Original Article

The ISME Journal (2015) 9, 1222–1234; doi:10.1038/ismej.2014.214; published online 14 November 2014

From deep-sea volcanoes to human pathogens: a conserved quorum-sensing signal in Epsilonproteobacteria

Ileana Pérez-Rodríguez1,2,3, Marie Bolognini1,2, Jessica Ricci1,2,4, Elisabetta Bini1,5 and Costantino Vetriani1,2

  1. 1Department of Biochemistry and Microbiology, Rutgers University, New Brunswick, NJ, USA
  2. 2Institute of Marine and Coastal Sciences, Rutgers University, New Brunswick, NJ, USA

Correspondence: C Vetriani, Institute of Marine and Coastal Sciences, Rutgers University, 71 Dudley Road, New Brunswick, NJ 08901, USA. E-mail: vetriani@marine.rutgers.edu

3Current address: Geophysical Laboratory, Carnegie Institution of Washington, Washington, DC, USA.

4Current address: Department of Biology, California Institute of Technology, Pasadena, CA, USA.

5Current address: Department of Pharmacy Practice and Administration, Rutgers University, Piscataway, NJ, USA.

Received 27 May 2014; Revised 27 September 2014; Accepted 1 October 2014
Advance online publication 14 November 2014

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Abstract

Chemosynthetic Epsilonproteobacteria from deep-sea hydrothermal vents colonize substrates exposed to steep thermal and redox gradients. In many bacteria, substrate attachment, biofilm formation, expression of virulence genes and host colonization are partly controlled via a cell density-dependent mechanism involving signal molecules, known as quorum sensing. Within the Epsilonproteobacteria, quorum sensing has been investigated only in human pathogens that use the luxS/autoinducer-2 (AI-2) mechanism to control the expression of some of these functions. In this study we showed that luxS is conserved in Epsilonproteobacteria and that pathogenic and mesophilic members of this class inherited this gene from a thermophilic ancestor. Furthermore, we provide evidence that the luxS gene is expressed—and a quorum-sensing signal is produced—during growth of Sulfurovum lithotrophicum and Caminibacter mediatlanticus, two Epsilonproteobacteria from deep-sea hydrothermal vents. Finally, we detected luxS transcripts in Epsilonproteobacteria-dominated biofilm communities collected from deep-sea hydrothermal vents. Taken together, our findings indicate that the epsiloproteobacterial lineage of the LuxS enzyme originated in high-temperature geothermal environments and that, in vent Epsilonproteobacteria, luxS expression is linked to the production of AI-2 signals, which are likely produced in situ at deep-sea vents. We conclude that the luxS gene is part of the ancestral epsilonproteobacterial genome and represents an evolutionary link that connects thermophiles to human pathogens.