Shallow-Water Hydrothermal Vents as Natural Accelerators of Bacterial Antibiotic Resistance in Marine Coastal Areas
Environmental contamination by heavy metals (HMs) poses several indirect risks to human health, including the co-spreading of genetic traits conferring resistance to both HMs and antibiotics among micro-organisms. Microbial antibiotic resistance (AR) acquisition is enhanced at sites anthropogenicall...
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| Format: | Article |
| Language: | English |
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MDPI AG
2022-02-01
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| Series: | Microorganisms |
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| Online Access: | https://www.mdpi.com/2076-2607/10/2/479 |
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| author | Erika Arcadi Eugenio Rastelli Michael Tangherlini Carmen Rizzo Monique Mancuso Marilena Sanfilippo Valentina Esposito Franco Andaloro Teresa Romeo |
| author_facet | Erika Arcadi Eugenio Rastelli Michael Tangherlini Carmen Rizzo Monique Mancuso Marilena Sanfilippo Valentina Esposito Franco Andaloro Teresa Romeo |
| author_sort | Erika Arcadi |
| collection | DOAJ |
| description | Environmental contamination by heavy metals (HMs) poses several indirect risks to human health, including the co-spreading of genetic traits conferring resistance to both HMs and antibiotics among micro-organisms. Microbial antibiotic resistance (AR) acquisition is enhanced at sites anthropogenically polluted by HMs, as well as in remote systems naturally enriched in HMs, such as hydrothermal vents in the deep sea. However, to date, the possible role of hydrothermal vents at shallower water depths as hot spots of microbial AR gain and spreading has not been tested, despite the higher potential risks associated with the closer vicinity of such ecosystems to coasts and human activities. In this work, we collected waters and sediments at the Panarea shallow-water hydrothermal vents, testing the presence of culturable marine bacteria and their sensitivity to antibiotics and HMs. All of the bacterial isolates showed resistance to at least one antibiotic and one HM and, most notably, 80% of them displayed multi-AR on average to 12 (min 8, max 15) different antibiotics, as well as multi-HM tolerance. We show that our isolates displayed high similarity (≥99%) to common marine bacteria, affiliating with Actinobacteria, Gammaproteobacteria, Alphaproteobacteria and Firmicutes, and all displayed wide growth ranges for temperature and salinity during in vitro physiological tests. Notably, the analysis of the genomes available in public databases for their closest relatives highlighted the lack of genes for AR, posing new questions on the origin of multi-AR acquisition in this peculiar HM-rich environment. Overall, our results point out that shallow-water hydrothermal vents may contribute to enhance AR acquisition and spreading among common marine bacteria in coastal areas, highlighting this as a focus for future research. |
| first_indexed | 2024-03-09T21:22:48Z |
| format | Article |
| id | doaj.art-776192f012744859944a1093247ff7ed |
| institution | Directory Open Access Journal |
| issn | 2076-2607 |
| language | English |
| last_indexed | 2024-03-09T21:22:48Z |
| publishDate | 2022-02-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | Microorganisms |
| spelling | doaj.art-776192f012744859944a1093247ff7ed2023-11-23T21:16:50ZengMDPI AGMicroorganisms2076-26072022-02-0110247910.3390/microorganisms10020479Shallow-Water Hydrothermal Vents as Natural Accelerators of Bacterial Antibiotic Resistance in Marine Coastal AreasErika Arcadi0Eugenio Rastelli1Michael Tangherlini2Carmen Rizzo3Monique Mancuso4Marilena Sanfilippo5Valentina Esposito6Franco Andaloro7Teresa Romeo8Department of Integrative Marine Ecology, Stazione Zoologica “Anton Dohrn”, Sicily Marine Centre, Contrada Porticatello, 29, 98167 Messina, ItalyDepartment of Marine Biotechnology, Stazione Zoologica “Anton Dohrn”, Fano Marine Centre, Viale Adriatico 1-N, 61032 Fano, ItalyDepartment of Research Infrastructures for Marine Biological Resources, Stazione Zoologica “Anton Dohrn”, Villa Comunale, 80121 Napoli, ItalyStazione Zoologica Anton Dohrn–Marine Biotechnology Department, Sicily Marine Centre, Villa Pace, Contrada Porticatello 29, 98167 Messina, ItalyDepartment of Integrative Marine Ecology, Stazione Zoologica “Anton Dohrn”, Sicily Marine Centre, Contrada Porticatello, 29, 98167 Messina, ItalyDepartment of Research Infrastructures for Marine Biological Resources, Stazione Zoologica “Anton Dohrn”, Sicily Marine Centre, Contrada Porticatello, 29, 98167 Messina, ItalyIstituto Nazionale di Oceanografia e di Geofisica Sperimentale—OGS Borgo Grotta Gigante 42/C, 34010 Sgonico, ItalyDepartment of Integrative Marine Ecology, Stazione Zoologica “Anton Dohrn”, Sicily Marine Centre, Lungomare Cristoforo Colombo (Complesso Roosevelt), 90149 Palermo, ItalyDepartment of Integrative Marine Ecology, Stazione Zoologica “Anton Dohrn”, Sicily Marine Centre, Via dei Mille 46, 98057 Milazzo, ItalyEnvironmental contamination by heavy metals (HMs) poses several indirect risks to human health, including the co-spreading of genetic traits conferring resistance to both HMs and antibiotics among micro-organisms. Microbial antibiotic resistance (AR) acquisition is enhanced at sites anthropogenically polluted by HMs, as well as in remote systems naturally enriched in HMs, such as hydrothermal vents in the deep sea. However, to date, the possible role of hydrothermal vents at shallower water depths as hot spots of microbial AR gain and spreading has not been tested, despite the higher potential risks associated with the closer vicinity of such ecosystems to coasts and human activities. In this work, we collected waters and sediments at the Panarea shallow-water hydrothermal vents, testing the presence of culturable marine bacteria and their sensitivity to antibiotics and HMs. All of the bacterial isolates showed resistance to at least one antibiotic and one HM and, most notably, 80% of them displayed multi-AR on average to 12 (min 8, max 15) different antibiotics, as well as multi-HM tolerance. We show that our isolates displayed high similarity (≥99%) to common marine bacteria, affiliating with Actinobacteria, Gammaproteobacteria, Alphaproteobacteria and Firmicutes, and all displayed wide growth ranges for temperature and salinity during in vitro physiological tests. Notably, the analysis of the genomes available in public databases for their closest relatives highlighted the lack of genes for AR, posing new questions on the origin of multi-AR acquisition in this peculiar HM-rich environment. Overall, our results point out that shallow-water hydrothermal vents may contribute to enhance AR acquisition and spreading among common marine bacteria in coastal areas, highlighting this as a focus for future research.https://www.mdpi.com/2076-2607/10/2/479shallow-water hydrothermal ventsantibiotic resistanceheavy metal pollutionmarine heterotrophic bacteriaTyrrhenian seaPanarea |
| spellingShingle | Erika Arcadi Eugenio Rastelli Michael Tangherlini Carmen Rizzo Monique Mancuso Marilena Sanfilippo Valentina Esposito Franco Andaloro Teresa Romeo Shallow-Water Hydrothermal Vents as Natural Accelerators of Bacterial Antibiotic Resistance in Marine Coastal Areas Microorganisms shallow-water hydrothermal vents antibiotic resistance heavy metal pollution marine heterotrophic bacteria Tyrrhenian sea Panarea |
| title | Shallow-Water Hydrothermal Vents as Natural Accelerators of Bacterial Antibiotic Resistance in Marine Coastal Areas |
| title_full | Shallow-Water Hydrothermal Vents as Natural Accelerators of Bacterial Antibiotic Resistance in Marine Coastal Areas |
| title_fullStr | Shallow-Water Hydrothermal Vents as Natural Accelerators of Bacterial Antibiotic Resistance in Marine Coastal Areas |
| title_full_unstemmed | Shallow-Water Hydrothermal Vents as Natural Accelerators of Bacterial Antibiotic Resistance in Marine Coastal Areas |
| title_short | Shallow-Water Hydrothermal Vents as Natural Accelerators of Bacterial Antibiotic Resistance in Marine Coastal Areas |
| title_sort | shallow water hydrothermal vents as natural accelerators of bacterial antibiotic resistance in marine coastal areas |
| topic | shallow-water hydrothermal vents antibiotic resistance heavy metal pollution marine heterotrophic bacteria Tyrrhenian sea Panarea |
| url | https://www.mdpi.com/2076-2607/10/2/479 |
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