Skip to main content
Log in

Mechanism of arsenic resistance in endophytic bacteria isolated from endemic plant of mine tailings and their arsenophore production

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

Abstract

Arsenic contamination is an important environmental problem around the world since its high toxicity, and bacteria resist to this element serve as valuable resource for its bioremediation. Aiming at searching the arsenic-resistant bacteria and determining their resistant mechanism, a total of 27 strains isolated from roots of Prosopis laevigata and Spharealcea angustifolia grown in a heavy metal-contaminated region in Mexico were investigated. The minimum inhibitory concentration (MIC) and transformation abilities of arsenate (As5+) and arsenite (As3+), arsenophore synthesis, arsenate uptake, and cytoplasmatic arsenate reductase (arsC), and arsenite transporter (arsB) genes were studied for these strains. Based on these results and the 16S rDNA sequence analysis, these isolates were identified as arsenic-resistant endophytic bacteria (AREB) belonging to the genera Arthrobacter, Bacillus, Brevibacterium, Kocuria, Microbacterium, Micrococcus, Pseudomonas, and Staphylococcus. They could tolerate high concentrations of arsenic with MIC from 20 to > 100 mM for As5+ and 10–20 mM for As3+. Eleven isolates presented dual abilities of As5+ reduction and As3+ oxidation. As the most effective strains, Micrococcus luteus NE2E1 reduced 94% of the As5+ and Pseudomonas zhaodongensis NM2E7 oxidized 46% of As3+ under aerobic condition. About 70 and 44% of the test strains produced arsenophores to chelate As5+ and As3+, respectively. The AREB may absorb arsenate via the same receptor of phosphate uptake or via other way in some case. The cytoplasmic arsenate reductase and alternative arsenate reduction pathways exist in these AREB. Therefore, these AREB could be candidates for the bioremediation process.

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

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 158:126–137

    Article  CAS  Google Scholar 

  • Ahsan N, Faruque K, Shamma F, Islam N, Akhand AA (2011) Arsenic adsorption by bacteria extracellular polymeric substances. Bangladesh J Microbiol 28:80–83

    Google Scholar 

  • Anderson AR, Cook GM (2004) Isolation and characterization of arsenate-reducing Bacteria from arsenic-contaminated sites in New Zealand. Curr Microbiol 48:341–347

    Article  PubMed  CAS  Google Scholar 

  • Andrades-Moreno L, Del Castillo I, Parra R, Doukkali B, Redondo-Gómez S, Pérez-Palacios P, Rodríguez-Llorente ID (2014) Prospecting metal-resistant plant-growth promoting rhizobacteria for rhizoremediation of metal contaminated estuaries using Spartina densiflora. Environ Sci Pollut Res Int 21:3713–3721

    Article  PubMed  CAS  Google Scholar 

  • Arco-Lázaro E, Agudo I, Clemente R, Bernal MP (2016) Arsenic (V) adsorption-desorption in agricultural and mine soils: effects of organic matter addition and phosphate competition. Environ Pollut 216:71–79

    Article  PubMed  CAS  Google Scholar 

  • Baker AJM (1981) Accumulators and excluders-strategies in the response of plants to heavy metals. J Plant Nutr 3:643–654

    Article  CAS  Google Scholar 

  • Behera KK (2014) Phytoremediation, transgenic plants and microbes. Sustainable Agriculture Reviews. Springer International Publishing, pp 65–85

  • Bundschuh J, Bhattacharya P, Sracek O, Mellano MF, Ramírez AE, Storniolo AR, Martín RA, Cortés J, Litter MI, Jean JS (2011) Arsenic removal from groundwater of the Chaco-Pampean plain (Argentina) using natural geological materials as adsorbents. J Environ Sci Health 46:1297–1310

    Article  CAS  Google Scholar 

  • Campanella JJ, Bitincka L, Smalley J (2003) MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences. BMC Bioinformatics 4:29

    Article  PubMed  PubMed Central  Google Scholar 

  • Carlin A, Shi W, Dey S, Rosen BP (1995) The ars operon of Escherichia coli confers arsenical and antimonial resistance. J Bacteriol 177:981–986

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chandraprabha MN, Natarajan KA (2011) Mechanism of arsenic tolerance and bioremoval of arsenic by Acidithiobacilus ferrooxidans. J Biochem Technol 3:257–265

    CAS  Google Scholar 

  • Chaney RL (1989) Toxic element accumulation in soils and crops: protecting soil fertility and agricultural food chains. In: Inorganic contaminants in the vadose zone. Springer, Berlin Heidelberg, pp 140–158

    Chapter  Google Scholar 

  • Chang JS, Kim YH, Kim KW (2008) The ars genotype characterization of arsenic-resistant bacteria from arsenic-contaminated gold–silver mines in the Republic of Korea. Appl Microbiol Biotechnol 80:155–165

    Article  PubMed  CAS  Google Scholar 

  • Chang JS, Yoon IH, Lee JH, Kim KR, An J, Kim KW (2010) Arsenic detoxification potential of aox genes in arsenite-oxidizing bacteria isolated from natural and constructed wetlands in the Republic of Korea. Environ Geochem Health 32:95–105

    Article  PubMed  CAS  Google Scholar 

  • Cherian S, Oliveira MM (2005) Transgenic plants in phytoremediation: recent advances and new possibilities. Environ Sci Technol 39:9377–9390

    Article  PubMed  CAS  Google Scholar 

  • Das S, Jean JS, Chou ML, Rathod J, Liu CC (2016) Arsenite-oxidizing bacteria exhibiting plant growth promoting traits isolated from the rhizosphere of Oryza sativa L.: Implications for mitigation of arsenic contamination in paddies. J Hazard Mater 302:10–18

    Article  PubMed  CAS  Google Scholar 

  • Dickinson NM, Baker AJ, Doronila A, Laidlaw S, Reeves RD (2009) Phytoremediation of inorganics: realism and synergies. Inter J Phytorem 11:97–114

    Article  CAS  Google Scholar 

  • Drewniak L, Matlakowska R, Rewerski B, Sklodowska A (2010) Arsenic release from gold mine rocks mediated by the activity of indigenous bacteria. Hydrometallurgy 104:437–442

    Article  CAS  Google Scholar 

  • Fitz WJ, Wenzel WW (2002) Arsenic transformations in the soil–rhizosphere–plant system: fundamentals and potential application to phytoremediation. J Biotechnol 99:259–278

    Article  PubMed  CAS  Google Scholar 

  • Franco-Hernández MO, Vásquez-Murrieta MS, Patiño-Siciliano A, Dendooven L (2010) Heavy metals concentration in plants growing on mine tailings in Central Mexico. Biores Technol 101:3864–3869

    Article  CAS  Google Scholar 

  • Gadd GM (2010) Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156:609–643

    Article  PubMed  CAS  Google Scholar 

  • Galtier N, Gouy M, Gautier C (1996) SEAVIEW and PHYLO_WIN: two graphic tools for sequence alignment and molecular phylogeny. Comput Appl Biosci 12:543–548

    PubMed  CAS  Google Scholar 

  • Ghosh P, Rathinasabapathi B, Teplitski M, Ma LQ (2015) Bacterial ability in AsIII oxidation and AsV reduction: relation to arsenic tolerance, P uptake, and siderophore production. Chemosphere 138:995–1000

    Article  PubMed  CAS  Google Scholar 

  • Govarthanan M, Lee SM, Kamala-Kannan S, Oh BT (2015a) Characterization, real-time quantification and in silico modeling of arsenate reductase (arsC) genes in arsenic-resistant Herbaspirillum sp. GW103. Res Microbiol 166:196–204

    Article  PubMed  CAS  Google Scholar 

  • Govarthanan M, Park JH, Praburaman L, Yi YJ, Cho M, Myung H, Gnanendra S, Kamala-Kannan S, Oh BT (2015b) relative expression of low molecular weight protein, tyrosine phosphatase (wzb gene) of Herbaspirillum sp. GW103 toward arsenic stress and molecular modeling. Curr Microbioi 71:311–316

    Article  CAS  Google Scholar 

  • Govarthanan M, Mythili R, Selvankumar T, Kamala-Kannan S, Rajasekar A, Chang YC (2016) Bioremediation of heavy metals using an endophytic bacterium Paenibacillus sp. RM isolated from the roots of Tridax procumbens. 3 Biotech 6:242

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gunduz O, Simsek C, Hasozbek A (2010) Arsenic pollution in the groundwater of Simav Plain, Turkey: its impact on water quality and human health. Water Air Soil Pollu 205:43–62

    Article  CAS  Google Scholar 

  • Guo H, Liu Z, Ding S, Hao C, Xiu W, Hou W (2015) Arsenate reduction and mobilization in the presence of indigenous aerobic bacteria obtained from high arsenic aquifers of the Hetao basin, Inner Mongolia. Environ Pollut 203:50–59

    Article  PubMed  CAS  Google Scholar 

  • Han YH, Fu JW, Chen Y, Rathinasabapathi B, Ma LQ (2016) Arsenic uptake, arsenite efflux and plant growth in hyperaccumulator Pteris vittata: role of arsenic-resistant bacteria. Chemosphere 144:1937–1942

    Article  PubMed  CAS  Google Scholar 

  • Han YH, Jia MR, Liu X, Zhu Y, Cao Y, Chen DL, Chen Y, Ma LQ (2017) Bacteria from the rhizosphere and tissues of As-hyperaccumulator Pteris vittata and their role in arsenic transformation. Chemosphere 186:599–606

    Article  PubMed  CAS  Google Scholar 

  • Hu S, Lu J, Jing C (2012) A novel colorimetric method for field arsenic speciation analysis. J Environ Sci 24:1341–1346

    Article  CAS  Google Scholar 

  • Jareonmit P, Sajjaphan K, Sadowsky MJ (2012) Structure and diversity of Arsenic-resistant bacteria in an old mine area of Thailand. J Microbiol Biotechnol 20:169–178

    Google Scholar 

  • Joshi DN, Flora SJS, Kalia K (2009) Bacillus sp. strain DJ-1, potent arsenic hipertolerant bacterium isolated from industrial effluent of India. J Hazard Mater 166:1500–1505

    Article  PubMed  CAS  Google Scholar 

  • Karczewska A, Bogda A, Krysiak A (2007) Arsenic in soils in the areas of former mining and mineral processing in Lower Silesia, southwestern Poland. Trace Met Other Contam Environ 9:411–440

    Article  CAS  Google Scholar 

  • Khan Z, Doty SL (2009) Characterization of bacterial endophytes of sweet potato plants. Plant Soil 322:197–207

    Article  CAS  Google Scholar 

  • Krumanova K, Nikolavska M, Groudeva V (2008) Isolation and identification of arsenic-transforming bacteria from arsenic contaminated sites in Bulgaria. Biotechnol Equip 22:721–728

    Article  Google Scholar 

  • Lampis S, Santi C, Ciurli A, Andreolli M, Vallini G (2015) Promotion of arsenic phytoextraction efficiency in the fern Pteris vittata by the inoculation of As-resistant bacteria: a soil bioremediation perspective. Front Plant Sci 6:80

    Article  PubMed  PubMed Central  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  PubMed  CAS  Google Scholar 

  • Lasat MM (2002) Phytoextraction of toxic metals. J Environ Qual 31:109–120

    Article  PubMed  CAS  Google Scholar 

  • Lett MC, Paknikar K, Lievremont D (2001) A simple and rapid method for arsenite and arsenate speciation. In: Ciminelli V. S. T. Jr., García O (eds) Biohydrometallurgy-fundamentals technology and sustainable development, Part B. Elsevier Science, New York, pp 541–546

    Google Scholar 

  • Li MS, Luo YP, Su ZY (2007) Heavy metal concentrations in soils and plant accumulation in a restored manganese mineland in Guangxi, South China. Environ Poll 147:168–175

    Article  CAS  Google Scholar 

  • Lombi E, Wenzel WW, Adriano DC (2000) Arsenic-contaminated soils: II Remedial action. In: Wise DL, Torantolo DJ, Chicon WJ, Inyang HI, Stottmeister U (eds) Remediation Engineering of Contaminated soil. Marcel Dekker, New York, pp 739–758

    Google Scholar 

  • Long X, Chen X, Chen Y, Woon-Chung WJ, Wei Z, Wu Q (2011) Isolation and characterization endophytic bacteria from hyperaccumulator Sedum alfredii Hance and their potential to promote phytoextraction of zinc polluted soil. World J Microbiol Biotechnol 27:1197–1207

    Article  CAS  Google Scholar 

  • Luo S, Wan Y, Xiao X, Guo H, Chen L, Xi Q, Zeng G, Liu C, Chen J (2011) Isolation and characterization of endophytic bacterium LRE07 from cadmium hyperaccumulator Solanum nigrum L. and its potential for remediation. Appl Microbiol Biotechnol 89:1637–1644

    Article  PubMed  CAS  Google Scholar 

  • Ma LQ, Komar KMM, Tu C, Zhang W, Cai Y, Kennelley ED (2001) A fern that hyperaccumulates arsenic. Nature 409:579

    Article  PubMed  CAS  Google Scholar 

  • Mailloux BJ, Alexandrova E, Keimowitz AR, Wovkulich K, Freyer GA, Herron M, Stolz J, Kenna TC, Pichler T, Polizzotto ML, Dong H, Bishop M, Knappett PS (2009) Microbial mineral weathering for nutrient acquisition releases arsenic. Appl Environ Microbiol 75:2558–2565

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Majumder A, Bhattacharyya K, Bhattacharyya S, Kole SC (2013) Arsenic-tolerant, arsenite-oxidising bacterial strains in the contaminated soils of West Bengal, India. Sci Total Environ 463–464:1006–1014

    Article  PubMed  CAS  Google Scholar 

  • Mallick I, Hossain ST, Sinha S, Mukherjee SK (2014) Brevibacillus sp. KUMAs2, a bacterial isolate for possible bioremediation of arsenic in rhizosphere. Ecotoxicol Environ Saf 107:236–244

    Article  PubMed  CAS  Google Scholar 

  • Mallick I, Bhattacharyya C, Mukherji S, Dey D, Sarkar SC, Mukhopadhyay UK, Ghosh A (2018) Effective rhizoinoculation and biofilm formation by arsenic immobilizing halophilic plant growth promoting bacteria (PGPB) isolated from mangrove rhizosphere: a step towards arsenic rhizoremediation. Sci Total Environ 610:1239–1250

    Article  PubMed  CAS  Google Scholar 

  • Meng YL, Liu Z, Rosen BP (2004) As(III) and Sb (III) uptake by GlpF and efflux by ArsB in Escherichia coli. J Biol Chem 279:1834–1841

    Google Scholar 

  • Mondal P, Majumder CB, Mohanty B (2008) Effects of adsorbent dose, its particle size and initial arsenic concentration on the removal of arsenic, iron and manganese from simulated ground water by Fe3+ impregnated activated carbon. J Hazard Mater 150:695–702

    Article  PubMed  CAS  Google Scholar 

  • Mukhopadhyay R, Rosen BP, Phung LT, Silver S (2002) Microbial arsenic: from geocycles to genes and enzymes. FEMS Microbiol Rev 26:311–325

    Article  PubMed  CAS  Google Scholar 

  • Nair A, Juwarkar AA, Singh SK (2007) Production and characterization of siderophores and its application in arsenic removal from contaminated soil. Water Air Soil Poll 180:199–212

    Article  CAS  Google Scholar 

  • Nriagu JO, Bhattacharya P, Mukherjee AB, Bundschuh J, Zevenhoven R, Loppert RH (2007) Arsenic in soil and groundwater: an overview. In: Bhattcharya P, Mukherjee AB, Bundschuh J, Zevenhoven R, Loeppert RH (eds) Arsenic in soil and groundwater environment. Trace metals and other contaminants in the environment. Elsevier Science Ltd, Oxford, pp 3–60

    Google Scholar 

  • Oremland RS, Stolz F (2003) The ecology of arsenic. Science 300:939–944

    Article  PubMed  CAS  Google Scholar 

  • Páez-Espino D, Tamames J, de Lorenzo V, Cánovas D (2009) Microbial responses to environmental arsenic. Biometals 22:117–130

    Article  PubMed  CAS  Google Scholar 

  • Páez-Espino D, Durante-Rodríguez G, Lorenzo V (2015) Functional coexistence of twin arsenic resistance systems in Psedomonas putida KT2440. Environ microbial 17:229–238

    Article  CAS  Google Scholar 

  • Pais I, Jones JB (2000) The Handbook of Trace Elements. St. Luice Press, Florida

    Google Scholar 

  • Parvatiyar K, Alsabbag EM, Ochsner UA, Stegemeyer MA, Smulian AG, Hwang SH, Jackson CR, McDermott TR, Hassett DJ (2005) Global analysis of cellular factors and responses involved in Pseudomonas aeruginosa resistance to arsenite. J Bacteriol 187:4853–4864

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Pearce CI, Lloyd JR, Guthrie JT (2003) The removal of colour from textile wastewater using whole bacterial cells: a review. Dyes Pigm 58:179–196

    Article  CAS  Google Scholar 

  • Pickering IJ, Prince RC, George MJ, Smith RD, George GN, Salt DE (2000) Reduction and coordination of arsenic in Indian mustard. Plant Physiol 122:1171–1178

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Prasad KS, Ramanathan AL, Paul J, Subramanian V, Prasad R (2013) Biosorption of arsenite As3+ and arsenate As5+ from aqueous solution by Arthrobacter sp. biomass. Environ Technol 34:2701–2708

    Article  PubMed  CAS  Google Scholar 

  • Qamar N, Rehman Y, Hasnain S (2017) Arsenic-resistant and plant growth promoting Firmicutes and γ-Proteobacteria species from industrially polluted irrigation water and corresponding cropland. J Appl Microbiol 123:748–758

    Article  PubMed  CAS  Google Scholar 

  • R Core Team (2012) R: a language and environment for statistical computing. Viena Austria. ISBN: 3-900051-07-0. http://www.R-project.org/

  • Rajkumar M, Prasad MNV, Freitas H, Ae N (2009) Biotechnological applications of serpentine soil bacteria for phytoremediation of trace metals. Crit Rev Biotechnol 29:120–130

    Article  PubMed  CAS  Google Scholar 

  • Ramos-Garza J, Bustamante-Brito R, De la Paz GA, Medina-Canales MG, Vásquez-Murrieta MS, Wang ET, Rodríguez-Tovar AV (2016) Isolation and characterization of yeasts associated with plants growing in heavy metals and arsenic contaminated soils. Can J Microbiol 62:307–319

    Article  PubMed  CAS  Google Scholar 

  • Rathnayake IVN, Megharaj M, Krishnamurti GSR, Bolan NS, Naidu R (2013) Heavy metal toxicity to bacteria—are the existing growth media accurate enough to determine heavy metal toxicity? Chemosphere 90:1195–1200

    Article  PubMed  CAS  Google Scholar 

  • Rocovich SE, West DA (1975) Arsenic tolerance in a population of the grass Andropogon scoparius Michx. Science 188:263–264

    Article  PubMed  CAS  Google Scholar 

  • Román-Ponce B, Li YH, Vásquez-Murrieta MS, Sui XH, Chen WF, Estrada-De los Santos P, Wang ET (2015) Brevibacterium metallicus sp. nov., an endophytic bacterium isolated from roots of Prosopis laegivata grown at the edge of a mine tailing in Mexico. Arch Microbiol 197:1151–1158

    Article  PubMed  CAS  Google Scholar 

  • Román-Ponce B, Ramos-Garza J, Vásquez-Murrieta MS, Rivera-Orduña FN, Chen WF, Yan J, Wang ET (2016) Cultivable endophytic bacteria from heavy metal (loid)-tolerant plants. Arch Microbiol 198:941–956

    Article  PubMed  CAS  Google Scholar 

  • Rosen BP, Liu Z (2009) Transport pathways for arsenic and selenium: a minireview. Enviro Int 35:512–515

    Article  CAS  Google Scholar 

  • Rosselló-Mora R, Amman R (2001) The species concept for prokaryotes. FEMS Microbiol Rev 25:39–67

    Article  PubMed  Google Scholar 

  • Schwyn B, Neilands JB (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    Article  PubMed  CAS  Google Scholar 

  • Selvankumar T, Radhika R, Mythili R, Arunprakash S, Srinivasan P, Govarthanan M, Kim H (2017) Isolation, identification and characterization of arsenic transforming exogenous endophytic Citrobacter sp. RPT from roots of Pteris vittata. 3 Biotech 7:264

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Silver S, Phung LT (2005) Genes and enzymes involved in bacterial oxidation and reduction of inorganic arsenic. Appl Environ Microbiol 71:599–608

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Singh A, Minsker BS (2008) Uncertainty-based multiobjective optimization of groundwater remediation design. W Resources Research 44

  • Singh R, Singh S, Parihar P, Singh VP, Prasad SM (2015) Arsenic contamination, consequences and remediation techniques: a review. Ecotoxicol Environ Saf 112:247–270

    Article  PubMed  CAS  Google Scholar 

  • Slaughter DC, Macur DE, Inspeek WP (2012) Inhibition of microbial arsenate reduction by phosphate. Microbiol Res 167:151–156

    Article  PubMed  CAS  Google Scholar 

  • Smedley PL, Kinniburgh DG (2002) A review of the source, behaviour and distribution of arsenic in natural waters. Appl Geochem 17:517–568

    Article  CAS  Google Scholar 

  • Stolz JF, Basu P, Santini JM, Oremland RS (2006) Arsenic and selenium in microbial metabolism. Annu Rev Microbiol 60:107–130

    Article  PubMed  CAS  Google Scholar 

  • Sun Y, Polishchuk EA, Radaja U, Cullen WR (2004) Identification and quantification of arsC genes in environment samples by using real-time PCR. J Microbiol Methods 58:335–349

    Article  PubMed  CAS  Google Scholar 

  • Tiwari S, Sarangi BK, Thul ST (2016) Identification of arsenic resistant endophytic bacteria from Pteris vittata roots and characterization for arsenic remediation application. J Environ Manag 180:359–365

    Article  CAS  Google Scholar 

  • Tsang S, Phu F, Baum MM, Poskrebyshev GA (2007) Determination of phosphate/arsenate by a modified molybdenum blue method and reduction of arsenate by S2O4 2–. Talanta 71:1560–1568

    Article  PubMed  CAS  Google Scholar 

  • Vásquez-Murrieta MS, Migueles-Garduño I, Franco-Hernández O, Govaerts B, Dendooven L (2006) C and N mineralization and microbial biomass in heavy metal-contaminated soil. E J Soil Biol 42:89–98

    Article  CAS  Google Scholar 

  • Weeger W, Lievremont D, Perret ML, Fagarde JC, Hubert M, Lett MC (1999) Oxidation of arsenite to arsenate by bacteria isolation from an aquatic environment. Biometals 12:141–149

    Article  PubMed  CAS  Google Scholar 

  • Willsky GR, Malamy MH (1980) Effect of arsenate on inorganic phosphate transport in Escherichia coli. J Bacteriol 144:366–374

    PubMed  PubMed Central  CAS  Google Scholar 

  • Wu Q, Du J, Zhuang G, Jing C (2013) Bacillus sp. SXB and Pantoea sp. IMH, aerobic As (V)-reducing bacteria isolated from arsenic-contaminated soil. J Appl Microbiol 114:713–721

    Article  PubMed  CAS  Google Scholar 

  • Xu C, Zhou T, Masayuki K, Rosen BP (1998) Metalloid resistance mechanisms in prokaryotes. J Biochem 123:16–23

    Article  PubMed  CAS  Google Scholar 

  • Xu JY, Han YH, Chen Y, Zhu LJ, Ma LQ (2016) Arsenic transformation and plant growth promotion characteristics of As-resistant endophytic bacteria from As-hyperaccumulator Pteris vittata. Chemosphere 144:1233–1240

    Article  PubMed  CAS  Google Scholar 

  • Xue XM, Yan Y, Xiong C, Raber G, Francesconi K, Pan T, Ye J, Zhu YG (2017) Arsenic biotransformation by a cyanobacterium Nostoc sp. PCC 7120. Environ Pollut 228:111–117

    Article  PubMed  CAS  Google Scholar 

  • Zhu LJ, Guan DX, Luo J, Rathinasabapathi B, Ma LQ (2014) Characterization of arsenic-resistant endophytic bacteria from hyperaccumulators Pteris vittata and Pteris multifida. Chemosphere 113:9–16

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

B. Román-Ponce, J. Ramos-Garza, I. Arroyo-Herrera, Y. Bahena-Osorio, and J. Maldonado-Hernández received scholarships support from the Consejo Nacional de Ciencia y Tecnología (CONACyT) and BEPIFI. M. S. Vásquez-Murrieta and E. T. Wang appreciate the scholarships of Comisión de Operación y Fomento de Actividades Académicas (COFAA) and Estímulos al Desempeño de los Investigadores (EDI-IPN) and Sistema Nacional de Investigadores (SNI-CONACyT).

Funding

This work was carried out under the financial support from Projects Secretaría de Investigación y Posgrado del Instituto Politécnico Nacional (SIP-IPN) 20130722 and 20130828.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to María Soledad Vásquez-Murrieta or En Tao Wang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with humans or animals performed by any of the authors.

Additional information

Communicated by Jorge Membrillo-Hernández.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PPTX 4660 KB)

Supplementary material 2 (DOCX 42 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Román-Ponce, B., Ramos-Garza, J., Arroyo-Herrera, I. et al. Mechanism of arsenic resistance in endophytic bacteria isolated from endemic plant of mine tailings and their arsenophore production. Arch Microbiol 200, 883–895 (2018). https://doi.org/10.1007/s00203-018-1495-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00203-018-1495-1

Keywords

Navigation