UV-B resistant extremotrophic and extremophilic bacteria isolated from Salinas Lake, a high Andean wetland of Peru
DOI:
https://doi.org/10.22201/ib.20078706e.2024.95.5312Keywords:
Extremophiles, Extremotrophs, UV-B resistance, Salinas LagoonAbstract
The Salinas Lagoon is a high Andean saline wetland located in the Arequipa region of southern Peru. Currently, it is subject to anthropogenic activities such as salt extraction, adventure tourism and climate change. Despite being an environment of biological importance, the diversity of microbial populations has been little explored. The location of this environment in a region with extreme UV index, altitude above 4,000 m and other adverse factors highlight this environment as a potential for the bioprospection of extremotroph and extremotrofile microorganisms. In the present study, we isolated native bacterial strains from water samples of the Salinas Lagoon and performed phenotypic
characterization at the morphological and physiological levels by means of tolerance assays to NaCl, temperature, pH and UV-B radiation. We reported halotolerant, psychrotolerant, moderate alkalophilic and UV-B radiation resistant strains and one obligate alkalophilic strain. Identification was performed by molecular analysis based on 16S rDNA.
The genera identified were Arthrobacter, Brachybacterium, Dietzia, Bacillus and Planococcus. To our knowledge, the present work is the first report on extremophilic and extremotrophic microorganisms present in the Salinas Lagoon,
promoting a new approach to survey this environment.
References
Albarracín, V. H., Gärtner, W. y Farías, M. E. (2016). Forged under the sun: life and art of extremophiles from Andean Lakes. Photochemistry and Photobiology, 92, 14–28. https://doi.org/https://doi.org/10.1111/php.12555
Albarracín, V. H., Kurth, D., Ordoñez, O. F., Belfiore, C., Luccini, E., Salum, G. M. et al. (2015). High-up: a remote reservoir of microbial extremophiles in central Andean Wetlands. Frontiers in Microbiology, 6, 01404. https://doi.org/https://doi.org/10.3389/fmicb.2015.01404
Albarracín, V. H., Pathak, G. P., Douki, T., Cadet, J., Borsarelli, C. D., Gärtner, W. et al. (2012). Extremophilic Acinetobacter strains from high-altitude lakes in Argentinean Puna: remarkable UV-B resistance and efficient DNA damage repair. Origins of Life and Evolution of Biospheres, 42, 201–221. https://doi.org/https://doi.org/10.1007/s11084-012-9276-3
Albarracín, V. H., Simon, J., Pathak, G. P., Valle, L., Douki, T., Cadet, J. et al. (2014). First characterization of a CPD-class I photolyase from a UV-resistant extremophile isolated from High-Altitude Andean Lakes. Photochemical and Photobiological Sciences, 13, 739–750. https://doi.org/https://doi.org/10.1039/C3PP50399B
Alonso-Reyes, D. G., Farías, M. E. y Albarracín, V. H. (2020). Uncovering cryptochrome/photolyase gene diversity in aquatic microbiomes exposed to diverse UV-B regimes. Aquatic Microbial Ecology, 85, 141–154. https://doi.org/https://doi.org/10.3354/ame01947
Alonso-Reyes, D. G., Galván, F. S., Portero, L. R., Alvarado, N. N., Farías, M. E., Vázquez, M. P. et al. (2021). Genomic insights into an Andean multiresistant soil actinobacterium of biotechnological interest. World Journal of Microbiology and Biotechnology, 37, 166. https://doi.org/https://doi.org/10.1007/s11274-021-03129-9
Álvarez-Campos, O., Olson, E. J., Welp, L. R., Frisbee, M. D., Zúñiga-Medina, S. A., Rodríguez, J. D. et al. (2022). Evidence for high-elevation salar recharge and interbasin groundwater flow in the Western Cordillera of the Peruvian Andes. Hydrology and Earth System Sciences, 26, 483–503. https://doi.org/https://doi.org/10.5194/hess-26-483-2022
Arya, P. y Ravindra. (2020). Metagenomics based approach to reveal the secrets of unculturable microbial diversity from aquatic environment. En S. De Mandal y P. Bhatt (Eds.), Recent advancements in microbial diversity (pp. 537–559). Cambridge: Elsevier Academic Press. https://doi.org/https://doi.org/10.1016/B978-0-12-821265-3.00022-0
Bequer-Urbano, S., Albarracín, V. H., Ordoñez, O. F., Farías, M. E. y Álvarez, H. M. (2013). Lipid storage in high-altitude Andean Lakes extremophiles and its mobilization under stress conditions in Rhodococcus sp. A5, a UV-resistant actinobacterium. Extremophiles, 17, 217–227. https://doi.org/https://doi.org/10.1007/s00792-012-0508-2
Bernard, G., Pathmanathan, J. S., Lannes, R., López, P. y Bapteste, E. (2018). Microbial dark matter investigations: how microbial studies transform biological knowledge and empirically sketch a logic of scientific discovery. Genome Biology and Evolution, 10, 707–715. https://doi.org/https://doi.org/10.1093/gbe/evy031
Blumthaler, M., Ambach, W. y Huber, M. (1993). Altitude effect of solar UV radiation dependent on albedo, turbidity, and solar elevation. Meteorologische Zeitschrift, 2, 116–120. https://doi.org/https://doi.org/10.1127/metz/2/1993/116
Bull, A. T. (2011). Actinobacteria of the Extremobiosphere. En K. Horikoshi (Ed.), Extremophiles handbook (pp. 1203–1240). Tokio: Springer. https://doi.org/https://doi.org/10.1007/978-4-431-53898-1_58
Caballero, K. C., Taya, V., Cornejo, A., Avendaño, M., Escobar, E. y Zeballos, H. (2010). Aves acuáticas de los sitios Ramsar de la Reserva Nacional de Salinas y Aguada Blanca, sur del Perú. En H. Zeballos, J. A. Ochoa, y E. López (Eds.), Diversidad biológica de la Reserva Nacional de Salinas y Aguada Blanca (pp. 33–47).Lima: Desco, PROFONANPE, SERNANP.
Cabrol, N. A., Feister, U., Häder, D. P., Piazena, H., Grin, E. A. y Klein, A. (2014). Record solar UV irradiance in the tropical Andes. Frontiers in Environmental Science, 2, 0019. https://doi.org/https://doi.org/10.3389/fenvs.2014.00019
Cabrol, N. A., Grin, E. A., Chong, G., Minkley, E., Hock, A. N., Yu, Y. et al. (2009). The High-Lakes Project. Journal of Geophysical Research: Biogeosciences, 114, 1–20. https://doi.org/https://doi.org/10.1029/2008JG000818
Castelán-Sánchez, H. G., Elorrieta, P., Romoacca, P., Liñan-Torres, A., Sierra, J. L., Vera, I. et al. (2019). Intermediate-salinity systems at high altitudes in the Peruvian Andes unveil a high diversity and abundance of bacteria and viruses. Genes, 10, 891. https://doi.org/https://doi.org/10.3390/genes10110891
Castro-Severyn, J., Pardo-Esté, C., Méndez, K. N., Fortt, J., Márquez, S., Molina, F. et al. (2021). Living to the high extreme: unraveling the composition, structure, and functional insights of bacterial communities thriving in the Arsenic-rich Salar de Huasco altiplanic ecosystem. Microbiology Spectrum, 9, e00444-21. https://doi.org/https://doi.org/10.1128/Spectrum.00444-21
Catorci, A., Piermarteri, K. y Tardella, F. M. (2014). Distribution of the nurse species Pycnophyllum molle J. Rémy and P. weberbaueri Muschl. in the Andean Dry Puna (Arequipa District — Southern Peru): role of topographic/soil variability and disturbance regime. Polish Journal of Ecology, 62, 385–390. https://doi.org/https://doi.org/10.3161/104.062.0201
Cordero, R. R., Damiani, A., Seckmeyer, G., Jorquera, J., Caballero, M., Rowe, P. et al. (2016). The solar spectrum in the Atacama Desert. Scientific Reports, 6, 22457. https://doi.org/https://doi.org/10.1038/srep22457
Dib, J., Motok, J., Fernández-Zenoff, V., Ordoñez, O. y Farías, M. E. (2008). Occurrence of resistance to antibiotics, UV-B, and Arsenic in bacteria isolated from extreme environments in high-altitude (above 4,400 m) Andean Wetlands. Current Microbiology, 56, 510–517. https://doi.org/https://doi.org/10.1007/s00284-008-9103-2
Douki, T. y Cadet, J. (2001). Individual determination of the yield of the main UV-induced dimeric pyrimidine photoproducts in DNA suggests a high mutagenicity of CC photolesions. Biochemistry, 40, 2495–2501. https://doi.org/https://doi.org/10.1021/bi0022543
Dubey, A., Malla, M. A. y Kumar, A. (2022). Role of next-generation sequencing (NGS) in understanding the microbial diversity. En A. Kumar, B. Choudhury, S. Dayanandan y M. L. Khan (Eds.), Molecular Genetics and genomics tools in biodiversity conservation (pp. 307–328). Singapur: Springer Nature.
https://doi.org/https://doi.org/10.1007/978-981-16-6005-4_16
Duckworth, A. W., Grant, W. D., Jones, B. E. y Steenbergen, R. (1996). Phylogenetic diversity of soda lake alkaliphiles. FEMS Microbiology Ecology, 19, 181–191. https://doi.org/https://doi.org/10.1111/j.1574-6941.1996.tb00211.x
Dyall-Smith, M. (Ed.). (2009). The halohandbook, protocols for haloarchaeal genetics. Recuperado el 07 de junio de, 2022 de:
https://haloarchaea.com/wp-content/uploads/2018/10/Halohandbook_2009_v7.3mds.pdf
Farías, M. E. (2020). Microbial ecosystems in central Andes extreme environments: biofilms, microbial mats, microbialites and endoevaporites. En Microbial ecosystems in Central Andes extreme environments: biofilms, microbial mats, microbialites and endoevaporites. Cham, Suiza: Springer International Publishing. https://doi.org/https://doi.org/10.1007/978-3-030-36192-1
Farías, M. E. y Contreras, M. (2018). Extremofilos y origen de la vida en Atacama. Santiago, Chile: Alvimpress.
Farías, M. E., Rascovan, N., Toneatti, D. M., Albarracín, V. H., Flores, M. R., Poiré, D. G. et al. (2013). The discovery of stromatolites developing at 3,570 m above sea level in a high-altitude volcanic Lake Socompa, Argentinean Andes. Plos One, 8, e53497. https://doi.org/https://doi.org/10.1371/journal.pone.0053497
Fernández-Zenoff, V., Heredia, J., Ferrero, M., Siñeriz, F. y Farías, M. E. (2006). Diverse UV-B resistance of culturable bacterial community from high-altitude wetland water. Current Microbiology, 52, 359–362. https://doi.org/https://doi.org/10.1007/s00284-005-0241-5
Fernández-Zenoff, V., Siñeriz, F. y Farías, M. E. (2006). Diverse responses to UV-B radiation and repair mechanisms of bacteria isolated from high-altitude aquatic environments. Applied and Environmental Microbiology, 72, 7857–7863. https://doi.org/https://doi.org/10.1128/AEM.01333-06
Flores, M. R., Ordoñez, O. F., Maldonado, M. J. y Farías, M. E. (2009). Isolation of UV-B resistant bacteria from two high altitude Andean lakes (4,400 m) with saline and non-saline conditions. The Journal of General and Applied Microbiology, 55, 447–458. https://doi.org/https://doi.org/10.2323/jgam.55.447
Gholami, M. y Etemadifar, Z. (2015). Isolation and characterization of a novel strain of genus Dietzia capable of multiple-extreme resistance. Microbiology, 84, 389–397. https://doi.org/https://doi.org/10.1134/S0026261715030054
Horikoshi, K. (2011). Extremophiles handbook (Vol. 1). Tokyo: Springer. https://doi.org/https://doi.org/10.1007/978-4-431-53898-1
INRENA (Instituto Nacional de Recursos Naturales). (2007). Plan maestro de la Reserva Nacional de Salinas y Aguada Blanca. Lima: INRENA.
Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution, 16, 111–120. https://doi.org/https://doi.org/10.1007/BF01731581
Kurth, D., Belfiore, C., Gorriti, M. F., Cortez, N., Farías, M. E. y Albarracín, V. H. (2015). Genomic and proteomic evidences unravel the UV-resistome of the poly-extremophile Acinetobacter sp. Ver3. Frontiers in Microbiology, 6, 328. https://doi.org/https://doi.org/10.3389/fmicb.2015.00328
Manya, W. F., Lizárraga, W. C., Mormontoy, C. G., Taira, M. A. y Ramírez, P. S. (2021). Complete genome sequence of Halomonas sp. strain SH5A2, a dye-degrading halotolerant bacterium isolated from the Salinas and Aguada Blanca National Reserve in Peru. Microbiology Resource Announcements, 10, e01083-20. https://doi.org/https://doi.org/10.1128/MRA.01083-20
Matallana-Surget, S., Meador, J. A., Joux, F. y Douki, T. (2008). Effect of the GC content of DNA on the distribution of UVB-induced bipyrimidine photoproducts. Photochemical and Photobiological Sciences, 7, 794–801. https://doi.org/http://doi.org/10.1039/b719929e
McKinney, C. W. y Pruden, A. (2012). Ultraviolet disinfection of antibiotic resistant bacteria and their antibiotic resistance genes in water and wastewater. Environmental Science and Technology, 46, 13393–13400. https://doi.org/https://doi.org/10.1021/es303652q
Moreno, J. R. y Albarracín, V. H. (2012). Aislamiento, cultivo e identificación de microorganismos ambientales a partir de muestras naturales. Reduca (Biología). Serie Microbiología, 5, 79–93. https://ri.conicet.gov.ar/handle/11336/17156
Negri, T., Mantri, S., Angelov, A., Peter, S., Muth, G., Eustáquio, A. S. et al. (2022). A rapid and efficient strategy to identify and recover biosynthetic gene clusters from soil metagenomes. Applied Microbiology and Biotechnology, 106, 3293–3306. https://doi.org/https://doi.org/10.1007/s00253-022-11917-y
Ordoñez, O. F., Flores, M. R., Dib, J. R., Paz, A. y Farías, M. E. (2009). Extremophile culture collection from Andean lakes: extreme pristine environments that host a wide diversity of microorganisms with tolerance to UV radiation. Microbial Ecology, 58, 461–473. https://doi.org/http://doi.org/10.1007/s00248-009-9527-7
Pfeifer, G. P. (1997). Formation and processing of UV photoproducts: effects of DNA sequence and chromatin environment. Photochemistry and Photobiology, 65, 270–283. https://doi.org/https://doi.org/10.1111/j.1751-1097.1997.tb08560.x
Portero, L. R., Alonso-Reyes, D. G., Zannier, F., Vázquez, M. P., Farías, M. E., Gärtner, W. et al. (2019). Photolyases and cryptochromes in UV-resistant bacteria from high-altitude Andean lakes. Photochemistry and Photobiology, 95, 315–330. https://doi.org/https://doi.org/10.1111/php.13061
Pullerits, K., Ahlinder, J., Holmer, L., Salomonsson, E., Öhrman, C., Jacobsson, K. et al. (2020). Impact of UV irradiation at full scale on bacterial communities in drinking water. Npj Clean Water, 3, 11. https://doi.org/https://doi.org/10.1038/s41545-020-0057-7
Rascovan, N., Maldonado, J., Vázquez, M. P. y Farías, M. E. (2016). Metagenomic study of red biofilms from Diamante Lake reveals ancient arsenic bioenergetics in haloarchaea. ISME Journal, 10, 299–309. https://doi.org/https://doi.org/10.1038/ismej.2015.109
Rasuk, M. C., Ferrer, G. M., Kurth, D., Portero, L. R., Farías, M. E. y Albarracín, V. H. (2017). UV-resistant actinobacteria from high-altitude Andean lakes: isolation, characterization and antagonistic activities. Photochemistry and Photobiology, 93, 865–880. https://doi.org/https://doi.org/10.1111/php.12759
Rasuk, M. C., Ferrer, G. M., Moreno, J. R., Farías, M. E. y Albarracín, V. H. (2016). The diversity of microbial extremophiles. En T. B. Rodrigues y A. E. Trindade (Eds.), Molecular diversity of environmental Prokaryotes (pp. 87–126). Boca Raton: CRC Press. https://doi.org/https://doi.org/10.1201/9781315381909
Saitou, N. y Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution, 4, 406–425. https://doi.org/https://doi.org/10.1093/oxfordjournals.molbev.a040454
Santos, A. L., Gomes, N. C. M., Henriques, I., Almeida, A., Correia, A. y Cunha, Â. (2012). Contribution of reactive oxygen species to UV-B-induced damage in bacteria. Journal of Photochemistry and Photobiology B: Biology, 117, 40–46. https://doi.org/https://doi.org/10.1016/j.jphotobiol.2012.08.016
Santos, A. P., Belfiore, C., Úrbez, C., Ferrando, A., Blázquez, M. A. y Farías, M. E. (2023). Extremophiles as plant probiotics to promote germination and alleviate salt stress in soybean. Journal of Plant Growth Regulation, 42, 946–959. https://doi.org/https://doi.org/10.1007/s00344-022-10605-5
Singh, O. V. y Gabani, P. (2011). Extremophiles: radiation resistance microbial reserves and therapeutic implications. Journal of Applied Microbiology, 110, 851–861. https://doi.org/https://doi.org/10.1111/j.1365-2672.2011.04971.x
Suárez-Salas, L. F., Flores-Rojas, J. L., Pereira-Filho, A. J. y Karam, H. A. (2017). Ultraviolet solar radiation in the tropical central Andes (12.0°S). Photochemical and Photobiological Sciences, 16, 954–971. https://doi.org/https://doi.org/10.1039/C6PP00161K
Sysoev, M., Grötzinger, S. W., Renn, D., Eppinger, J., Rueping, M. y Karan, R. (2021). Bioprospecting of novel extremozymes from prokaryotes— The advent of culture-independent methods. Frontiers in Microbiology, 12, 630013. https://doi.org/https://doi.org/10.3389/fmicb.2021.630013
Tamura, K., Stecher, G. y Kumar, S. (2021). MEGA11: Molecular Evolutionary Genetics Analysis Version 11. Molecular Biology and Evolution, 38, 3022–3027. https://doi.org/10.1093/molbev/msab120
Visscher, P. T., Gallagher, K. L., Bouton, A., Farías, M. E., Kurth, D., Sancho-Tomás, M. et al. (2020). Modern arsenotrophic microbial mats provide an analogue for life in the anoxic Archean. Communications Earth and Environment, 1, 1–10.
https://doi.org/https://doi.org/10.1038/s43247-020-00025-2
Warnecke, F., Sommaruga, R., Sekar, R., Hofer, J. S. y Pernthaler, J. (2005). Abundances, identity, and growth state of Actinobacteria in mountain lakes of different UV transparency. Applied and Environmental Microbiology, 71, 5551–5559. https://doi.org/https://doi.org/10.1128/AEM.71.9.5551-5559.2005
Zeballos, H., Ochoa, J. A. y Cornejo, A. (2010). La Reserva Nacional de Salinas y Aguada Blanca, una muestra representativa de la puna seca de América del Sur. En H. Zeballos, J. A. Ochoa y E. López (Eds.), Diversidad biológica de la Reserva Nacional de Salinas y Aguada Blanca (pp. 17–31). Lima: Desco/ PROFONANPE/ SERNANP.
Zha, Y., Chong, H., Yang, P. y Ning, K. (2022). Microbial dark matter: from discovery to applications. Genomics, Proteomics and Bioinformatics, 20, 867–881. https://doi.org/https://doi.org/10.1016/j.gpb.2022.02.007
