From deep-sea volcanoes to human pathogens: a conserved quorum-sensing signal in Epsilonproteobacteria
Open accessAbstract
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.
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This capacity to settle quickly on different types of surfaces shows a strong ability for colonization in deep sea vent for these groups especially for Epsilonbacteraeota for which a highly conserved quorum sensing machinery enabling biofilm formation has been retrieved in every lineages.
“This capacity to settle quickly on different types of surfaces shows a strong ability for colonization in deep sea vent for these groups especially for Epsilonbacteraeota for which a highly conserved quorum sensing machinery enabling biofilm formation has been retrieved in every lineages (Pérez-Rodriguez et al., 2015).”
From Is It First the Egg or the Shrimp? – Diversity and Variation in Microbial Communities Colonizing Broods of the Vent Shrimp Rimicaris exoculata During Embryonic Development (2019) · cites this paper as Pérez-Rodriguez et al., 2015
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Chauhan, A., Pathak, A., Rodolfo‐Metalpa, R., Milazzo, M., Green, S. J., & Hall-Spencer, J. M. (2015) · Genome Announcements · doi:10.1128/genomea.01543-14 · Cited by 7 · see citing works
Ladd, T. M., Selci, M., Davis, D., Cannon, O., Plowman, C. Q., Schlegel, I., Inaba, A., Mills, S. W., Vetriani, C., Mullineaux, L. S., et al. (2024) · Deep Sea Research Part I Oceanographic Research Papers · doi:10.1016/j.dsr.2024.104314 · Cited by 5 · see citing works
The chemosynthetic biofilm microbiome of deep-sea hydrothermal vents across space and time
Grosche, A., Selci, M., Smedile, F., Giovannelli, D., Borin, S., Bris, N. L., & Vetriani, C. (2025) · Environmental Microbiome · doi:10.1186/s40793-025-00738-x · Cited by 5 · see citing works
Marchese, P., Bracegirdle, J., Young, R. M., Ferrari, E., Garzoli, L., Murphy, M. J., Tuohy, M. G., Allcock, A. L., & Baker, B. J. (2025) · Environmental Microbiology Reports · doi:10.1111/1758-2229.70092 · Cited by 3 · see citing works
Mei, Y.-X., Yang, K., Zhang, L., Jin, Y., Yang, N., Yang, H. Y., Zheng, Y.-L., Pang, Y., Gong, Y., Zhou, H., et al. (2024) · Frontiers in Psychiatry · doi:10.3389/fpsyt.2024.1335554 · Cited by 3 · see citing works
Mechanistic Adaptation of Microbiomes in Extreme Environments
Viswadeepika, K., & Bramhachari, P. V. (2022) · Springer eBooks · doi:10.1007/978-981-19-3696-8_3 · Cited by 3 · see citing works
Patwardhan, S., Phan, J. B., Smedile, F., & Vetriani, C. (2023) · Microorganisms · doi:10.3390/microorganisms11061366 · Cited by 3 · see citing works
Mino, S., Fukazawa, S., Tsuchiya, J., McNichol, J. C., Sievert, S. M., Yamaki, S., Ando, Y., & Sawabe, T. (2023) · INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY · doi:10.1099/ijsem.0.006132 · Cited by 3 · see citing works
Quorum Sensing from Two Engineers’ Perspectives
Stephens, K., & Bentley, W. E. (2023) · Israel Journal of Chemistry · doi:10.1002/ijch.202200083 · Cited by 3 · see citing works
Cordone, A., Coppola, A., Severino, A., Correggia, M., Selci, M., Cascone, A., Vetriani, C., & Giovannelli, D. (2022) · Methods in molecular biology · doi:10.1007/978-1-0716-2313-8_5
Epsilonproteobacteria: specialist in specific environments
聡, 中. (2014) · Kyokugen Kankyo Seibutsu Gakkaishi · doi:10.3118/extremophiles.13.2_63
Zheng, X., Zheng, C., Zhou, S., & Zou, D. (2025) · Processes · doi:10.3390/pr13092931
Godini, E., & Siavoshi, F. (2026) · International Microbiology · doi:10.1007/s10123-026-00784-6
- Authors
- Pérez-Rodríguez, I., Bolognini, M., Ricci, J., Bini, E., & Vetriani, C.
- Affiliations
- Department of Biochemistry and Microbiology, Rutgers University , New Brunswick, NJ,
- Rutgers, The State University of New Jersey (US)
- Corresponding author
- Vetriani, Costantino
- ORCID
- Vetriani, Costantino
- Venue
- The ISME Journal
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-11-14
- Volume
- 9
- Issue
- 5
- Pages
- 1222-1234
- ISSN
- 1751-7362 (ISSN-L)
- 1751-7370
- PMC
- PMC4409165
- OpenAlex
- W1964962841
- Cited by
- 44
- References
- 67
- Citations by year
- 2026: 1 · 2025: 4 · 2024: 3 · 2023: 5 · 2022: 3 · 2021: 5 · 2020: 2 · 2019: 8 · 2018: 4 · 2017: 4 · 2016: 1 · 2015: 3 · 2014: 1
- FWCI
- 1.23
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The ISME Journal (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (0843678, 0456676)
- Center for Dark Energy Biosphere Investigations
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bacterial biofilms and quorum sensing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › bioluminescence and chemiluminescence research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Keywords
- quorum sensing, Epsilonproteobacteria, deep-sea hydrothermal vents, chemosynthetic bacteria, biofilm formation, human pathogens, gene evolution, virulence gene regulation, chemotaxis
- MeSH terms
- Biological Assay, Homoserine, Humans, Lactones, Oxidation-Reduction, Phylogeny, Temperature, Water Microbiology, Likelihood Functions, Genome, Bacterial, Biofilms, Epsilonproteobacteria, Quorum Sensing, Hydrothermal Vents
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