Abstract
Quorum sensing is a system of stimuli and response correlated to population density and involves in pathogen infection, colonization, and pathogenesis. Quorum quenching enzymes as quorum sensing inhibitors have been identified in a number of bacteria and been used to control by triggering the pathogenic phenotype. The marine bacteria of Pseudoalteromonas had wide activity of degrading AHLs as a type of signal molecule associated with quorum sensing. We screened many Pseudoalteromonas strains in large scale to explore genes of quorum quenching enzymes from the China seas by whole-genome sequencing rather than genomic library construction. Nine target strains were obtained and an acylases gene APTM01 from the strain MQS005 belonging to PvdQ type on sub-branch in phylogenetic tree. And the heterogenous host containing the vector with target gene could degrade C10-HSL, C12-HSL and OC12-HSL. The obtained AHL acylase gene would be a candidate quorum quenching gene to apply in some fields. We identified that the strains of Pseudoalteromonas have wide AHL-degrading ability depending on quorum quenching. The strains would be a resource to explore new quorum quenching enzymes.
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References
Jayaraman A, Wood TK (2008) Bacterial quorum sensing: signals, circuits, and implications for biofilms and disease. Annu Rev Biomed Eng 10:145–167. https://doi.org/10.1146/annurev.bioeng.10.061807.160536
Fuqua C, Greenberg EP (2002) Listening in on bacteria: acyl-homoserine lactone signalling. Nat Rev Mol Cell Biol 3:685–695. https://doi.org/10.1038/nrm907
Taga ME, Bassler BL (2003) Chemical communication among bacteria. Proc Natl Acad Sci USA 100(Suppl):14549–14554. https://doi.org/10.1073/pnas.1934514100
Chapalain A, Vial L, Laprade N et al (2013) Identification of quorum sensing-controlled genes in Burkholderia ambifaria. Microbiologyopen 2:226–242. https://doi.org/10.1002/mbo3.67
Whiteley M, Lee KM, Greenberg EP (1999) Identification of genes controlled by quorum sensing in Pseudomonas aeruginosa. Proc Natl Acad Sci USA 96:13904–13909. https://doi.org/10.1073/pnas.96.24.13904
Schuster M (2011) Global expression analysis of quorum-sensing controlled genes. Methods Mol Biol 692:173–187. https://doi.org/10.1007/978-1-60761-971-0_13
Jimenez JC, Federle MJ (2014) Quorum sensing in group A Streptococcus. Front Cell Infect Microbiol 4:127. https://doi.org/10.3389/fcimb.2014.00127
Case RJ, Labbate M, Kjelleberg S (2008) AHL-driven quorum-sensing circuits: their frequency and function among the Proteobacteria. ISME J 2:345–349. https://doi.org/10.1038/ismej.2008.13
Smith R (2003) P. aeruginosa quorum-sensing systems and virulence. Curr Opin Microbiol 6:56–60. https://doi.org/10.1016/s1369-5274(03)00008-0
Devescovi G, Bigirimana J, Degrassi G et al (2007) Involvement of a quorum-sensing-regulated lipase secreted by a clinical isolate of Burkholderia glumae in severe disease symptoms in rice. Appl Environ Microbiol 73:4950–4958. https://doi.org/10.1128/AEM.00105-07
Hentzer M, Wu H, Andersen JB et al (2003) Attenuation of Pseudomonas aeruginosa virulence by quorum sensing inhibitors. EMBO J 22:3803–3815. https://doi.org/10.1093/emboj/cdg366
Wang WZ, Morohoshi T, Ikenoya M et al (2010) AiiM, a novel class of N-acylhomoserine lactonase from the leaf-associated bacterium Microbacterium testaceum. Appl Environ Microbiol 76:2524–2530. https://doi.org/10.1128/AEM.02738-09
Huang JJ, Han JI, Zhang LH, Leadbetter JR (2003) Utilization of acyl-homoserine lactone quorum signals for growth by a soil pseudomonad and Pseudomonas aeruginosa PAO1. Appl Environ Microbiol 69:5941–5949. https://doi.org/10.1128/Aem.69.10.5941-5949.2003
Czajkowski R, Jafra S (2009) Quenching of acyl-homoserine lactone-dependent quorum sensing by enzymatic disruption of signal molecules. Acta Biochim Pol 56:1–16
Chen F, Gao Y, Chen X et al (2013) Quorum quenching enzymes and their application in degrading signal molecules to block quorum sensing-dependent infection. Int J Mol Sci 14:17477–17500. https://doi.org/10.3390/ijms140917477
Estin ML, Stoltz DA, Zabner J (2010) Paraoxonase 1, quorum sensing, and P. aeruginosa infection: a novel model. Adv Exp Med Biol 660:183–193. https://doi.org/10.1007/978-1-60761-350-3_17
Dong YH, Xu JL, Li XZ, Zhang LH (2000) AiiA, an enzyme that inactivates the acylhomoserine lactone quorum-sensing signal and attenuates the virulence of Erwinia carotovora. Proc Natl Acad Sci USA 97:3526–3531. https://doi.org/10.1073/pnas.060023897
Pirhonen M, Flego D, Heikinheimo R, Palva ET (1993) A small diffusible signal molecule is responsible for the global control of virulence and exoenzyme production in the plant pathogen Erwinia carotovora. EMBO J 12:2467–2476
Von Bodman SB, Bauer WD, Coplin DL (2003) Quorum sensing in plant-pathogenic bacteria. Annu Rev Phytopathol 41:455–482. https://doi.org/10.1146/annurev.phyto.41.052002.095652
Dong YH, Gusti AR, Zhang Q et al (2002) Identification of quorum-quenching N-acyl homoserine lactonases from Bacillus species. Appl Environ Microbiol 68:1754–1759. https://doi.org/10.1128/AEM.68.4.1754-1759.2002
Wang WZ, Morohoshi T, Someya N, Ikeda T (2012) AidC, a novel N-acylhomoserine lactonase from the potato root-associated cytophaga-flavobacteria-bacteroides (CFB) group bacterium Chryseobacterium sp. strain StRB126. Appl Environ Microbiol 78:7985–7992. https://doi.org/10.1128/AEM.02188-12
Park SY, Lee SJ, Oh TK et al (2003) AhlD, an N-acylhomoserine lactonase in Arthrobacter sp., and predicted homologues in other bacteria. Microbiology 149:1541–1550. https://doi.org/10.1099/mic.0.26269-0
Khan SR, Farrand SK (2009) The BlcC (AttM) lactonase of Agrobacterium tumefaciens does not quench the quorum-sensing system that regulates Ti plasmid conjugative transfer. J Bacteriol 191:1320–1329. https://doi.org/10.1128/JB.01304-08
Riaz K, Elmerich C, Raffoux A et al (2008) Metagenomics revealed a quorum quenching lactonase QlcA from yet unculturable soil bacteria. Commun Agric Appl Biol Sci 73:3–6
Huang JJ, Petersen A, Whiteley M, Leadbetter JR (2006) Identification of QuiP, the product of gene PA1032, as the second acyl-homoserine lactone acylase of Pseudomonas aeruginosa PAO1. Appl Environ Microbiol 72:1190–1197. https://doi.org/10.1128/AEM.72.2.1190-1197.2006
Zhang X, Enomoto K (2011) Characterization of a gene cluster and its putative promoter region for violacein biosynthesis in Pseudoalteromonas sp. 520P1. Appl Microbiol Biotechnol 90:1963–1971. https://doi.org/10.1007/s00253-011-3203-9
Wang Y, Ikawa A, Okaue S et al (2008) Quorum sensing signaling molecules involved in the production of violacein by Pseudoalteromonas. Biosci Biotechnol Biochem 72:1958–1961. https://doi.org/10.1271/bbb.80090
Dheilly A, Soum-Soutera E, Klein GL et al (2010) Antibiofilm activity of the marine bacterium Pseudoalteromonas sp. strain 3J6. Appl Environ Microbiol 76:3452–3461. https://doi.org/10.1128/AEM.02632-09
Papa R, Parrilli E, Sannino F et al (2013) Anti-biofilm activity of the Antarctic marine bacterium Pseudoalteromonas haloplanktis TAC125. Res Microbiol 164:450–456. https://doi.org/10.1016/j.resmic.2013.01.010
Guo X, Zheng L, Zhou W et al (2011) A case study on chemical defense based on quorum sensing: antibacterial activity of sponge-associated bacterium Pseudoalteromonas sp. NJ6-3-1 induced by quorum sensing mechanisms. Annu Microbiol 61:247–255. https://doi.org/10.1007/s13213-010-0129-x
Fineran PC, Slater H, Everson L et al (2005) Bioactivity and phylogeny of the marine bacterial genus Pseudoalteromonas. PhD thesis, Division of Industrial Food Research. National Food Institute (DTU Food), Technical University of Denmark. https://doi.org/10.1111/j.1365-2958.2005.04660.x
Li R, Zhu H, Ruan J et al (2010) De novo assembly of human genomes with massively parallel short read sequencing. Genome Res 20:265–272. https://doi.org/10.1101/gr.097261.109
Li R, Li Y, Kristiansen K, Wang J (2008) SOAP: short oligonucleotide alignment program. Bioinformatics 24:713–714. https://doi.org/10.1093/bioinformatics/btn025
Besemer J, Lomsadze A, Borodovsky M (2001) GeneMarkS: a self-training method for prediction of gene starts in microbial genomes. Implications for finding sequence motifs in regulatory regions. Nucleic Acids Res 29:2607–2618
Altschul SF, Gish W, Miller W et al (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Kanehisa M, Goto S, Kawashima S et al (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32:D277–D280. https://doi.org/10.1093/nar/gkh063
Tatusov RL, Fedorova ND, Jackson JD et al (2003) The COG database: an updated version includes eukaryotes. BMC Bioinform 4:41. https://doi.org/10.1186/1471-2105-4-41
Ashburner M, Ball CA, Blake JA et al (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25–29. https://doi.org/10.1038/75556
Darling ACE, Mau B, Blattner FR, Perna NT (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res 14:1394–1403. https://doi.org/10.1101/gr.2289704
Lee RD, Jospin G, Lang JM et al (2015) Draft genome sequence of Pseudoalteromonas tetraodonis strain UCD-SED8 (phylum gammaproteobacteria). Genome Announc 3:e01276-15. https://doi.org/10.1128/genomeA.01276-15
Thompson JD, Gibson TJ, Higgins DG (2002) Multiple sequence alignment using ClustalW and ClustalX. Curr Protoc Bioinform. https://doi.org/10.1002/0471250953.bi0203s00
Nicholas KBKBBKB, Jr HBN, Ii DWD et al (1997) GeneDoc: analysis and visualization of genetic variation. EMBnet News 4:14
Sio CF, Otten LG, Cool RH et al (2006) Quorum quenching by an N-acyl-homoserine lactone acylase from Pseudomonas aeruginosa PAO1. Infect Immun. https://doi.org/10.1128/iai.74.3.1673-1682.2006
Lamont IL, Martin LW (2003) Identification and characterization of novel pyoverdine synthesis genes in Pseudomonas aeruginosa. Microbiology. https://doi.org/10.1099/mic.0.26085-0
Solovyev V, Salamov A (2011) Automatic annotation of microbial genomes and metagenomic sequences. In: Li RW (ed) Metagenomics and its applications in agriculture, biomedicine and environmental studies. Nova Biomedical, New Delhi, pp 61–78
Huang Y, Wang J, Luan S (2012) Research status and trends in limnology journals: a bibliometric analysis based on SCI database. Scientometrics 92:735–746
Mei G-Y, Yan X-X, Turak A et al (2010) AidH, an alpha/beta-hydrolase fold family member from an Ochrobactrum sp. strain, is a novel N-acylhomoserine lactonase. Appl Environ Microbiol 76:4933–4942. https://doi.org/10.1128/AEM.00477-10
Mayer C, Romero M, Muras A, Otero A (2015) Aii20 J, a wide-spectrum thermostable N-acylhomoserine lactonase from the marine bacterium Tenacibaculum sp. 20 J, can quench AHL-mediated acid resistance in Escherichia coli. Appl Microbiol Biotechnol 99:9523–9539. https://doi.org/10.1007/s00253-015-6741-8
Ochiai S, Yasumoto S, Morohoshi T, Ikeda T (2014) AmiE, a novel N-acylhomoserine lactone acylase belonging to the amidase family, from the activated-sludge isolate Acinetobacter sp. strain Ooi24. Appl Environ Microbiol 80:6919–6925. https://doi.org/10.1128/AEM.02190-14
Nusrat H, Shankar P, Kushwah J et al (2011) Diversity and polymorphism in AHL-lactonase gene (aiiA) of Bacillus. J Microbiol Biotechnol 21:1001–1011. https://doi.org/10.4014/jmb.1105.05056
Acknowledgements
This work was supported by Guangdong Science and Technology Department (2013B030800001), Shenzhen Science and Technology Project (Grant Nos. JCYJ20140509174140691 and JCYJ20140417113430641), and CAS Adjunct Professorship (2013T1G0038, GJHS2014090100463583).
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Pan, Y., Wang, Y., Yan, X. et al. Quorum Quenching Enzyme APTM01, an Acylhomoserine-Lactone Acylase from Marine Bacterium of Pseudoalteromonas tetraodonis Strain MQS005. Curr Microbiol 76, 1387–1397 (2019). https://doi.org/10.1007/s00284-019-01739-z
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DOI: https://doi.org/10.1007/s00284-019-01739-z