Skip to main content
Log in

Microbiomes in agricultural and mining soils contaminated with arsenic in Guanajuato, Mexico

  • Original Paper
  • Published:
Archives of Microbiology Aims and scope Submit manuscript

Abstract

In this report, physical and chemical properties, and total arsenic (As) concentrations were analyzed in agricultural (MASE) and mining soils (SMI) in the State of Guanajuato, México. Additionally, a metagenomic analysis of both types of soils was the bases for the identification and selection of bacteria and fungi resistant to As. The SMI soil showed higher concentration of As (39 mg kg−1) as compared to MASE soil (15 mg kg−1). The metagenome showed a total of 175,240 reads from both soils. MASE soil showed higher diversity of bacteria, while the SMI soil showed higher diversity of fungi. 16S rRNA analysis showed that the phylum Proteobacteria showed the highest proportion (39.6% in MASE and 36.4% in SMI) and Acidobacteria was the second most representative (24.2% in SMI and 11.6% in MASE). 18S rRNA analysis, showed that the phylum Glomeromycota was found only in the SMI soils (11.6%), while Ascomycota was the most abundant, followed by Basidiomycota, and Zygomycota, in both soils. Genera Bacillus and Penicillium were able to grow in As concentrations as high as 5 and 10 mM, reduced As (V) to As (III), and removed As at 9.8% and 12.1% rates, respectively. When aoxB, arsB, ACR3(1), ACR3(2,) and arrA genes were explored, only the arsB gene was identified in Bacillus sp., B. simplex, and B. megaterium. In general, SMI soils showed more microorganisms resistant to As than MASE soils. Bacteria and fungi selected in this work may show potential to be used as bioremediation agents in As contaminated soils.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Achour AR, Bauda P, Billard P (2007) Diversity of arsenite transporter genes from arsenic-resistant soil bacteria. Res Microbiol 158:128–137. https://doi.org/10.1016/j.resmic.2006.11.006

    Article  CAS  PubMed  Google Scholar 

  • Baldani J, Videira S, dos Santos Teixeira K, Reis V, Martínez de Oliveira A, Schwab S, de Souza EM, Pedraza RO, Divan Baldani VL, Hartmann A (2014) The family Rhodospirillaceae. In: Rosenberg E, Lory S, Stackebrandt E, Thompson F (eds) The prokaryotes. Springer, Berlin, pp 533–618

    Google Scholar 

  • Barns SM, Cain EC, Sommerville L, Kuske CR (2007) Acidobacteria phylum sequences in uranium-contaminated subsurface sediments greatly expand the known diversity within the phylum. Appl Environ Microbiol 73:3113–3116

    CAS  PubMed  PubMed Central  Google Scholar 

  • Battistuzzi FU, Hedges SB (2009) A major clade of prokaryotes with ancient adaptations to life on land. Mol Biol Evol 26:335–343

    CAS  PubMed  Google Scholar 

  • Benson DA, Karsch-Mizrachi I, Lipman DJ, Ostell J, Wheeler DL (2007) GenBank. Nucleic Acids Res 35:D21–D25

    CAS  PubMed  Google Scholar 

  • Blum JS, Bindi AB, Buzzelli J, Stolz JF, Oremland RS (1998) Bacillus arsenicoselenatis, sp. nov., and Bacillus selenitireducens, sp. nov.: two haloalkaliphiles from Mono Lake, California that respire oxyanions of selenium and arsenic. Arch Microbiol 171:19–30

    CAS  Google Scholar 

  • Brady NC (1984) The nature and properties of soils. Macmillan Publishing Company, New York

    Google Scholar 

  • Branco R, Francisco R, Chung AP, Morais PV (2009) Identification of an aox system that requires cytochrome c in the highly arsenic-resistant bacterium Ochrobactrum tritici SCII24. Appl Environ Microbiol 75:5141–5147

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bundschuh J, Giménez Forcada E, Guérèquiz R et al (2008) Fuentes geogénicas de arsénico y su liberación al medio ambiente. In: Bundschuh J, Pérez Carrera A, Litter M (eds) Distribución del Arsénico en las regiones Ibérica e Iberoamericana. CYTED, Iberoarsen, pp 33–48

    Google Scholar 

  • Cai L, Liu G, Rensing C, Wang G (2009) Genes involved in arsenic transformation and resistance associated with different levels of arsenic-contaminated soils. BMC Microbiol 9:1–11

    Google Scholar 

  • Campos V, Valenzuela C, Alcorta M, Escalante G, Monsaca MA (2007) Aislamiento de Bacterias Resistentes a Arsénico desde Muestras de Rocas Volcánicas de la Quebrada Camarones, Región Parinacota: Chile. Gayana 71:150–155

    Google Scholar 

  • Carrillo-Chávez A, Morton-Bermea O, González-Partida E, Rivas-Solorzano H, Oesler G, García-Meza V, Hernández E, Morale P, Cienfuegos E (2003) Environmental geochemistry of the Guanajauto Mining District, Mexico. Ore Geol Rev 23:277–297

    Google Scholar 

  • Corbera Gorotiza J, Nápoles García MC (2013) Efecto de la inoculación conjunta Bradyrhizobium elkanii-hongos MA y la aplicación de un bioestimulador del crecimiento vegetal en soya (Glycine max (L.) Merrill), cultivar INCASOY-27. Cultivos Tropicales 34:05–11

    Google Scholar 

  • Cruz-Avalos AM, Bivián-Hernández MDLÁ, Ibarra JE, Del Rincón-Castro MC (2019) High virulence of Mexican entomopathogenic fungi against fall armyworm, (Lepidoptera: Noctuidae). J Econ Entomol 112:99–107

    CAS  PubMed  Google Scholar 

  • Das S, Bora SS, Yadav R, Barooah M (2017) A metagenomic approach to decipher the indigenous microbial communities of arsenic contaminated groundwater of Assam. Genomics Data 12:89–96

    PubMed  PubMed Central  Google Scholar 

  • DOF (2002) Norma Oficial Mexicana NOM-021-SEMARNAT-2000 que establece las especificaciones de fertilidad, salinidad y clasificación de suelos, estudio, muestreo y análisis: Diario Oficial de la Federación (DOF)

  • DOF (2007) Norma Oficial Mexicana NOM-147-SEMARNAT/SSA1-2004 que establece criterios para determinar las concentraciones de remediación de suelos contaminados por arsénico, bario, berilio, cadmio, cromo hexavalente, mercurio, níquel, plata, plomo, selenio, talio y/o vanadio: Diario Oficial de la Federación (DOF)

  • EPA (2001) Trace elements in water, solids, and biosolids by inductively coupled plasma-atomic emission spectrometry Revision 5.0. US Environmental Protection Agency, Washington DC

  • Feng G, Xie T, Wang X, Bai J, Tang L, Zhao H, Wei W, Wang M, Zhao Y (2018) Metagenomic analysis of microbial community and function involved in Cd-contaminated soil. BMC Microbiol 18:11

    PubMed  PubMed Central  Google Scholar 

  • Fierer N, Lauber CL, Ramirez KS, Zaneveld J, Bradford MA, Knight R (2012) Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J 6:1007–1017

    CAS  PubMed  Google Scholar 

  • Gardes M, Bruns D (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118. https://doi.org/10.1111/j.1365-294X.1993.tb00005.x

    Article  CAS  PubMed  Google Scholar 

  • Ghosh PK, Maiti TK, Pramanik K, Ghosh SK, Mitra S, De TK (2018) The role of arsenic resistant Bacillus aryabhattai MCC3374 in promotion of rice seedlings growth and alleviation of arsenic phytotoxicity. Chemosphere 211:407–419

    CAS  PubMed  Google Scholar 

  • Gondim-Porto C (2013) Análisis microbiológico de un suelo agrícola mediterráneo tras la aplicación de lodos de depuradora urbana. Universidad Complutense de Madrid, Madrid

    Google Scholar 

  • Gu Y, Wang Y, Sun Y, Zhao K, Xiang Q, Yu X, Zhang X, Chen Q (2018) Genetic diversity and characterization of arsenic-resistant endophytic bacteria isolated from Pteris vittata, an arsenic hyperaccumulator. BMC Microbiol 18:42

    PubMed  PubMed Central  Google Scholar 

  • Habtegebriel B, Getu E, Dawd M, Seyoum E, Atnafu G, Khamis F, Hilbur Y, Ekesi S, Larsson MC (2016) Molecular characterization and evaluation of indigenous entomopathogenic fungal isolates against Sorghum Chafer, Pachnoda interrupta (Olivier) in Ethiopia. J Entomol Nematol 8:34–45

    Google Scholar 

  • Inskeep WP, Macur RE, Hamamura N, Warelow TP, Ward SA, Santini JM (2007) Detection, diversity and expression of aerobic bacterial arsenite oxidase genes. Environ Microbiol 9:934–943

    CAS  PubMed  Google Scholar 

  • Jackson CR, Dugas SL, Harrison KG (2005) Enumeration and characterization of arsenate-resistant bacteria in arsenic free soils. Soil Biol Biochem 37:2319–2322

    CAS  Google Scholar 

  • Kaneko T, Nakamura Y, Sato S, Minamisawa K, Uchiumi T, Sasamoto S, Watanabe A, Idesawa K, Iriguchi M, Kawashima K, Kohara M, Matsumoto M, Shimpo S, Tsuruoka H, Wada T, Yamada M, Tabata S (2002) Complete genomic sequence of nitrogen-fixing symbiotic bacterium Bradyrhizobium japonicum USDA110. DNA Res 9:189–197

    PubMed  Google Scholar 

  • Keikha M (2018) Williamsia spp. are emerging opportunistic bacteria. New Microbes New Infect 21:88–89

    PubMed  Google Scholar 

  • López-Pérez ME, Del Rincón-Castro MC, Muñoz-Torres C, Ruiz-Aguilar GM, Solís-Valdez S, Zanor GA (2017) Evaluación de la contaminación por elementos traza en suelos agrícolas del suroeste de Guanajuato, México. Acta Universitaria 27:10–21

    Google Scholar 

  • Loska K, Wiechula D, Korus I (2004) Metal contamination of farming soils affected by industry. Environ Int 30:159–165

    CAS  PubMed  Google Scholar 

  • Lu Y, Dong F, Deacon C, Chen HJ, Raab A, Meharg AA (2010) Arsenic accumulation and phosphorus status in two rice (Oryza sativa L.) cultivars surveyed from fields in South China. Environ Pollut 158:1536–1541

    CAS  PubMed  Google Scholar 

  • Mellado C, Campos V, Mondaca MA (2011) Distribución de genes de resistencia a arsénico en bacterias aisladas de sedimentos con concentraciones variables del metaloide. Gayana 75:131–137

    Google Scholar 

  • Mirza BS, Sorensen DL, Dupont RR, McLean JE (2017) New arsenate reductase gene (arrA) PCR primers for diversity assessment and quantification in environmental samples. Appl Environ Microbiol 83:e02725-16

    PubMed  PubMed Central  Google Scholar 

  • Mora-Donjuán CA, Burbano-Vargas ON, Méndez-Osorio C, Castro-Rojas DF (2017) Evaluación de la biodiversidad y caracterización estructural de un Bosque de Encino (Quercus L.) en la Sierra Madre del Sur, México. Revista Forestal Mesoamericana Kurú 14:68–75

    Google Scholar 

  • Mukhopadhyay R, Rosen BP (2002) Arsenate reductases in prokaryotes and eukaryotes. Environ Health Perspect 110:745–748

    CAS  PubMed  PubMed Central  Google Scholar 

  • Müller G (1969) Index of geoaccumulation in sediments of the Rhine River. GeoJournal 2:108–118

    Google Scholar 

  • Nieto-Samaniego AF, Ojeda-García AC, Alaniz-Álvarez SA, Xu S (2012) Geología de la región de Salamanca, Guanajuato, México. Bol Soc Geol Mex 64:411–425

    Google Scholar 

  • Nuñez SJ (1985) Fundamentos de edafología. Editorial de la Universidad Estatal a Distancia, Costa Rica

    Google Scholar 

  • Orberá Ratón T, Pérez Portuondo I, Ferrer Salas D, Cortés Ramos N, González Giro Z (2005) Aislamiento de cepas del genero Bacillus sp. con potencialidades para la bioprotección y la estimulación del crecimiento vegetal. Revista Cubana de Química XVII:189–195

    Google Scholar 

  • Porta J, López-Acevedo M, Roquero de Laburu C (2003) Edafología para la agricultura y el medio ambiente. Mundi-Prensa, Madrid

    Google Scholar 

  • Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:590–596

    Google Scholar 

  • Ramos-Arroyo YR, Siebe-Grabach CD (2006) Estrategia para identificar jales con potencial de riesgo ambiental en un distrito minero: estudio de caso en el Distrito de Guanajuato, México. Revista mexicana de ciencias geológicas 23:54–74

    Google Scholar 

  • Ramos-Arroyo YR, Prol-Ledesma RM, Siebe-Grabach CD (2004) Características geológicas y mineralógicas e historia de extracción del Distrito de Guanajuato, México. Posibles escenarios geoquímicos para los residuos mineros. Revista mexicana de ciencias geológicas 21:268–284

    Google Scholar 

  • Rangel-Montoya EA, Montañez Hernández LE, Luévanos Escareño MP, Luévanos Escareño MP, Balagurusamy N (2015) Impacto del arsénico en el ambiente y su transformación por microorganismos. Terra Latinoamericana 33:103–118

    Google Scholar 

  • Rodríguez R, Morales-Arredondo I, Rodríguez I (2016) Geological differentiation of groundwater threshold concentrations of arsenic, vanadium and fluorine in el bajío Guanajuatense, Mexico. Geofis Int 55–1:5–15

    Google Scholar 

  • Sait M, Davis KE, Janssen PH (2006) Effect of pH on isolation and distribution of members of subdivision 1 of the phylum acidobacteria occurring in soil. Appl Environ Microbiol 72:1852–1857

    CAS  PubMed  PubMed Central  Google Scholar 

  • Saldaña-Robles A, Saldaña-Robles N, Saldaña-Robles A, Zanor GA, Ruiz-Aguilar GM, Gutiérrez-Vaca C (2018) Efecto del fósforo en la acumulación de arsénico en cebada (Hordeum vulgare L.) por riego con agua contaminada. Agrociencia 52–3:407–418

    Google Scholar 

  • SCFI (2006) Norma Mexicana NMX-AA-132-SCFI-2006. Muestreo de suelos para la identificación y la cuantificación de metales y metaloides, y manejo de la muestra. Secretaría de Comercio y Fomento Industrial (SCFI)

  • Schüßler A, Schwarzott D, Walker C (2001) A new fungal phylum, the Glomeromycota: phylogeny and evolution. Mycol Res 105:1413–1421

    Google Scholar 

  • Shannon C (1948) The mathematical theory of communication. Press Urbana, University of Illinois, Urbana

    Google Scholar 

  • Shuhaimi M, Ali AM, Saleh NM, Yazid AM (2001) Utilisation of enterobacterial repetitive intergenic consensus (ERIC) sequence-based PCR to fingerprint the genomes of Bifidobacterium isolates and other probiotic bacteria. Biotech Lett 23:731–736

    CAS  Google Scholar 

  • Simeonova DD, Lievremont D, Lagarde F, Muller DA, Groudeva VI, Lett MC (2004) Microplate screening assay for the detection of arsenite-oxidizing and arsenate-reducing bacteria. FEMS Microbiol Lett 237:249–253

    CAS  PubMed  Google Scholar 

  • Šimonovičová A, Peťková K, Jurkovič Ľ, Ferianc P, Vojtková H, Remenár M, Kraková L, Pangallo D, Hiller E, Čerňanský S (2016) Autochthonous microbiota in arsenic-bearing technosols from Zemianske Kostoľany (Slovakia) and its potential for bioleaching and biovolatilization of arsenic. Water Air Soil Pollut 227:1–17

    Google Scholar 

  • Simpson EH (1949) Measurement of diversity. Nature 163:688

    Google Scholar 

  • Srivastava PK, Vaish A, Dwivedi S, Chakrabarty D, Singh N, Tripathi RD (2011) Biological removal of arsenic pollution by soil fungi. Sci Total Environ 409:2430–2442

    CAS  PubMed  Google Scholar 

  • Srivastava S, Verma PC, Chaudhry V, Singh N, Abhilash PC, Kumar KV, Sharma N, Singh N (2013) Influence of inoculation of arsenic-resistant Staphylococcus arlettae on growth and arsenic uptake in Brassica juncea (L.) Czern. Var. R-46. J Hazard Mater 262:1039–1047

    CAS  PubMed  Google Scholar 

  • Sumner ME (1999) Handbook of soil science. CRC Press, Boca Ratón

    Google Scholar 

  • Suresh K, Prabagaran SR, Sengupta S, Shivaji S (2004) Bacillus indicus sp. nov., an arsenic-resistant bacterium isolated from an aquifer in West Bengal, India. J Syst Evol Microbiol 54(4):1369–1375

    CAS  Google Scholar 

  • Tripti K, Sayantan D, Shardendu S, Singh DN, Tripathi AK (2014) Potential for the uptake and removal of arsenic [As (V) and As (III)] and the Reduction of As (V) to As (III) by Bacillus licheniformis (DAS1) under different stresses. Korean J Microbiol Biotechnol 42:238–248

    Google Scholar 

  • Visagie C, Houbraken J, Frisvad J, Hong SB, Klaassen C, Perrone G, Seifert K, Varga J, Yaguchi T, Samson R (2014) Identification and nomenclature of the genus Penicillium. Stud Mycol 78:343–371

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    CAS  PubMed  PubMed Central  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    CAS  PubMed  PubMed Central  Google Scholar 

  • White T, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MAGD, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic Press, San Diego, pp 315–322

    Google Scholar 

  • Wu D, Zhang Z, Gao Q, Ma Y (2018) Isolation and characterization of aerobic, culturable, arsenic-tolerant bacteria from lead–zinc mine tailing in southern China. World J Microbiol Biotechnol 34:177

    PubMed  Google Scholar 

  • Yang T, Chen ML, Liu LH, Wang JH, Dasgupta PK (2012) Iron(III) modification of Bacillus subtilis membranes provides record sorption capacity for arsenic and endows unusual selectivity for As(V). Environ Sci Technol 46:2251–2256

    CAS  PubMed  Google Scholar 

  • Yoo JY et al (2016) 16S rRNA gene-based metagenomic analysis reveals differences in bacteria-derived extracellular vesicles in the urine of pregnant and non-pregnant women. Exp Mol Med 48:e208. https://doi.org/10.1038/emm.2015.110

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zanor GA, García MG, Venegas-Aguilera LE, Saldaña-Robles A, Saldaña-Robles N, Martínez-Jaime OA, Segoviano-Garfias JJN, Ramírez-Santoyo LF (2019) Sources and distribution of arsenic in agricultural soils of Central Mexico. J Soils Sediments 19–6:2795–2808

    Google Scholar 

Download references

Acknowledgements

MELP was supported by a fellowship (365607) from CONACYT (Mexico) during the development of this project.

Funding

This work was partially supported by the University of Guanajuato annual allocation.

Author information

Authors and Affiliations

Authors

Contributions

MELP and MCDRC conceived the study. MELP, GAZ, and ASR performed the research. MELP and MCDRC analyzed data and wrote MS, JEI interpreted and analyzed the data, structured and wrote the MS. All authors read and approved the manuscript.

Corresponding author

Correspondence to María Cristina Del Rincón-Castro.

Ethics declarations

Conflict of interest

Authors declare that they have no conflict of interest.

Ethical approval

This work does not involve any study with human participants or animals.

Consent to participate

All authors consent to participate.

Consent for publication

All authors consent for publication of this paper.

Additional information

Communicated by Erko Stackebrandt.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

López-Pérez, M.E., Saldaña-Robles, A., Zanor, G.A. et al. Microbiomes in agricultural and mining soils contaminated with arsenic in Guanajuato, Mexico. Arch Microbiol 203, 499–511 (2021). https://doi.org/10.1007/s00203-020-01973-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-020-01973-1

Keywords

Navigation