence in Pseudomonas aeruginosa[J]. Applied Microbiology and Biotechnology, 2017, 6(101)：2383-2395.
[50]Chowdhary PK, Keshavan N, Nguyen HQ, et al. Bacillus megaterium CYP102A1 oxidation of acyl homoserine lactones and acyl homoserines[J]. Biochemistry, 2007, 46(50)：14429-14437.
[51]Uroz S, Chhabra SR, Camara M, et al. N-acylhomoserine lactone quorum-ssensing molecules are modified and degraded by Rhodococcus erythropolis W2 by both amidolytic and novel oxidoreductase activities[J]. Microbiology-SGM, 2005, 151(10)：3313-3322.
[52]Chan K, Atkinson S, Mathee K, et al. Characterization of N-acylhomoserine lactone-degrading bacteria associated with the Zingiber officinale(Ginger)rhizosphere：co-existence of quorum quenching and quorum sensing in Acinetobacter and Burkholderia[J]. BMC Microbiology, 2011, 11：51.
[53]Barber CE, Tang JL, Feng JX, et al. A novel regulatory system required for pathogenicity of Xanthomonas campestris is mediated by a small diffusible signal molecule[J]. Molecular Microbiology, 1997, 24(3)：555-566.
[54]Wang LH, He YW, Gao YF, et al. A bacterial cell-cell communication signal with cross-kingdom structural analogues[J]. Mol Microbiol, 2004, 51(3)：903-912.
[55]Newman KL, Chatterjee S, Ho KA, et al. Virulence of plant pathogenic bacteria attenuated by degradation of fatty acid cell-to-cell signaling factors[J]. Molecular Plant-Microbe Interactions, 2008, 21(3)：326-334.
[56]Caicedo JC, Villamizar S, Ferro MIT, et al. Bacteria from the citrus phylloplane can disrupt cell-cell signalling in Xanthomonas citri and reduce citrus canker disease severity[J]. Plant Pathology, 2016, 65(5)：782-791.
[57]Pustelny C, Albers A, Bueldt-Karentzopoulos K, et al. Dioxygenase-mediated quenching of quinolone-dependent quorum sensing in Pseudomonas aeruginosa[J]. Chemistry & Biology, 2009, 16(12)：1259-1267.
[58]Soh EY, Chhabra SR, Halliday N, et al. Biotic inactivation of the Pseudomonas aeruginosa quinolone signal molecule[J]. Environ Microbiol, 2015, 17(11)：4352-4365.
[59]Mueller C, Birmes FS, Rueckert C, et al. Rhodococcus erythropolis BG43 genes mediating Pseudomonas aeruginosa quinolone signal degradation and virulence factor attenuation[J]. Appl Environ Microbiol, 2015, 81(22)：7720-7729.
[60]Ma R, Qiu S, Jiang Q, et al. AI-2 quorum sensing negatively regulates rbf expression and biofilm formation in Staphylococcus aureus[J]. Int J Med Microbiol, 2017, 307(4-5)：257：267.
[61]Roy V, Fernandes R, Tsao C, et al. Cross species quorum quenching using a native AI-2 processing enzyme[J]. ACS Chemical Biology, 2010, 5(2)：223-232.
[62]Weiland-Braeuer N, Kisch MJ, Pinnow N, et al. Highly effective inhibition of biofilm formation by the first metagenome-derived Al-2 quenching enzyme[J]. Front Microbiol, 2016, 7：1098.
[63]Shinohara M, Nakajima N, Uehara Y. Purification and characterization of a novel esterase(beta-hydroxypalmitate methyl ester hydrolase)and prevention of the expression of virulence by Ralstonia solanacearum[J]. J Appl Microbiol, 2007, 1：152-162.
[64]Achari GA, Ramesh R. Characterization of bacteria degrading 3-hydroxy palmitic acid methyl ester(3OH-PAME), a quorum sensing molecule of Ralstonia solanacearum[J]. Letters in Applied Microbiology, 2015, 60(5)：447-455.