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

  • José Carlos Reina
  • Marta Torres
  • Inmaculada LlamasEmail author
Original Article

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.

Keywords

Quorum quenching N-Acylhomoserine lactones Stenotrophomonas Acylase 

Notes

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 information

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

Compliance with Ethical Standards

Conflicts of Interest

The authors declare that they have no conflict of interest.

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Authors and Affiliations

  1. 1.Department of Microbiology, Faculty of PharmacyUniversity of GranadaGranadaSpain
  2. 2.Institute of Biotechnology, Biomedical Research Center (CIBM)University of GranadaGranadaSpain
  3. 3.Institute for Integrative Biology of the Cell, CEA, CNRS, University Paris-SudUniversity Paris-SaclayGif sur YvetteFrance

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