Skip to main content

Advertisement

SpringerLink
Log in

Bacterial biodiversity from anthropogenic extreme environments: a hyper-alkaline and hyper-saline industrial residue contaminated by chromium and iron

  • Environmental biotechnology
  • Published:
Applied Microbiology and Biotechnology Aims and scope Submit manuscript

Abstract

Anthropogenic extreme environments are among the most interesting sites for the bioprospection of extremophiles since the selection pressures may favor the presence of microorganisms of great interest for taxonomical and astrobiological research as well as for bioremediation technologies and industrial applications. In this work, T-RFLP and 16S rRNA gene library analyses were carried out to describe the autochthonous bacterial populations from an industrial waste characterized as hyper-alkaline (pH between 9 and 14), hyper-saline (around 100 PSU) and highly contaminated with metals, mainly chromium (from 5 to 18 g kg−1) and iron (from 2 to 108 g kg−1). Due to matrix interference with DNA extraction, a protocol optimization step was required in order to carry out molecular analyses. The most abundant populations, as evaluated by both T-RFLP and 16S rRNA gene library analyses, were affiliated to Bacillus and Lysobacter genera. Lysobacter related sequences were present in the three samples: solid residue and lixiviate sediments from both dry and wet seasons. Sequences related to Thiobacillus were also found; although strains affiliated to this genus are known to have tolerance to metals, they have not previously been detected in alkaline environments. Together with Bacillus (already described as a metal reducer), such organisms could be of use in bioremediation technologies for reducing chromium, as well as for the prospection of enzymes of biotechnological interest.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alam MZ, Ahmad S, Malik A (2011) Prevalence of heavy metal resistance in bacteria isolated from tannery effluents and affected soil. Environ Monit Assess 178:281–291

    Article  CAS  Google Scholar 

  • Armienta MA, Rodríguez R, Queré A, Juárez F, Ceniceros N, Aguayo A (1993) Groundwater pollution with chromium in León Valley, México. J Environ Qual 8:31–35

    Google Scholar 

  • Barton HA, Taylor NM, Lubbers BR, Pemberton AC (2006) DNA extraction from low-biomass carbonate rock: an improved method with reduced contamination and the low-biomass contaminant database. J Microbiol Methods 66:21–31

    Article  CAS  Google Scholar 

  • Bopp LH, Ehrlich HL (1988) Chromate resistance and reduction in Pseudomonas fluorescens strain LB300. Arch Microbiol 150:426–431

    Article  CAS  Google Scholar 

  • Bruce KD, Hiorns WD, Hobman JL, Osborn AM, Strike P, Ritchie DA (1992) Amplification of DNA from native populations of soil bacteria by using the polymerase chain reaction. Appl Environ Microbiol 58:3413–3416

    CAS  Google Scholar 

  • Butcher BG, Deane SM, Rawlings DE (2000) The chromosomal arsenic resistance genes of Thiobacillus ferrooxidans have an unusual arrangement and confer increased arsenic and antimony resistance to Escherichia coli. Appl Environ Microbiol 66:1826–1833

    Article  CAS  Google Scholar 

  • Campos J, Martinez-Pacheco M, Cervantes C (1995) Hexavalent-chromium reduction by a chromate-resistant Bacillus sp. strain. Ant van Leeuwenhoek 68:203–208

    Article  CAS  Google Scholar 

  • Caretta CA, Brito EMS (2011) In silico restriction analysis for identifying microbial communities in T-RFLP fingerprints. J Comp Interdisciplinary Sc (in press)

  • Chen SY, Lin J-G (2001) Bioleaching of heavy metals from sediment: significance of pH. Chemosphere 44(5):1093–1102

    Article  CAS  Google Scholar 

  • Collmer AR, Temple KT, Hinkle ME (1950) An iron-oxidizing bacterium from the acid mine drainage of some bituminous coal mines. J Bacteriol 59:317–328

    Google Scholar 

  • Desai C, Madamwar D (2006) Extraction of inhibitor-free metagenomic DNA from polluted sediments, compatible with molecular diversity analysis using adsorption and ion-exchange treatments. Bioresource Technol 98:761–768

    Article  Google Scholar 

  • Desai C, Parikh RY, Shouche YS, Madamwar D (2009) Tracking the influence of long-term chromium pollution on soil bacterial community structures by comparative analyses of 16S rRNA gene phylotypes. Res Microbiol 160:1–9

    Article  CAS  Google Scholar 

  • Elangovan R, Abhipsa S, Rohit B, Ligy P, Chandraraj K (2006) Reduction of Cr(VI) by a Bacillus sp. Biotechnol Let 28:247–252

    Article  CAS  Google Scholar 

  • Environmental Protection Agency (US EPA) Methods (1996) Test methods for evaluating solid waste SW-846, 3rd ed. Washington, DC: Office of Solid Waste. (http://www.veridianenv.com/docs/SW-846-Methodologies/Methods)

  • Fortin N, Beaumier D, Lee K, Greer CW (2004) Soil washing improves the recovery of total community DNA from polluted and high organic content sediments. J Microbiol Methods 56:181–191

    Article  CAS  Google Scholar 

  • Fujinami S, Fujisawa M (2010) Industrial applications of alkaliphiles and their enzymes—past, present and future. Environ Technol 31:845–856

    Article  CAS  Google Scholar 

  • Garbisu C, Alkorta I, Llama MJ, Serra JL (1998) Aerobic chromate reducion by Bacillus subtilis. Biodegradetion 9:133–148

    Article  CAS  Google Scholar 

  • Good IJ (1953) The population frequencies of species and the estimation of the population parameters. Biometrika 40:237–264

    Google Scholar 

  • Griffiths RI, Whiteley AS, O’donnell AG, Bailey MJ (2000) Oligonucleotide microarray for 16S rRNA gene-based detection of all recognized lineages of sulfate-reducing prokaryotes. Appl Environ Microbiol 68:5064–5081

    Google Scholar 

  • Hayward AC, Fegan N, Fegan M, Stirling GR (2010) Stenotrophomonas and Lysobacter: ubiquitous plant-associated Gammaproteobacteria of developing significance in applied microbiology. J Appl Microbiol 108:756–770

    Article  CAS  Google Scholar 

  • Herrera A, Cockell CS (2007) Exploring microbial diversity in volcanic environments: a review of methods in DNA extraction. J Microbiol Methods 70:1–12

    Article  CAS  Google Scholar 

  • Hewson I, Fuhrman JA (2006) Improved strategy for comparing microbial assemblage fingerprints. Microb Ecol 51:147–153

    Article  Google Scholar 

  • Hinoue M, Fukuda K, Wan Y, Yamauchi K, Ogawa H, Taniguchi H (2004) An effective method for extracting DNA from contaminated soil due to industrial waste. J Univ Occup Environ Health (Jpn) 26:13–21

    CAS  Google Scholar 

  • Hoshino YT, Matsumoro N (2005) Skim milk drastically improves the efficacy of DNA extraction from andisol, a volcanic ash soil. JARQ 39:247–252, http://www.jircas.affrc.go.jp

    Google Scholar 

  • Huber H, Stetter KO (1990) Thiobacillus cuprinus sp. nov., a novel facultatively organotrophic metal-mobilizing bacterium. Appl Environ Microbiol 56:315–322

    CAS  Google Scholar 

  • Ishibashi Y, Cervantes C, Silver S (1990) Chromium reduction in Pseudomonas putida. Appl Environ Microbiol 56:2268–2270

    CAS  Google Scholar 

  • Justin P, Kelly DP (1978) Metabolic changes in Thiobacillus denitrificans in anaerobic and aerobic chemostat culture. J Gen Microbiol 107:131–137

    Article  CAS  Google Scholar 

  • Katz SA, Salem H (1993) The toxicity of chromium with respect to its chemical speciation—a review. J Appl Toxicol 13(3):217–224

    Article  CAS  Google Scholar 

  • Kelly DP, Wood AP (2000) Confirmation of Thiobacillus denitrificans as a species of the genus Thiobacillus, in the subclass of the Proteobacteria, with strain NCIMB 9548 as the type strain. Int J Syst Evol Microbiol 50:547–550

    Article  Google Scholar 

  • La Montagne MG, Michel FC Jr, Holden PA, Reddy CA (2002) Evaluation of extraction and purification methods for obtaining PCR-amplifiable DNA from compost for microbial community analysis. J Microbiol Methods 49:255–264

    Article  Google Scholar 

  • Lane DJ (1991) rRNA sequencing. In Stachebrandt E, Goodfellow M (eds) Nucleic acid techniques in bacterial systematics, John Wiley & Sons, Chichester, pp 115–175

  • Lane DJ, Pace B, Olsen GJ, Stahl DA, Sogin ML (1985) Rapid determination of 16S ribosomal RNA sequences for phylogenetic analysis. Proc Natl Acad Sci USA 82:6955–6959

    Article  CAS  Google Scholar 

  • Liu M, Liu Y, Wang Y, Luo X, Dai J, Fang C (2011) Lysobacter xinjiangensis sp. nov., a moderately thermotolerant and alkalitolerant bacterium isolated from a gamma-irradiated sand soil sample. Int J Syst Evol Microbiol 61:433–437

    Article  CAS  Google Scholar 

  • Losi ME, Amrhein C, Frankenberger W Jr (1994) Factors affecting chemical and biological reduction of hexavalent chromium in soil. Environ Toxicol Chem 13:1727–1735

    Article  CAS  Google Scholar 

  • Mahony J, Chong S, Jang D, Luinstra K, Faught M, Dalby D, Sellors J, Chernesky M (1998) Urine specimens from pregnant and nonpregnant women inhibitory to amplification of Chlamydia trachomatis nucleic acid by PCR, ligase chain reaction, and transcription-mediated amplification: identification of urinary substances associated with inhibition and removal of inhibitory activity. J Clin Microbiol 36:3122–3126

    CAS  Google Scholar 

  • Mera N, Iwasaki K (2007) Use of plate-wash samples to monitor the fates of culturable bacteria in mercury- and trichloroethylene-contaminated soils. Appl Microbiol Biotechnol 77:437–445

    Article  CAS  Google Scholar 

  • Miller LG, Warner K, Baesman SM, Oremland RS, McDonald IR, Radajewski S, Murrell JC (2004) Degradation of methyl bromide and methyl chloride in soil microcosms: use of stable C isotope fractionation and stable isotope probing to identify reactions and the responsible microorganisms. Geochim Cosmochim Acta 68:3271–3283

    Article  CAS  Google Scholar 

  • Nies DH (2003) Efflux-mediated heavy metal resistance in prokaryotes. FEMS Microbiol Rev 27:313–339

    Article  CAS  Google Scholar 

  • Official Mexican Standard (NOM-052-SEMARNAT-2005) (2006) Norma Oficial Mexicana, residuos peligrosos, Diario Oficial, Tomo DCXXXIII No. 17 (http://www.glin.gov/view.action?glinID=181729)

  • Ogram A, Sayler GS, Barkay T (1987) The extraction and purification of microbial DNA from sediments. J Microbiol Methods 7:57–66

    Article  CAS  Google Scholar 

  • Paissé S, Coulon F, Goñi-Urriza M, Peperzak L, McGenity TJ, Duran R (2008) Structure of bacterial communities along a hydrocarbon contamination gradient in a coastal sediment. FEMS Microbiol Ecol 66:295–305

    Article  Google Scholar 

  • Pal A, Paul AK (2004) Aerobic chromate reduction by chromium-resistant bacteria isolated from serpentine soil. Microbiol Res 159:347–354

    Article  CAS  Google Scholar 

  • Piñon-Castillo HA, Brito EMS, Goñi-Urriza M, Guyoneaud R, Duran R, Nevarez-Moorillon G, Gutiérrez-Corona JF, Caretta CA, Reyna-López GH (2010) Hexavalent chromium reduction by bacterial consortia and pure strains from an alkaline industrial effluent. J Appl Microbiol 109:2173–2182

    Article  Google Scholar 

  • Rajendhrana J, Gunasekaran P (2008) Strategies for accessing soil metagenome for desired applications. Biotechnol Adv 26:576–590

    Article  Google Scholar 

  • Rochelle PA, Fry JC, Parkes RJ, Weightman AW (1992) DNA extraction for 16S rRNA gene analysis to determine genetic diversity in deep sediment communities. FEMS Microbiol Lett 100:59–66

    CAS  Google Scholar 

  • Sand W, Rhode K, Sobotke B, Zenneck C (1992) Evaluation of Leptospirillum ferrooxidans for leaching. Appl Environ Microbiol 58:85–92

    CAS  Google Scholar 

  • Shen H, Wang Y-T (1994) Biological reduction of chromium by E. coli. J Environ Eng 120:560–572

    Article  CAS  Google Scholar 

  • Sorokin DY, Lysenko AM, Mityushina LL, Tourova TP, Jones BE, Rainey FA, Robertson LA, Kuenen GJ (2001) Thioalkalimicrobium aerophilum gen. nov., sp nov and Thioalkalimicrobium sibericum sp nov., and Thioalkalivibrio versutus gen. nov., sp nov., Thioalkalivibrio nitratis sp nov and Thioalkalivibrio denitrificans sp nov., novel obligately alkaliphilic and obligately chemolithoautotrophic sulfur-oxidizing bacteria from soda lakes. Int J Sys Evol Microbiol, 51: 565-580

    Google Scholar 

  • Sorokin ID, Kravchenko IK, Doroshenko EV, Boulygina ES, Zadorina EV, Tourova TP, Sorokin DY (2008) Haloalkaliphilic diazotrophs in soda solonchak soils. FEMS Microbiol Ecol 65: 425–433

    Google Scholar 

  • Torsvik V, Goksyr J, Daae FL (1990) High diversity in DNA of soil bacteria. Appl Environ Microbiol 56:782–787

    CAS  Google Scholar 

  • Tsai YL, Olson BH (1991) Rapid method for direct extraction of DNA from soil and sediments. Appl Environ Microbiol 57:1070–1074

    CAS  Google Scholar 

  • Tsai YL, Olson BH (1992) Rapid method for separation of bacterial DNA from humic substances in sediments for polymerase chain reaction. App Environ Microbiol 58:2292–2295

    CAS  Google Scholar 

  • Tuovinen OH, Niemelä SI, Gyllenberg HG (1971) Tolerance of Thiobacillus ferrooxidans to some metals. Ant van Leeuwenhoek 37:489–496

    Article  Google Scholar 

  • Van Elsas JD, Mäntynen V, Wolters AC (1997) Soil DNA extraction and assessment of the fate of Mycobacterium chlorophenolicum strain PCP-1 in different soils by 16S ribosomal RNA gene sequence based most-probable-number PCR and immunofluorescence. Biol Fertil Soils 24:188–195

    Article  Google Scholar 

  • Whitehouse CA, Hotte HE (2007) Comparison of five commercial DNA extraction kits for the recovery of Francisella tularensis DNA from spiked soil samples. Mol Cell Probes 21:92–96

    Article  CAS  Google Scholar 

  • Yassin AF, Chen W-M, Hupfer H, Siering C, Kroppenstedt RM, Arun AB, Lai W-A, Shen F-T, Rekha PD, Young CC (2007) Lysobacter defluvii sp. nov., isolated from municipal solid waste. Int J Sys Evol Microbiol 57:1131-1136

    Google Scholar 

  • Zhou J, Bruns MA, Tiedje JM (1996) DNA recovery from soils of diverse composition. Appl Environ Microbiol 62:316–322

    CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by Grants from ECOS-NORD-SEP-CONACyT-ANUIES (M07A01) and FONCICyT (BIOCHROME project Ref. 95887). We acknowledge the financial support by the Aquitaine Regional Government Council (France). H.A. Piñón-Castillo received a fellowship from CONACyT, Mexico.

Author information

Authors and Affiliations

  1. Grupo de Ingeniería Ambiental, Departamento de Ingeniería Civil, División de Ingenierías, Universidad de Guanajuato, Guanajuato, Guanajuato, Mexico

    Elcia M. S. Brito

  2. Departamento de Biología, División de Ciencias Naturales y Exactas, Universidad de Guanajuato, Guanajuato, Guanajuato, Mexico

    Hilda A. Piñón-Castillo, J. Félix Gutiérrez-Corona & Georgina E. Reyna-López

  3. Equipe Environnement et Microbiologie—UMR IPREM5254, Université de Pau et des Pays de l’Adour, Pau Cedex, France

    Rémy Guyoneaud, Robert Duran, Anne Fahy & Marisol Goñi-Urriza

  4. Departamento de Astronomía, División de Ciencias Naturales y Exactas, Universidad de Guanajuato, Guanajuato, Guanajuato, Mexico

    César A. Caretta

  5. Facultad de Ciencias Químicas, Universidad Autónoma de Chihuahua, Chihuahua, Chih, Mexico

    G. Virginia Nevárez-Moorillón

Authors
  1. Elcia M. S. Brito
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hilda A. Piñón-Castillo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Rémy Guyoneaud
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. César A. Caretta
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. J. Félix Gutiérrez-Corona
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Robert Duran
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Georgina E. Reyna-López
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. G. Virginia Nevárez-Moorillón
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Anne Fahy
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Marisol Goñi-Urriza
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Elcia M. S. Brito.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Brito, E.M.S., Piñón-Castillo, H.A., Guyoneaud, R. et al. Bacterial biodiversity from anthropogenic extreme environments: a hyper-alkaline and hyper-saline industrial residue contaminated by chromium and iron. Appl Microbiol Biotechnol 97, 369–378 (2013). https://doi.org/10.1007/s00253-012-3923-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-012-3923-5

Keywords

Search

Navigation