Flow Cytometric Investigation of Salinicola halophilus S28 Physiological Response Provides Solid Evidence for Its Uncommon and High Ability to Face Salt-Stress Conditions
Abstract
:1. Introduction
2. Materials and Methods
2.1. Microorganisms and Culture Conditions
2.2. Liquid Cultures
2.3. Flow Cytometric Analysis
2.4. Statistical Data Analysis
3. Results and Discussion
3.1. Growth in Liquid Medium at Different NaCl Concentrations
3.2. Physiological Response at Increasing NaCl Concentrations
4. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Kushner, D.J. Life in high salt and solute concentrations: Halophilic bacteria. In Microbial Life in Extreme Environments; Kushner, D.J., Ed.; Academic Press: London, UK, 1978; pp. 317–318. [Google Scholar]
- Margesin, R.; Schinner, F. Potential of halotolerant and halophilic microorganisms for biotechnology. Extremophiles 2001, 5, 73–83. [Google Scholar] [CrossRef] [PubMed]
- Ollivier, B.; Caumette, P.; Garcia, J.L.; Mah, R.A. Anaerobic bacteria from hypersaline environments. Microbiol. Rev. 1994, 58, 27–38. [Google Scholar] [CrossRef] [PubMed]
- Pesciaroli, C.; Cupini, F.; Selbmann, L.; Barghini, P.; Fenice, M. Temperature preferences of bacteria isolated from seawater collected in Kandalaksha Bay, White Sea, Russia. Polar. Biol. 2012, 35, 435–445. [Google Scholar] [CrossRef]
- Barghini, P.; Pasqualetti, M.; Gorrasi, S.; Fenice, M. Bacteria from the “Saline di Tarquinia” marine salterns reveal very atypical growth profiles with regards to salinity and temperature. Mediterr. Mar. Sci. 2018, 19, 513–525. [Google Scholar] [CrossRef]
- Barghini, P.; Aquilanti, A.; Silvi, S.; Gorrasi, S.; Juarez-Jimenez, B.; Cordova-Salas, K.; Fenice, M. Study on the Bacterial Diversity of the Productive Marine Salterns ‘Saline di Trapani-Paceco’, Trapani, Italy. J. Environ. Prot. Ecol. 2015, 16, 1389–1396. [Google Scholar]
- Ventosa, A.; Fernández, A.B.; León, M.J.; Sánchez-Porro, C.; Rodriguez-Valera, F. The Santa Pola Saltern as a Model for Studying the Microbiota of Hypersaline Environments. Extremophiles 2014, 18, 811–824. [Google Scholar] [CrossRef]
- Gorrasi, S.; Franzetti, A.; Ambrosini, R.; Pittino, F.; Pasqualetti, M.; Fenice, M. Spatio-temporal variation of the bacterial communities along a salinity gradient within a thalassohaline environment (Saline di Tarquinia salterns, Italy). Molecules 2021, 26, 1338. [Google Scholar] [CrossRef]
- Song, T.; Liang, Q.; Du, Z.; Wang, X.; Chen, G.; Du, Z.; Mu, D. Salinity Gradient Controls Microbial Community Structure and Assembly in Coastal Solar Salterns. Genes 2022, 13, 385. [Google Scholar] [CrossRef] [PubMed]
- Barghini, P.; Giovannini, V.; Fenice, M.; Gorrasi, S.; Pasqualetti, M. High lutein production by a halo-tolerant strain of Dunaliella sp. (Chlorophyceae) isolated from solar salterns in central Italy. J. Environ. Prot. Ecol. 2018, 19, 704–712. [Google Scholar]
- Sultanpuram, V.R.; Mothe, T. Microbial Ecology of Saline Ecosystems. In Microorganisms in Saline Environments: Strategies and Functions; Giri, B., Varma, A., Eds.; Springer: Cham, Switzerland, 2019; Volume 56. [Google Scholar] [CrossRef]
- Gorrasi, S.; Pasqualetti, M.; Franzetti, A.; Pittino, F.; Fenice, M. Vibrio communities along a salinity gradient within a marine saltern hypersaline environment (Saline di Tarquinia, Italy). Environ. Microbiol. 2020, 22, 4356–4366. [Google Scholar] [CrossRef]
- Gorrasi, S.; Pasqualetti, M.; Franzetti, A.; Gonzalez-Martinez, A.; Gonzalez-Lopez, J.; Muñoz-Palazon, B.; Fenice, M. Persistence of Enterobacteriaceae drawn into a marine saltern (Saline di Tarquinia, Italy) from the adjacent coastal zone. Water 2021, 13, 1443. [Google Scholar] [CrossRef]
- Durán-Viseras, A.; Sánchez-Porro, C.; Ventosa, A. Genomic insights into new species of the genus Halomicroarcula reveals potential for new osmoadaptative strategies in halophilic Archaea. Front. Microbiol. 2021, 12, 3336. [Google Scholar] [CrossRef]
- Gorrasi, S.; Pasqualetti, M.; Braconcini, M.; Muñoz-Palazon, B.; Fenice, M. Could Pontimonas Harbour Halophilic Members Able to Withstand Very Broad Salinity Variations? Microorganisms 2022, 10, 790. [Google Scholar] [CrossRef] [PubMed]
- Reboleiro-Rivas, P.; Juarez-Jimenez, B.; Martinez-Toledo, M.V.; Rodelas, M.; Andrade, L.; Gonzalez-Lopez, J.; Fenice, M. Bacterial Communities Structure in a High Mountain Lake During the Ice-free Season: Cultural and PCR-TGGE Investigations. Int. J. Environ. Res. 2013, 7, 685–696. [Google Scholar]
- Andrade, L.; González-López, J.; Fenice, M.; Martínez-Toledo, M.V.; Pesciaroli, C.; Maza-Márquez, P.; Juárez-Jiménez, B. Application of Response Surface Methodology (RSM) for Culture Conditions and Biomass Production of Psychrophilic Microalgae Isolated from High Mountains Lake During the Ice-free Season. Int. J. Environ. Res. 2014, 8, 799–812. [Google Scholar] [CrossRef]
- Gorrasi, S.; Pesciaroli, C.; Barghini, P.; Pasqualetti, M.; Fenice, M. Structure and Diversity of the Bacterial Community of an Arctic Estuarine System (Kandalaksha Bay) Subject to Intense Tidal Currents. J. Mar. Syst. 2019, 196, 77–85. [Google Scholar] [CrossRef]
- Barghini, P.; Pasqualetti, M.; Gorrasi, S.; Fenice, M. Study of Bacterial Diversity of a Saltern Crystallisation Pond (‘Saline di Tarquinia’, Italy) and Its Correlation with Salinity Variations. J. Environ. Prot. Ecol. 2018, 19, 139–145. [Google Scholar]
- Aguilera, M.; Cabrera, A.; Incerti, C.; Fuentes, S.; Russell, N.J.; Ramos-Cormenzana, A.; Monteoliva-Sánchez, M. Chromohalobacter salarius sp. nov., a moderately halophilic bacterium isolated from a solar saltern in Cabo de Gata, Almeria, southern Spain. Int. J. Syst. Evol. Microbiol. 2007, 57, 1238–1242. [Google Scholar] [CrossRef]
- Kim, K.K.; Jin, L.; Yang, H.C.; Lee, S.T. Halomonas gomseomensis sp. nov., Halomonas janggokensis sp. nov., Halomonas salaria sp. nov. and Halomonas denitrificans sp. nov., moderately halophilic bacteria isolated from saline water. Int. J. Syst. Evol. Microbiol. 2007, 57, 675–681. [Google Scholar] [CrossRef] [PubMed]
- Lepcha, R.T.; Poddar, A.; Schumann, P.; Das, S.K. Comparative 16S rRNA signatures and multilocus sequence analysis for the genus Salinicola and description of Salinicola acroporae sp. nov., isolated from coral Acropora digitifera. Antonie Van Leeuwenhoek 2015, 108, 59–73. [Google Scholar] [CrossRef]
- del Rocío Mora-Ruíz, M.; Font-Verdera, F.; Díaz-Gil, C.; Urdiaín, M.; Rodríguez-Valdecantos, G.; González, B.; Orfila, A.; Rosselló-Móra, R. Moderate halophilic bacteria colonizing the phylloplane of halophytes of the subfamily Salicornioideae (Amaranthaceae). Syst. Appl. Microbiol. 2015, 38, 406–416. [Google Scholar] [CrossRef]
- Plotnikova, E.G.; Anan’ina, L.N.; Ariskina, E.V.; Evtushenko, L.I. Salinicola. In Bergey’s Manual of Systematics of Archaea and Bacteria; John Wiley & Sons: New York, NY, USA, 2020; pp. 1–29. [Google Scholar] [CrossRef]
- Ambriz-Aviña, V.; Contreras-Garduño, J.A.; Pedraza-Reyes, M. Applications of flow cytometry to characterize bacterial physiological responses. Biomed. Res. Int. 2014, 2014, 461941. [Google Scholar] [CrossRef]
- Joyce, E.; Al-Hashimi, A.; Mason, T.J. Assessing the effect of different ultrasonic frequencies on bacterial viability using flow cytometry. J. Appl. Microbiol. 2011, 110, 862–870. [Google Scholar] [CrossRef] [PubMed]
- Schenk, M.; Raffellini, S.; Guerrero, S.; Blanco, G.A.; Alzamora, S.M. Inactivation of Escherichia coli, Listeria innocua and Saccharomyces cerevisiae by UV-C light: Study of cell injury by flow cytometry. LWT 2011, 44, 191–198. [Google Scholar] [CrossRef]
- Chiang, E.L.; Lee, S.; Medriano, C.A.; Li, L.; Bae, S. Assessment of physiological responses of bacteria to chlorine and UV disinfection using a plate count method, flow cytometry and viability PCR. J. Appl. Microbiol. 2022, 132, 1788–1801. [Google Scholar] [CrossRef] [PubMed]
- Ananta, E.; Heinz, V.; Knorr, D. Assessment of high pressure induced damage on Lactobacillus rhamnosus GG by flow cytometry. Food Microbiol. 2004, 21, 567–577. [Google Scholar] [CrossRef]
- Rault, A.; Béal, C.; Ghorbal, S.; Ogier, J.C.; Bouix, M. Multiparametric flow cytometry allows rapid assessment and comparison of lactic acid bacteria viability after freezing and during frozen storage. Cryobiology 2007, 55, 35–43. [Google Scholar] [CrossRef] [PubMed]
- Scoma, A.; Garrido-Amador, P.; Nielsen, S.D.; Roy, H.; Kjeldsen, K.U. The polyextremophilic bacterium Clostridium paradoxum attains piezophilic traits by modulating its energy metabolism and cell membrane composition. Appl. Environ. Microbiol. 2019, 85, e00802–e008019. [Google Scholar] [CrossRef]
- Juárez-Jiménez, B.; Manzanera, M.; Rodelas, B.; Martínez-Toledo, M.V.; Gonzalez-López, J.; Crognale, S.; Pesciaroli, C.; Fenice, M. Metabolic characterization of a strain (BM90) of Delftia tsuruhatensis showing highly diversified capacity to degrade low molecular weight phenols. Biodegradation 2010, 21, 475–489. [Google Scholar] [CrossRef] [PubMed]
- Fernández-Castané, A.; Li, H.; Thomas, O.R.T.; Overton, T.W. Flow cytometry as a rapid analytical tool to determine physiological responses to changing O2 and iron concentration by Magnetospirillum. Sci. Rep. 2017, 7, 13118. [Google Scholar] [CrossRef]
- Singh, P.K.; Kushwaha, A.; Hans, N.; Gautam, A.; Rani, R. Evaluation of the cytotoxicity and interaction of lead with lead resistant bacterium Acinetobacter junii Pb1. Braz. J. Microbiol. 2019, 50, 223–230. [Google Scholar] [CrossRef] [PubMed]
- Braschi, G.; Patrignani, F.; Siroli, L.; Lanciotti, R.; Schlueter, O.; Froehling, A. Flow cytometric assessment of the morphological and physiological changes of Listeria monocytogenes and Escherichia coli in response to natural antimicrobial exposure. Front. Microbiol. 2018, 9, 2783. [Google Scholar] [CrossRef] [PubMed]
- Baatout, S.; De Boever, P.; Mergeay, M. Temperature-induced changes in bacterial physiology as determined by flow cytometry. Ann. Microbiol. 2005, 55, 73–80. [Google Scholar]
- Cal-Sabater, P.; Caro, I.; Castro, M.J.; Cao, M.J.; Mateo, J.; Quinto, E.J. Flow cytometry to assess the counts and physiological state of Cronobacter sakazakii cells after heat exposure. Foods 2019, 8, 688. [Google Scholar] [CrossRef]
- Gandhi, A.; Shah, N.P. Effect of salt on cell viability and membrane integrity of Lactobacillus acidophilus, Lactobacillus casei and Bifidobacterium longum as observed by flow cytometry. Food Microbiol. 2015, 49, 197–202. [Google Scholar] [CrossRef]
- Kim, L.H.; Chong, T.H. Physiological responses of salinity-stressed Vibrio sp. and the effect on the biofilm formation on a nanofiltration membrane. Environ. Sci. Technol. 2017, 51, 1249–1258. [Google Scholar] [CrossRef]
- Wang, J.; Liu, Q.; Wu, B.; Hu, H.; Dong, D.; Yin, J.; Ren, H. Effect of salinity on mature wastewater treatment biofilm microbial community assembly and metabolite characteristics. Sci. Total Environ. 2020, 711, 134437. [Google Scholar] [CrossRef]
- Reis, A.; da Silva, T.L.; Kent, C.A.; Kosseva, M.; Roseiro, J.C.; Hewitt, C.J. Monitoring population dynamics of the thermophilic Bacillus licheniformis CCMI 1034 in batch and continuous cultures using multi-parameter flow cytometry. J. Biotechnol. 2005, 115, 199–210. [Google Scholar] [CrossRef]
- Silvi, S.; Barghini, P.; Aquilanti, A.; Juarez-Jimenez, B.; Fenice, M. Physiologic and metabolic characterization of a new marine isolate (BM39) of Pantoea sp. producing high levels of exopolysaccharide. Microb. Cell Fact. 2013, 12, 10. [Google Scholar] [CrossRef]
- Nebe-von Caron, G.; Badley, R.A. Bacterial characterization by flow cytometry. In Flow Cytometry Applications in Cell Culture; CRC Press: Boca Raton, FL, USA, 2020; pp. 257–290. [Google Scholar]
- Ramos-Cormenzana, A. Ecology of moderately halophilic bacteria. In The Biology of Halophilic Bacteria; Vreeland, R.H., Hochstein, L.I., Eds.; CRC Press: Boca Raton, FL, USA, 2020; pp. 55–86. [Google Scholar] [CrossRef]
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Juárez-Jiménez, B.; Fenice, M.; Pasqualetti, M.; Muñoz-Palazon, B.; Correa-Galeote, D.; Braconcini, M.; Gorrasi, S. Flow Cytometric Investigation of Salinicola halophilus S28 Physiological Response Provides Solid Evidence for Its Uncommon and High Ability to Face Salt-Stress Conditions. Microbiol. Res. 2023, 14, 454-465. https://doi.org/10.3390/microbiolres14020034
Juárez-Jiménez B, Fenice M, Pasqualetti M, Muñoz-Palazon B, Correa-Galeote D, Braconcini M, Gorrasi S. Flow Cytometric Investigation of Salinicola halophilus S28 Physiological Response Provides Solid Evidence for Its Uncommon and High Ability to Face Salt-Stress Conditions. Microbiology Research. 2023; 14(2):454-465. https://doi.org/10.3390/microbiolres14020034
Chicago/Turabian StyleJuárez-Jiménez, Belén, Massimiliano Fenice, Marcella Pasqualetti, Barbara Muñoz-Palazon, David Correa-Galeote, Martina Braconcini, and Susanna Gorrasi. 2023. "Flow Cytometric Investigation of Salinicola halophilus S28 Physiological Response Provides Solid Evidence for Its Uncommon and High Ability to Face Salt-Stress Conditions" Microbiology Research 14, no. 2: 454-465. https://doi.org/10.3390/microbiolres14020034