Skip to main content
SpringerLink
Log in

Stenotrophomonas maltophilia AHL-Degrading Strains Isolated from Marine Invertebrate Microbiota Attenuate the Virulence of Pectobacterium carotovorum and Vibrio coralliilyticus

Marine Biotechnology Aims and scope Submit manuscript

Abstract

Many Gram-negative aquacultural and agricultural pathogens control virulence factor expression through a quorum-sensing (QS) mechanism involving the production of N-acylhomoserine (AHL) signalling molecules. Thus, the interruption of QS systems by the enzymatic degradation of signalling molecules, known as quorum quenching (QQ), has been proposed as a novel strategy to combat these infections. Given that the symbiotic bacteria of marine invertebrates are considered to be an important source of new bioactive molecules, this study explores the presence of AHL-degrading bacteria among 827 strains previously isolated from the microbiota of anemones and holothurians. Four of these strains (M3-1, M1-14, M3-13 and M9-54-2), belonging to the species Stenotrophomonas maltophilia, were selected on the basis of their ability to degrade a broad range of AHLs, and the enzymes involved in their activity were identified. Strain M9-54-2, which showed the strongest AHL-degrading activity, was selected for further study. High-performance liquid chromatography–mass-spectrometry confirmed that the QQ enzyme is not a lactonase. Strain M9-54-2 degraded AHL accumulation and reduced the production of enzymatic activity in Pectobacterium carotovorum CECT 225T and Vibrio coralliilyticus VibC-Oc-193 in in vitro co-cultivation experiments. The effect of AHL inactivation was confirmed by a reduction in potato tuber maceration and brine shrimp (Artemia salina) mortality caused by P. carotovorum and Vibrio coralliilyticus, respectively. This study strengthens the evidence of marine organisms as an underexplored and promising source of QQ enzymes, useful to prevent infections in aquaculture and agriculture. To our knowledge, this is the first time that anemones and holothurians have been studied for this purpose.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price includes VAT (France)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

References

  • Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Austin B, Zhang XH (2006) Vibrio harveyi: a significant pathogen of marine vertebrates and invertebrates. Lett Appl Microbiol 43:119–124

    Article  CAS  PubMed  Google Scholar 

  • Baird-Parker AC (1963) A classification of micrococci and staphylococci based on physiological and biochemical tests. J Gen Microbiol 30:409–427

    Article  CAS  PubMed  Google Scholar 

  • Ban H, Chai X, Lin Y, Zhou Y, Peng D, Zhou Y, Zou Y, Yu Z, Sun M (2009) Transgenic Amorphophallus konjac expressing synthesized acyl-homoserine lactonase (aiiA) gene exhibit enhanced resistance to soft rot disease. Plant Cell Rep 28:1847–1855

    Article  CAS  PubMed  Google Scholar 

  • Bhardwaj AK, Vinothkumar K, Rajpara N (2013) Bacterial quorum sensing inhibitors: attractive alternatives for control of infectious pathogens showing multiple drug resistance. Recent Pat Antiinfect Drug Discov 8:68–83

    Article  CAS  PubMed  Google Scholar 

  • Bhatnagar I, Kim SK (2010) Immense essence of excellence: marine microbial bioactive compounds. Mar Drugs 8:2673–2701

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bijtenhoorn P, Schipper C, Hornung C, Quitschau M, Grond S, Weiland N, Streit WR (2011) BpiB05, a novel metagenome-derived hydrolase acting on N-acylhomoserine lactones. J Biotechnol 155:86–94

    Article  CAS  PubMed  Google Scholar 

  • Bjarnsholt T, van Gennip M, Jakobsen TH, Christensen LD, Jensen PØ, Givskov M (2010) In vitro screens for quorum sensing inhibitors and in vivo confirmation of their effect. Nat Protoc 52(5):282

    Article  CAS  Google Scholar 

  • Brooke JS (2012) Stenotrophomonas maltophilia: an emerging global opportunistic pathogen. Clin Microbiol Rev 25:2–41

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cabello FC, Godfrey HP, Tomova A, Ivanova L, Dölz H, Millanao A, Buschmann AH (2013) Antimicrobial use in aquaculture re-examined: its relevance to antimicrobial resistance and to animal and human health. Environ Microbiol 15:1917–1942

    Article  PubMed  Google Scholar 

  • Carlier A, Uroz S, Smadja B, Fray R, Latour X, Dessaux Y, Faure D (2003) The Ti plasmid of Agrobactetium tumefaciens harbors an attM-paralogous gene, aiiB, also encoding N-acyl homoserine lactonase activity. Appl Environ Microbiol 69:4989–4993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chan KG, Yin WF, Sam CK, Koh CL (2009) A novel medium for the isolation of N-acylhomoserine lactone-degrading bacteria. J Ind Microbiol Biotechnol 36:247–251

    Article  CAS  PubMed  Google Scholar 

  • Chan KG, Atkinson S, Mathee K, Sam CK, Chhabra SR, Cmara M, Koh CL, Williams P (2011) 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. BMC Microbiol 11:51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen R, Zhou Z, Cao Y, Bai Y, Yao B (2010) High yield expression of an AHL-lactonase from Bacillus sp. B546 in Pichia pastoris and its application to reduce Aeromonas hydrophila mortality in aquaculture. Microb Cell Factories 9:39

    Article  CAS  Google Scholar 

  • Chen F, Gao Y, Chen X, Yu Z, Li X (2013) Quorum quenching enzymes and their application in degrading signal molecules to block quorum sensing-dependent infection. Int J Mol Sci 14:17477–17500

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Choopun N, Louis V, Huq A, Colwell RR (2002) Simple procedure for rapid identification of Vibrio cholerae from the aquatic environment. Appl Environ Microbiol 68:995–998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crépin A, Barbey C, Beury-Cirou A, Hélias V, Taupin L, Reverchon S, Nasser W, Faure D, Dufour A, Orange N, Feuilloley M, Heurlier K, Burini JF, Latour X (2012) Quorum sensing signaling molecules produced by reference and emerging soft-rot bacteria (Dickeya and Pectobacterium spp.). PLoS One 7:e35176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Defoirdt T, Bossier P, Sorgeloos P, Verstraete W (2005) The impact of mutations in the quorum sensing systems of Aeromonas hydrophila, Vibrio anguillarum and Vibrio harveyi on their virulence towards gnotobiotically cultured Artemia franciscana. Environ Microbiol 7:1239–1247

    Article  CAS  PubMed  Google Scholar 

  • Defoirdt T, Boon N, Bossier P (2010) Can bacteria evolve resistance to quorum sensing disruption? PLoS Pathog 6:e1000989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Defoirdt T, Sorgeloos P, Bossier P (2011) Alternatives to antibiotics for the control of bacterial disease in aquaculture. Curr Opin Microbiol 14:251–258

    Article  PubMed  Google Scholar 

  • Dong YH, Zhang LH (2005) Quorum sensing and quorum-quenching enzymes. J Microbiol 43:101–109

    CAS  PubMed  Google Scholar 

  • 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 U S A 97:3526–3531

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Food and Agriculture Organization (FAO) (2016) The state of world fisheries and aquaculture 2016. Food and Agriculture Organization of the United Nations, Rome, Italy

  • Fuqua C, Parsek MR, Greenberg EP (2001) Regulation of gene expression by cell-to-cell communication: acyl-homoserine lactone quorum sensing. Annu Rev Genet 35:439–468

    Article  CAS  PubMed  Google Scholar 

  • Furushita M, Okamoto A, Maeda T, Ohta M, Shiba T (2005) Isolation of multidrug-resistantStenotrophomonas maltophilia from cultured yellowtail (Seriola quinqueradiata) from a marine fish farm. Appl Environ Microbiol 71:5598–5600

  • Garg N, Manchanda G, Kumar A (2014) Bacterial quorum sensing: circuits and applications. Antonie Van Leeuwenhoek 105:289–305

    Article  PubMed  Google Scholar 

  • Garge SS, Nerurkar AS (2016) Attenuation of quorum sensing regulated virulence of Pectobacterium carotovorum subsp. carotovorum through an AHL lactonase produced by Lysinibacillus sp. Gs50. PLoS One 11:1–23

    Article  CAS  Google Scholar 

  • Givskov M, De Nys R, Manefield M, Gram L, Maximilien R, Eberl L, Molin SØ, Steinberg PD, Kjelleberg S (1996) Eukaryotic interference with homoserine lactone-mediated prokaryotic signalling. J Bacteriol 178:6618–6622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Golberg K, Pavlov V, Marks RS, Kushmaro A (2013) Coral-associated bacteria, quorum sensing disrupters, and the regulation of biofouling. Biofouling 29:669–682

    Article  CAS  PubMed  Google Scholar 

  • Grandclément C, Tannières M, Moréra S, Dessaux Y, Faure D (2016) Quorum quenching: role in nature and applied developments. FEMS Microbiol Rev 40:86–116

    Article  CAS  PubMed  Google Scholar 

  • Ha C, Kim SK, Lee MN, Lee JH (2014a) Quorum sensing-dependent metalloprotease VvpE is important in the virulence of Vibrio vulnificus to invertebrates. Microb Pathog 71–72:8–14

    Article  CAS  PubMed  Google Scholar 

  • Plate-based assay for swimming motility in Pseudomonas aeruginosa. Methods Mol Biol 1149:59–65

  • Ha D-G, Kuchma SL, O'Toole GA (2014c) Plate-based assay for swarming motility in Pseudomonas aeruginosa. Methods Mol Biol 1149:67–72

  • Hayward AC, Fegan N, Fegan M, Stirling GR (2010) Stenotrophomonas and Lysobacter: ubiquitous plant-associated gamma-proteobacteria of developing significance in applied microbiology. J Appl Microbiol 108:756–770

    Article  CAS  PubMed  Google Scholar 

  • Henke JM, Bassler BL (2004) Bacterial social engagements. Trends Cell Biol 14:648–656

    Article  CAS  PubMed  Google Scholar 

  • Hjort K, Presti I, Elväng A, Marinelli F, Sjöling S (2014) Bacterial chitinase with phytopathogen control capacity from suppressive soil revealed by functional metagenomics. Appl Microbiol Biotechnol 98:2819–2828

    Article  CAS  PubMed  Google Scholar 

  • Huang W, Lin Y, Yi S, Liu P, Shen J, Shao Z, Liu Z (2012) QsdH, a novel AHL lactonase in the RND-type inner membrane of marine Pseudoalteromonas byunsanensis strain 1A01261. PLoS One 7:1–12

    Article  Google Scholar 

  • Huedo P, Coves X, Daura X, Gibert I, Yero D (2018) Quorum sensing signaling and quenching in the multidrug-resistant pathogen Stenotrophomonas maltophilia. Front Cell Infect Microbiol 8:122

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hughes C, Fenical W (2012) Antibacterials from the sea. Chemistry (Easton) 42:12512–12525

    Google Scholar 

  • Jayaraman A, Wood TK (2008) Bacterial quorum sensing: signals, circuits, and implications for biofilms and disease. Annu Rev Biomed Eng 10:145–167

    Article  CAS  PubMed  Google Scholar 

  • Jeffries CD, Holtmian DF, Guse DG (1957) Rapid method for determining the activity of microorganisms on nucleic acids. J Bacteriol 73:590–591

  • Kang JE, Han JW, Jeon BJ, Kim BS (2016) Efficacies of quorum sensing inhibitors, piericidin A and glucopiericidin A, produced by Streptomyces xanthocidicus KPP01532 for the control of potato soft rot caused by Erwinia carotovora subsp. atroseptica. Microbiol Res 184:32–41

    Article  CAS  PubMed  Google Scholar 

  • Kelley LA, Mezulis S, Yates CM, Wass MN, Sternberg MJE (2015) The Phyre2 web portal for protein modeling, prediction and analysis. Nat Protoc 10:845–858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • León-Palmero E, Joglar V, Álvarez PA, Martín-Platero A, Llamas I, Reche I (2018) Diversity and antimicrobial potential in sea anemone and holothurian microbiomes. PLoS One 13:e0196178

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lin YH, Xu JL, Hu J, Wang LH, Leong Ong S, Renton Leadbetter J, Zhang LH (2003) Acyl-homoserine lactone acylase from Ralstonia strain XJ12B represents a novel and potent class of quorum-quenching enzymes. Mol Microbiol 47:849–860

    Article  PubMed  Google Scholar 

  • Lira F, Berg G, Martínez JL (2017) Double-face meets the bacterial world: the opportunistic pathogen Stenotrophomonas maltophilia. Front Microbiol 8:1–15

    Article  Google Scholar 

  • Llamas I, Quesada E, Martínez-Cánovas MJ, Gronquist M, Eberhard A, González JE (2005) Quorum sensing in halophilic bacteria: detection of N-acyl-homoserine lactones in the exopolysaccharide-producing species of Halomonas. Extremophiles 9:333–341

    Article  CAS  PubMed  Google Scholar 

  • Maeda T, García-Contreras R, Pu M, Sheng L, Garcia LR, Tomás M, Wood TK (2012) Quorum quenching quandary: resistance to antivirulence compounds. ISME J 6:493–501

    Article  CAS  PubMed  Google Scholar 

  • Marchler-Bauer A, Bryant SH (2004) CD-search: protein domain annotations on the fly. Nucleic Acids Res 32:W327–W331

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marchler-Bauer A, Lu S, Anderson JB, Chitsaz F, Derbyshire MK, DeWeese-Scott C, Fong JH, Geer LY, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Jackson JD, Ke Z, Lanczycki CJ, Lu F, Marchler GH, Mullokandov M, Omelchenko MV, Robertson CL, Song JS, Thanki N, Yamashita RA, Zhang D, Zhang N, Zheng C, Bryant SH (2011) CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res 39:D225–D229

    Article  CAS  PubMed  Google Scholar 

  • Marchler-Bauer A, Derbyshire MK, Gonzales NR, Lu S, Chitsaz F, Geer LY, Geer RC, He J, Gwadz M, Hurwitz DI, Lanczycki CJ, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Bryant SH (2015) CDD: NCBI’s conserved domain database. Nucleic Acids Res 43:D222–D226

    Article  CAS  PubMed  Google Scholar 

  • Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Geer LY, Bryant SH (2017) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45:D200–D203

    Article  CAS  PubMed  Google Scholar 

  • Marketon MM, Gronquist MR, Eberhard A, González JE (2002) Characterization of the Sinorhizobium meliloti sinR/sinI locus and the production of novel N-acyl homoserine lactones. J Bacteriol 184:5686–5695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Martín-Platero AM, Valdivia E, Maqueda M, Martínez-Bueno M (2007) Fast, convenient, and economical method for isolating genomic DNA from lactic acid bacteria using a modification of the protein “salting-out” procedure. Anal Biochem 366:102–104

    Article  CAS  PubMed  Google Scholar 

  • Martins PMM, Merfa MV, Takita MA, De Souza AA (2018) Persistence in phytopathogenic bacteria: do we know enough? Front Microbiol 9:1099

    Article  PubMed  PubMed Central  Google Scholar 

  • Mcclean KH, Winson MK, Fish L, Taylor A, Chhabra SR, Camara M, Daykin M, John H, Swift S, Bycroft BW, Stewart GS, Williams P (1997) Quorum sensing and Chromobacterium violaceum: exploitation of violacein production and inhibition for the detection of N-acyl homoserine lactones. Microbiology 143:3703–3711

    Article  CAS  PubMed  Google Scholar 

  • Molina L, Constantinescu F, Michel L, Reimmann C, Duffy B, Défago G (2003) Degradation of pathogen quorum-sensing molecules by soil bacteria: a preventive and curative biological control mechanism. FEMS Microbiol Ecol 45:71–81

    Article  CAS  PubMed  Google Scholar 

  • Morohoshi T, Kato M, Fukamachi K, Kato N, Ikeda T (2008) N-Acylhomoserine lactone regulates violacein production in Chromobacterium violaceum type strain ATCC 12472. FEMS Microbiol Lett 279:124–130

    Article  CAS  PubMed  Google Scholar 

  • Mourey A, Kilbertus G (1976) Simple media containing stabilized tributyrin for demonstrating lipolytic bacteria in foods and soils. J Appl Bacteriol 40:47–51

    Article  CAS  PubMed  Google Scholar 

  • Mukherjee P, Roy P (2016) Genomic potential of Stenotrophomonas maltophilia in bioremediation with an assessment of its multifaceted role in our environment. Front Microbiol 7:1–14

    CAS  Google Scholar 

  • Mukherji R, Varshney NK, Panigrahi P, Suresh CG, Prabhune A (2014) A new role for penicillin acylases: degradation of acyl homoserine lactone quorum sensing signals by Kluyvera citrophilapenicillin G acylase. Enzym Microb Technol 56:1–7

    Article  CAS  Google Scholar 

  • Natrah FMI, Defoirdt T, Sorgeloos P, Bossier P (2011) Disruption of bacterial cell-to-cell communication by marine organisms and its relevance to aquaculture. Mar Biotechnol 13:109–126

    Article  CAS  Google Scholar 

  • Ng W-L, Bassler BL (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nhan DT, Cam DTV, Wille M, Defoirdt T, Bossier P, Sorgeloos P (2010) Quorum quenching bacteria protect Macrobrachium rosenbergii larvae from Vibrio harveyi infection. J Appl Microbiol 109:1007–1016

    Article  CAS  PubMed  Google Scholar 

  • Niu B, Paulson JN, Zheng X, Kolter R (2017) Simplified and representative bacterial community of maize roots. Proc Natl Acad Sci U S A 114:E2450–E2459

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ochiai S, Morohoshi T, Kurabeishi A, Shinozaki M, Fujita H, Sawada I, Ikeda T (2013) Production and degradation of N-acylhomoserine lactone quorum sensing signal molecules in bacteria isolated from activated sludge. Biosci Biotechnol Biochem 77:2436–2440

    Article  CAS  PubMed  Google Scholar 

  • Park S, Kang H, Jang H, Koo B, Yum D, Park S, Kang H, Jang H, Lee J, Koo B (2005) Identification of extracellular N-acylhomoserine lactone acylase from a Streptomyces sp. and its application to quorum quenching. Appl Environ Microbiol 71:2632–2641

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Penesyan A, Gillings M, Paulsen IT (2015) Antibiotic discovery: combatting bacterial resistance in cells and in biofilm communities. Molecules 20:5286–5298

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pikovskaya RI (1948) Mobilization of phosphorus in soil in connection with the vital activity of some microbial species. Mikrobiologiya 17:362–370

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Quiñones B, Dulla G, Lindow SE (2005) Exopolysaccharide production, motility, and virulence in Pseudomonas syringae. Society 18:682–693

    Google Scholar 

  • Rasko DA, Sperandio V (2010) Anti-virulence strategies to combat bacteria-mediated disease. Nat Rev Drug Discov 9:117–128

    Article  CAS  PubMed  Google Scholar 

  • Romanenko LA, Uchino M, Tanaka N, Frolova GM, Slinkina NN, Mikhailov VV (2008) Occurrence and antagonistic potential of Stenotrophomonas strains isolated from deep-sea invertebrates. Arch Microbiol 189:337–344

    Article  CAS  PubMed  Google Scholar 

  • Romero M, Diggle SP, Heeb S, Cámara M, Otero A (2008) Quorum quenching activity in Anabaena sp. PCC 7120: identification of AiiC, a novel AHL-acylase. FEMS Microbiol Lett 280:73–80

    Article  CAS  PubMed  Google Scholar 

  • Romero M, Martin-Cuadrado AB, Roca-Rivada A, Cabello AM, Otero A (2011) Quorum quenching in cultivable bacteria from dense marine coastal microbial communities. FEMS Microbiol Ecol 75:205–217

    Article  CAS  PubMed  Google Scholar 

  • Romero M, Muras A, Mayer C, Buján N, Magariños B, Otero A (2014) In vitro quenching of fish pathogen Edwardsiella tarda AHL production using marine bacterium Tenacibaculum sp. strain 20J cell extracts. Dis Aquat Org 108:217–225

    Article  Google Scholar 

  • Rosenberg E, Koren O, Reshef L, Efrony R, Zilber-Rosenberg I (2007) The role of microorganisms in coral health, disease and evolution. Nat Rev Microbiol 5:355–362

    Article  CAS  PubMed  Google Scholar 

  • Rubio-Portillo E, Yarza P, Peñalver C, Ramos-Esplá AA, Antón J (2014) New insights into Oculina patagonica coral diseases and their associated Vibrio spp. communities. ISME J 8:1794–1807

    Article  PubMed  PubMed Central  Google Scholar 

  • Ryan RP, Monchy S, Cardinale M, Taghavi S, Crossman L, Avison MB, Berg G, van der Lelie D, Dow JM (2009) The versatility and adaptation of bacteria from the genus Stenotrophomonas. Nat Rev Microbiol 7:514–525

    Article  CAS  PubMed  Google Scholar 

  • Santhakumari S, Nilofernisha NM, Ponraj JG, Pandian SK, Ravi AV (2017) In vitro and in vivo exploration of palmitic acid from Synechococcus elongatus as an antibiofilm agent on the survival of Artemia franciscana against virulent vibrios. J Invertebr Pathol 150:21–31

    Article  CAS  PubMed  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shaw PD, Ping G, Daly SL, Cha C, Cronan JE, Rinehart KL, Farrand SK (1997) Detecting and characterizing N-acyl-homoserine lactone signal molecules by thin-layer chromatography. Proc Natl Acad Sci 94:6036–6041

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sunder AV, Utari PD, Ramasamy S, van Merkerk R, Quax W, Pundle A (2017) Penicillin V acylases from gram-negative bacteria degrade N-acylhomoserine lactones and attenuate virulence in Pseudomonas aeruginosa. Appl Microbiol Biotechnol 101:2383–2395

    Article  CAS  PubMed  Google Scholar 

  • Tait K, Havenhand J (2013) Investigating a possible role for the bacterial signal molecules N-acylhomoserine lactones in Balanus improvisus cyprid settlement. Mol Ecol 22:2588–2602

    Article  CAS  PubMed  Google Scholar 

  • Tan CH, Koh KS, Xie C, Zhang J, Tan XH, Lee GP, Zhou Y, Ng WJ, Rice SA, Kjelleberg S (2015) Community quorum sensing signalling and quenching: microbial granular biofilm assembly. NPJ Biofilms Microbiomes 1:15006

    Article  PubMed  PubMed Central  Google Scholar 

  • Tello E, Castellanos L, Duque C (2012) Disruption in quorum-sensing systems and bacterial biofilm inhibition by cembranoid diterpenes isolated from the octocoral Eunicea knighti. J Nat Prod 75:1637–1642

    Article  CAS  PubMed  Google Scholar 

  • Ter Kuile BH, Kraupner N, Brul S (2016) The risk of low concentrations of antibiotics in agriculture for resistance in human health care. FEMS Microbiol Lett 363:fnw210

    Article  CAS  PubMed  Google Scholar 

  • Torabi Delshad S, Soltanian S, Sharifiyazdi H, Haghkhah M, Bossier P (2018) Identification of N-acyl homoserine lactone-degrading bacteria isolated from rainbow trout (Oncorhynchus mykiss). J Appl Microbiol 125:356–369

    Article  CAS  PubMed  Google Scholar 

  • Torres M, Romero M, Prado S, Dubert J, Tahrioui A, Otero A, Llamas I (2013) N-acylhomoserine lactone-degrading bacteria isolated from hatchery bivalve larval cultures. Microbiol Res 168:547–554

    Article  CAS  PubMed  Google Scholar 

  • Torres M, Rubio-Portillo E, Antón J, Ramos-Esplá AA, Quesada E, Llamas I (2016) Selection of the N-acylhomoserine lactone-degrading bacterium Alteromonas stellipolaris PQQ-42 and of its potential for biocontrol in aquaculture. Front Microbiol 7:646

    Article  PubMed  PubMed Central  Google Scholar 

  • Torres M, Uroz S, Salto R, Fauchery L, Quesada E, Llamas I (2017) HqiA, a novel quorum-quenching enzyme which expands the AHL lactonase family. Sci Rep 7:943

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Torres M, Reina JC, Fuentes-Monteverde JC, Fernandez G, Rodriguez J, Jiménez C, Llamas I (2018) AHL-lactonase expression in three marine emerging pathogenic Vibrio spp. reduces virulence and mortality in brine shrimp (Artemia salina) and Manila clam (Venerupis philippinarum). PLoS One 13:1–23

    Google Scholar 

  • Uroz S, Chhabra SR, Cámara M, Williams P, Oger P, Dessaux Y (2005) N-Acylhomoserine lactone quorum-sensing molecules are modified and degraded by Rhodococcus erythropolis W2 by both amidolytic and novel oxidoreductase activities. Microbiology 151:3313–3322

    Article  CAS  PubMed  Google Scholar 

  • Uroz S, Oger PM, Chapelle E, Adeline MT, Faure D, Dessaux Y (2008) A Rhodococcus qsdA-encoded enzyme defines a novel class of large-spectrum quorum-quenching lactonases. Appl Environ Microbiol 74:1357–1366

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Utari PD, Vogel J, Quax WJ (2017) Deciphering physiological functions of AHL quorum quenching acylases. Front Microbiol 8:1123

    Article  PubMed  PubMed Central  Google Scholar 

  • Valliappan K, Sun W, Li Z (2014) Marine actinobacteria associated with marine organisms and their potentials in producing pharmaceutical natural products. Appl Microbiol Biotechnol 98:7365–7377

    Article  CAS  PubMed  Google Scholar 

  • Vinoj G, Vaseeharan B, Thomas S, Spiers AJ, Shanthi S (2014) Quorum-quenching activity of the AHL-lactonase from Bacillus licheniformis DAHB1 inhibits Vibrio biofilm formation in vitro and reduces shrimp intestinal colonisation and mortality. Mar Biotechnol 16:707–715

    Article  CAS  Google Scholar 

  • Whitehead NA, Barnard AML, Slater H, Simpson NJL, Salmond GPC (2001) Quorum-sensing in Gram-negative bacteria. FEMS Microbiol Rev 25:365–404

    Article  CAS  PubMed  Google Scholar 

  • Yates EA, Philipp B, Buckley C, Atkinson S, Chhabra SR, Sockett RE, Goldner M, Dessaux Y, Cámara M, Smith H, Williams P (2002) N-acylhomoserine lactones undergo lactonolysis in a pH-, temperature-, and acyl chain length-dependent manner during growth of Yersinia pseudotuberculosis and Pseudomonas aeruginosa. Infect Immun 70:5635–5646

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoon S-H, Ha S-M, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zaman SB, Hussain MA, Nye R, Mehta V, Mamun KT, Hossain N (2017) A review on antibiotic resistance: alarm bells are ringing. Cureus 9:e1403

    PubMed  PubMed Central  Google Scholar 

  • Zhang Z, Yuen GY (2000) The role of Chitinase production by Stenotrophomonas maltophilia strain C3 in biological control of Bipolaris sorokiniana. Phytopathology 90:384–389

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

José Carlos Reina is supported by an FPU fellowship from the Spanish Ministry of Education, Culture and Sport (FPU15/01717). The authors wish to thank Michael O’Shea for proofreading the manuscript.

Funding

This study was funded by the Spanish Ministry of the Economy and Competitiveness [AGL2015-68806-R].

Author information

Authors and Affiliations

  1. Department of Microbiology, Faculty of Pharmacy, University of Granada, 18071, Granada, Spain

    José Carlos Reina, Marta Torres & Inmaculada Llamas

  2. Institute of Biotechnology, Biomedical Research Center (CIBM), University of Granada, 18071, Granada, Spain

    Marta Torres & Inmaculada Llamas

  3. Institute for Integrative Biology of the Cell, CEA, CNRS, University Paris-Sud, University Paris-Saclay, Gif sur Yvette, France

    Marta Torres

Authors
  1. José Carlos Reina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marta Torres
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Inmaculada Llamas
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Inmaculada Llamas.

Ethics declarations

Conflicts of Interest

The authors declare that they have no conflict of interest.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Reina, J.C., Torres, M. & Llamas, I. Stenotrophomonas maltophilia AHL-Degrading Strains Isolated from Marine Invertebrate Microbiota Attenuate the Virulence of Pectobacterium carotovorum and Vibrio coralliilyticus. Mar Biotechnol 21, 276–290 (2019). https://doi.org/10.1007/s10126-019-09879-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10126-019-09879-w

Keywords

Search

Navigation