Abstract
The crater lake at “El Chichón” volcano is an extreme acid-thermal environment with high concentrations of heavy metals. In this study, two bacterial strains with the ability to resist high concentrations of arsenic (As) were isolated from water samples from the crater lake. Staphylococcus ARSC1-P and Stenotrophomonas ARSC2-V isolates were identified by use of the 16S rDNA gene. Staphylococcus ARSC1-P was able to grow in 400 mM of arsenate [As(V)] under oxic and anoxic conditions. The IC50 values were 36 and 382 mM for oxic and anoxic conditions, respectively. For its part, Stenotrophomonas ARSC2-V showed IC50 values of 110 mM and 2.15 for As(V) and arsenite [As(III)], respectively. Arsenic accumulated intracellularly in both species [11–25 nmol As × mg cellular prot−1 in cells cultured in 50 mM As(V)]. The present study shows evidence of microbes that can potentially be a resource for the bio-treatment of arsenic in contaminated sites, which highlights the importance of the “El Chichón” volcano as a source of bacterial strains that are adaptable to extreme conditions.
Similar content being viewed by others
Data Availability
All data presented in this article is available.
Code Availability
Not applicable.
References
Garbinski LD, Rosen BP, Chen J (2019) Pathways of arsenic uptake and efflux. Environ Int 126:585–597. https://doi.org/10.1016/J.ENVINT.2019.02.058
Morales-Simfors N, Bundschuh J, Herath I et al (2020) Arsenic in Latin America: a critical overview on the geochemistry of arsenic originating from geothermal features and volcanic emissions for solving its environmental consequences. Sci Total Environ 716:135564. https://doi.org/10.1016/j.scitotenv.2019.135564
Bundschuh J, Maity JP (2015) Geothermal arsenic: occurrence, mobility and environmental implications. Renew Sustain Energy Rev 42:1214–1222. https://doi.org/10.1016/j.rser.2014.10.092
Birkle P, Bundschuh J, Sracek O (2010) Mechanisms of arsenic enrichment in geothermal and petroleum reservoirs fluids in Mexico. Water Res 44:5605–5617. https://doi.org/10.1016/J.WATRES.2010.05.046
Taran Y, Rouwet D, Inguaggiato S, Aiuppa A (2008) Major and trace element geochemistry of neutral and acidic thermal springs at El Chichón volcano, Mexico. J Volcanol Geotherm Res 178:224–236. https://doi.org/10.1016/j.jvolgeores.2008.06.030
Rincón-Molina CI, Hernández-García JA, Rincón-Rosales R et al (2019) Structure and diversity of the bacterial communities in the acid and thermophilic crater-lake of the volcano “El Chichón”, Mexico. Geomicrobiol J 36:97–109. https://doi.org/10.1080/01490451.2018.1509158
Peña-Ocaña BA, Velázquez-Ríos IO, Alcántara-Hernández RJ et al (2020) Changes in the concentration of trace elements and heavy metals in el chichón crater lake active volcano. Polish J Environ Stud 30:295–304. https://doi.org/10.15244/pjoes/121045
Ovando-Chacon SL, Tacias-Pascacio VG, Ovando-Chacon GE et al (2020) Characterization of thermophilic microorganisms in the geothermal water flow of El Chichón volcano crater lake. Water (Switzerland) 12:2172. https://doi.org/10.3390/W12082172
Rincón-Molina CI, Martínez-Romero E, Ruiz-Valdiviezo VM et al (2020) Plant growth-promoting potential of bacteria associated to pioneer plants from an active volcanic site of Chiapas (Mexico). Appl Soil Ecol. https://doi.org/10.1016/J.APSOIL.2019.103390
Peña-Ocaña BA, Ovando-Ovando CI, Puente-Sánchez F et al (2022) Metagenomic and metabolic analyses of poly-extreme microbiome from an active crater volcano lake. Environ Res 203:111862. https://doi.org/10.1016/j.envres.2021.111862
Ali Z, Waheed H, Kazi AG et al (2016) Duckweed: an efficient hyperaccumulator of heavy metals in water bodies. Plant Met Interact Emerg Remediat Tech. https://doi.org/10.1016/B978-0-12-803158-2.00016-3
Gupta P (2018) Metals and micronutrients. Illustrated toxicology. Academic Press, pp 195–223
Mandal D, Sonar R, Saha I et al (2022) Isolation and identification of arsenic resistant bacteria: a tool for bioremediation of arsenic toxicity. Int J Environ Sci Technol 19:9883–9900. https://doi.org/10.1007/S13762-021-03673-9/METRICS
Shakya S, Pradhan B, Smith L et al (2012) Isolation and characterization of aerobic culturable arsenic-resistant bacteria from surfacewater and groundwater of Rautahat District. Nepal J Environ Manage 95:S250–S255. https://doi.org/10.1016/J.JENVMAN.2011.08.001
Xu S, Xu R, Nan Z, Chen P (2018) Bioadsorption of arsenic from aqueous solution by the extremophilic bacterium Acidithiobacillus ferrooxidans DLC-5. Biocatal Biotransform 37:35–43. https://doi.org/10.1080/10242422.2018.1447566
Armienta MA, Vilaclara G, De la Cruz-Reyna S et al (2008) Water chemistry of lakes related to active and inactive Mexican volcanoes. J Volcanol Geotherm Res 178:249–258. https://doi.org/10.1016/j.jvolgeores.2008.06.019
Verryckt LT, Vicca S, Van Langenhove L et al (2022) Vertical profiles of leaf photosynthesis and leaf traits and soil nutrients in two tropical rainforests in French Guiana before and after a 3-year nitrogen and phosphorus addition experiment. Earth Syst Sci Data 14:5–18. https://doi.org/10.5194/ESSD-14-5-2022
Olsen SR, Sommers LE (1983) Phosphorus. In: Page AL (ed) Methods of soil analysis, part 2, 2nd edn. John Wiley & Sons Ltd, Wisconsin, pp 403–430
Feregrino-Mondragón RD, Vega-Segura A, Sánchez-Thomas R et al (2021) The essential role of mitochondria in the consumption of waste-organic matter and production of metabolites of biotechnological interest in Euglena gracilis. Algal Res 56:102302. https://doi.org/10.1016/J.ALGAL.2021.102302
Sambrook J, Russell DW, David W (2001) Molecular cloning : a laboratory manual. Cold Spring Harbor Laboratory Press
Greenblatt CL, Schiff JA (1959) A Pheophytin-like pigment in dark-adapted Euglena gracilis. J Protozool 6:23–28. https://doi.org/10.1111/j.1550-7408.1959.tb03922.x
Macy JM, Santini JM, Pauling BV et al (2000) Two new arsenate/sulfate-reducing bacteria: mechanisms of arsenate reduction. Arch Microbiol 173:49–57
Liao V et al (2011) Arsenite-oxidizing and arsenate-reducing bacteria associated with arsenic-rich groundwater in Taiwan. J Contam Hydrol 123:20–29. https://doi.org/10.1016/j.jconhyd.2010.12.003
Lira-Silva E, Santiago-Martínez MG, García-Contreras R et al (2013) Cd2+ resistance mechanisms in Methanosarcina acetivorans involve the increase in the coenzyme M content and induction of biofilm synthesis. Environ Microbiol Rep 5:799–808. https://doi.org/10.1111/1758-2229.12080
Galkiewicz JP, Kellogg CA (2008) Cross-kingdom amplification using Bacteria-specific primers: complications for studies of coral microbial ecology. Appl Environ Microbiol. https://doi.org/10.1128/AEM.01303-08
Chen YL, Lee CC, Lin YL et al (2015) Obtaining long 16S rDNA sequences using multiple primers and its application on dioxin-containing samples. BMC Bioinform. https://doi.org/10.1186/1471-2105-16-S18-S13
Morton-Bermea O, Armienta M, Ramos S (2010) Rare-earth element distribution in water from El Chichón Volcano Crater Lake. Geof Int, Chiapas Mexico. https://doi.org/10.22201/igeof.00167169p.2010.49.1.1474
Rouwet D, Taran Y, Inguaggiato S et al (2008) Hydrochemical dynamics of the “lake-spring” system in the crater of El Chichón volcano (Chiapas, Mexico). J Volcanol Geotherm Res 178:237–248. https://doi.org/10.1016/j.jvolgeores.2008.06.026
Taran Y, Rouwet D (2008) Estimating thermal inflow to El Chichón crater lake using the energy-budget, chemical and isotope balance approaches. J Volcanol Geotherm Res 175:472–481. https://doi.org/10.1016/j.jvolgeores.2008.02.019
Taran YA, Peiffer L (2009) Hydrology, hydrochemistry and geothermal potential of El Chichón volcano-hydrothermal system, Mexico. Geothermics 38:370–378. https://doi.org/10.1016/J.GEOTHERMICS.2009.09.002
Armienta MA, De la Cruz-Reyna S, Ramos S et al (2014) Hydrogeochemical surveillance at El Chichón volcano crater lake, Chiapas, Mexico. J Volcanol Geotherm Res 285:118–128. https://doi.org/10.1016/j.jvolgeores.2014.08.011
Cuoco E, De Francesco S, Tedesco D (2013) Hydrogeochemical dynamics affecting steam-heated pools at El Chichón Crater (Chiapas—Mexico). Geofluids 13:331–343. https://doi.org/10.1111/gfl.12028
Quatrini R, Johnson DB (2018) Microbiomes in extremely acidic environments: functionalities and interactions that allow survival and growth of prokaryotes at low pH. Curr Opin Microbiol 43:139–147. https://doi.org/10.1016/J.MIB.2018.01.011
Macur RE, Jay ZJ, Taylor WP et al (2013) Microbial community structure and sulfur biogeochemistry in mildly-acidic sulfidic geothermal springs in Yellowstone National Park. Geobiology 11:86–99. https://doi.org/10.1111/gbi.12015
Héry M, Herrera A, Vogel TM et al (2005) Effect of carbon and nitrogen input on the bacterial community structure of Neocaledonian nickel mine spoils. FEMS Microbiol Ecol 51:333–340. https://doi.org/10.1016/J.FEMSEC.2004.09.008
Dean WE (2006) Characterization of organic matter in lake sediments from Minnesota and Yellowstone National Park. Open-File Rep. https://doi.org/10.3133/OFR20061053
Oliveira A, Pampulha ME, Neto MM, Almeida AC (2009) Enumeration andcharacterization of arsenic-tolerant diazotrophic bacteria in a long-term heavy-metal-contaminated soil. Water Air Soil Pollut. https://doi.org/10.1007/s11270-008-9907-5
Patel A, Tiwari S, Prasad SM (2021) Arsenate and arsenite-induced inhibition and recovery in two diazotrophic cyanobacteria Nostoc muscorum and Anabaena sp: study on time-dependent toxicity regulation. Environ Sci Pollut Res 28:51088–51104. https://doi.org/10.1007/S11356-021-13800-1
Crognale S, Zecchin S, Amalfitano S et al (2017) Phylogenetic structure and metabolic properties of microbial communities in Arsenic-rich waters of geothermal origin. Front Microbiol 8:2468. https://doi.org/10.3389/fmicb.2017.02468
Li X, Pan JF, Lu Z et al (2021) (2021) Arsenate toxicity to the marine microalga Chlorella vulgaris increases under phosphorus-limited condition. Environ Sci Pollut Res 2836(28):50908–50918. https://doi.org/10.1007/S11356-021-14318-2
Joshi DN, Flora SJS, Kalia K (2009) Bacillus sp. strain DJ-1, potent arsenic hypertolerant bacterium isolated from the industrial effluent of India. J Hazard Mater 166:1500–1505. https://doi.org/10.1016/j.jhazmat.2008.12.127
Sher S, Zajif Hussain S, Rehman A (2020) Multiple resistance mechanisms in Staphylococcus sp. strain AS6 under arsenite stress and its potential use in amelioration of wastewater. J King Saud Univ—Sci 32:3052–3058. https://doi.org/10.1016/J.JKSUS.2020.08.012
Biswas R, Majhi AK, Sarkar A (2019) The role of arsenate reducing bacteria for their prospective application in arsenic contaminated groundwater aquifer system. Biocatal Agric Biotechnol 20:101218. https://doi.org/10.1016/j.bcab.2019.101218
Anderson CR, Cook GM (2004) Isolation and characterization of arsenate-reducing bacteria from arsenic-contaminated sites in New Zealand. Curr Microbiol 48:341–347. https://doi.org/10.1007/s00284-003-4205-3
Slyemi D, Bonnefoy V (2011) How prokaryotes deal with arsenic†. Environ Microbiol Rep 4:no-no. https://doi.org/10.1111/j.1758-2229.2011.00300.x
Rodríguez-Martín D, Murciano A, Herráiz M et al (2022) Arsenate and arsenite differential toxicity in Tetrahymena thermophila. J Hazard Mater 431:128532. https://doi.org/10.1016/J.JHAZMAT.2022.128532
Kumar P, Dash B, Suyal DC et al (2021) Characterization of arsenic-resistant Klebsiella pneumoniae RnASA11 from contaminated soil and water samples and its bioremediation potential. Curr Microbiol 78:3258–3267. https://doi.org/10.1007/S00284-021-02602-W
Acknowledgements
Authors thank to Dr. Josef Galthier Roblero Lucchetti for his comments regarding grammar and structure of this manuscript.
Funding
This work was supported by CONACyT grant CB-253281(VM-RV), and Project No. 14277.22-P from the ‘Tecnológico Nacional de Mexico’ funds (TecNM, México). We would like to thank CONACyT for the doctoral fellowship assigned to C. I. Ovando-Ovando (No. 766260).
Author information
Authors and Affiliations
Contributions
“All authors contributed to the study conception and design, as well as to analyzing all data. Material preparation and developed experiments were performed by CIO-O and RD F-M Collection of data was carried out by RJ-C, VMR-V, and CIO-O, who were also in charge of writing the first draft. The last version was composed and reviewed by CIO-O, RDF-M, RR-R, RJ-C and VMR-V. Biological material collection was performed by CIO-O and VMR-V. All authors commented on previous versions of the manuscript. All authors read, discussed, and approved the final manuscript.
Corresponding authors
Ethics declarations
Competing interest
All authors certify that they have neither affiliations nor involvement with any organization or entity. They also have no financial or non-financial interests in regards to the research subject and to the materials discussed in this manuscript.
Ethical Approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Consent to Participate
Not applicable.
Consent for Publication
Not applicable.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Ovando-Ovando, C.I., Feregrino-Mondragón, R.D., Rincón-Rosales, R. et al. Isolation and Identification of Arsenic-Resistant Extremophilic Bacteria from the Crater-Lake Volcano “El Chichon”, Mexico. Curr Microbiol 80, 257 (2023). https://doi.org/10.1007/s00284-023-03327-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00284-023-03327-8