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Cultivable endophytic bacteria from heavy metal(loid)-tolerant plants

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Abstract

To evaluate the interactions among endophytes, plants and heavy metal/arsenic contamination, root endophytic bacteria of Prosopis laevigata (Humb and Bonpl. ex Willd) and Sphaeralcea angustifolia grown in a heavy metal(loid)-contaminated zone in San Luis Potosi, Mexico, were isolated and characterized. Greater abundance and species richness were found in Prosopis than in Sphaeralcea and in the nutrient Pb–Zn-rich hill than in the poor nutrient and As–Cu-rich mine tailing. The 25 species identified among the 60 isolates formed three groups in the correspondence analysis, relating to Prosopis/hill (11 species), Prosopis/mine tailing (4 species) and Sphaeralcea/hill (4 species), with six species ungrouped. Most of the isolates showed high or extremely high resistance to arsenic, such as ≥100 mM for As(V) and ≥20 mM for As(III), in mineral medium. These results demonstrated that the abundance and community composition of root endophytic bacteria were strongly affected by the concentration and type of the heavy metals and metalloids (arsenic), as well as the plant species.

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References

  • Achari GA, Rasmesh R (2014) Diversity, biocontrol and plant growth promoting abilities of xylem residing bacteria from Solanaceous crops. Int J Microbiol 2014:114

    Article  Google Scholar 

  • Agrawal J, Sherameti I, Varma A (2011) Detoxification of heavy metals: state of art. In: Sherameti I, Varma A (eds) Detoxification of heavy metals. Springer, Heidelberg

    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 

  • Ali S, Charles TC, Glick BR (2014) Amelioration of high salinity stress damage by plant growth-promoting endophytes that contain ACC deaminase. Plant Physiol Biochem 80:160–167

    Article  CAS  PubMed  Google Scholar 

  • Altimira F, Yáñez C, Bravo G, González M, Rojas LA, Seeger M (2012) Characterization of copper-resistant bacteria and bacterial communities from copper-polluted agricultural soils of central Chile. BMC Microbiol 12:193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arvind R, Kumur A, Eapen SJ, Ramana KU (2009) Endophytic bacterial flora in root and steam tissues of black pepper (Pipper nigrum L) genotype: isolation, identification and evolution against Phytophthora capsici. Lett Appl Microbiol 48:58–64

    Article  Google Scholar 

  • Azarbad H, Niklińska M, van Gestel CAM, van Straalen NM, Röling WFM, Laskowski R (2013) Microbial community structure and functioning along metal pollution gradients. Environ Toxicol Chem 32:1992–2002

    Article  CAS  PubMed  Google Scholar 

  • Bannert A, Kleineidam K, Wissing L, Mueller-Niggemann C, Vogelsang V, Welzl G, Cao Z, Schloter M (2011) Changes in diversity and functional gene abundances of microbial communities involved in nitrogen fixation, nitrification, and denitrification in a tidal wetland versus paddy soils cultivated for different time periods. J Appl Environ Microbiol 77:6109–6116

    Article  CAS  Google Scholar 

  • Barzanti R, Ozino F, Bazzicalupo M, Gabbrielli R, Galardi F, Gonnelli C, Mengon A (2007) Isolation and characterization of endophytic bacteria from the nickel hyperaccumulator plant Alyssum bertolonii. Microb Ecol 53:306–316

    Article  CAS  PubMed  Google Scholar 

  • Bhojiya AA, Joshi H (2012) Isolation and characterization of zinc tolerant bacteria from Zawar mines Udaipur, India. Int J Env Eng Manag 3:239–242

    Google Scholar 

  • Brocq-Rousseau D (1904) Sur un Streptothrix. Rev Bot 16:219–230

    Google Scholar 

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

    Article  Google Scholar 

  • Chen C, Wang J (2007) Response of Saccharomyces cerevisiae to lead ion stress. Appl Microbiol Biotechnol 74:683–687

    Article  CAS  PubMed  Google Scholar 

  • Chiprés JA, Castro-Lagarroitia J, Monroy MG (2007) Exploratory and spatial data analysis (EDA-SDA) for determining regional background levels and anomalies of potentially toxic elements in soil from Catorce-Matehuala, Mexico. Appl Geochem 24:1579–1589

    Article  Google Scholar 

  • Darriba D, Taboada GC, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Das S, Dash HR, Chakrabarty J (2016) Genetics basis and importance of metal resistant genes in bacteria for bioremediation of contaminated environments with toxic metal pollutants. Appl Microbiol Biotechnol 100:2967–2984

    Article  CAS  PubMed  Google Scholar 

  • Deng ZS, Zhao LF, Kong ZY, Yang WQ, Lindström K, Wang ET, Wei GH (2011) Diversity of endophytic bacteria within nodules of the Sphaerophysa salsula in different regions of Loess Plateau in China. FEMS Microbiol Ecol 76:463–475

    Article  CAS  PubMed  Google Scholar 

  • Ding T, Melcher U (2016) Influences of plant species, season and location on leaf endophytic bacterial communities of non-cultivated plants. PLoS One 11:e0150895. doi:10.1371/journal.pone.0150895

    Article  PubMed  PubMed Central  Google Scholar 

  • Ding T, Palmer MW, Melcher U (2013) Community terminal restriction fragment length polymorphisms reveal insights into the diversity and dynamics of leaf endophytic bacteria. BMC Microbiol 13:1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Espinosa-Reyes G, González-Mille DJ, Ilizaliturri-Hernández CA, Mejía-Savedra J, Cilia-López VG, Costilla-Salazar R, Díaz-Barriga F (2014) Effect of mining activities in biotic communities of Villa de la Paz, San Luis Potosí, Mexico. BioMed Res Int 2014:165046

    Article  PubMed  PubMed Central  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  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

    CAS  PubMed  Google Scholar 

  • Gamiño-Gutiérrez SP, González-Pérez CI, Gonsebatt ME, Monroy-Fernández MG (2013) Arsenic and lead contamination in urban soils of Villa de la Paz (Mexico) affected by historical mine wastes and its effect of children´s health studied by micronucleated exfoliated cells. Environ Geochem Health 35:37–51

    Article  PubMed  Google Scholar 

  • Ghush A, Maity B, Cakrabarti K, Chattopadhyay D (2007) Bacterial diversity of east Calcutta wet land area: possible identification of potential bacterial population for different biotechnological uses. Microb Ecol 54:452–459

    Article  Google Scholar 

  • Guideon S, Gascuel O (2003) A simple and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  Google Scholar 

  • Guo H, Luo S, Chen L, Xiao X, Xi Q, Wei W, Zeng G, Liu C, Wan Y, Chen J, He Y (2010) Bioremediation of heavy metals by growing hyperaccumulator endophytic bacterium Bacillus sp. L14. Biores Technol 101:8599–8605

    Article  CAS  Google Scholar 

  • Hartman WH, Richardson CJ, Vilgalys R, Bruland GL (2008) Environmental and anthropogenic controls over bacterial communities in wet-land soils. Proc Natl Acad Sci USA 105:17842–17847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hasnain S, Yasmin S, Yasmin A (1993) The effects of lead resistant Pseudomonads on the growth of Triticum aestivum seedlings under lead stress. Environ Pollut 81:179–184

    Article  CAS  PubMed  Google Scholar 

  • Idris R, Trifonava R, Puschenreiter M, Wenzel W, Sessitsch A (2004) Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goesingense. Appl Environ Microbiol 70:2667–2672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jasso-Pineda Y, Espinosa-Reyes G, González-Mille D, Razo-Soto I, Carrizales L, Torres-Dosal A, Mejía-Savedra J, Monrroy M, Ize AI, Yarto M, Díaz-Barriga F (2007) An integrated health risk assessment approach to the study of mining sites contaminated with arsenic and lead. Integr Environ Assess Manag 3:344–350

    Article  CAS  PubMed  Google Scholar 

  • Kovács G, Burghardt J, Pradella S, Schumann P, Stackebrendt E, Màrialigeti K (1999) Kocuria palustris sp. nov. and Kocuria rhizophila sp. nov., isolated from the rhizoplane of the narrow-leaved cattail (Typha angustifolia). Int J Syst Bacteriol 49:167–173

    Article  PubMed  Google Scholar 

  • Kruger MC, Bertin PN, Heipper HJ, Arséne-Ploetze F (2013) Bacterial metabolism of environmental arsenic-mechanism and biotechnological applications. Appl Microbiol Biotecnol 97:3827–3841

    Article  CAS  Google Scholar 

  • Kuiper I, Lagendijk EL, Bloemberg GV, Lugtenberg BJ (2004) Rhizoremediation: a beneficial plant-microbe interaction. Mol Plant Microbe Interact 17:6–15

    Article  CAS  PubMed  Google Scholar 

  • Kuklinsky-Sobral J, Araujo WL, Mendes R, Geraldi IO, Pizzirani-Kleiner AA, Azevedo JL (2004) Isolation and characterization of soybean-associated bacteria and their potential for plant growth promotion. Environ Microbiol 6:1244–1251

    Article  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Luo D, Zheng H, Chen Y, Wang G, Ding F (2010) Transfer characteristics of cobalt from soil to crops in the suburban areas of Fujian Province, Southeast China. J Environ Manag 91:2248–2253

    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  CAS  PubMed  Google Scholar 

  • Ma Y, Rajkumar M, Luo Y, Freitas H (2013) Phytoextraction of heavy metals polluted soil using Sedum plubizincicola inoculated with metal mobilizing Phyllobacterium myrsinacearum Rc6b. Chemosphere 93:1386–1392

    Article  CAS  PubMed  Google Scholar 

  • Machado-Estrada B, Calderón J, Moreno-Sánchez R, Rodríguez-Zavala JS (2013) Accumulation of arsenic, lead, copper and zinc and synthesis of phytochelatins by indigenous plant of mining impacted area. Environ Sci Pollut R 20:3946–3955

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marquez-Santacruz HA, Hernández-León R, Orozco-Mosqueda MC, Velázquez-Sepulveda I, Santoyo G (2010) Diversity of bacterial endophytes in roots of Mexican husk tomato plants (Physalis ixocarpa) and their detection in the rhizosphere. Gen Mol Res 9:2372–2380

    Article  CAS  Google Scholar 

  • Mastretta C, Barac T, Vangronsveld J, Newman L, Taghavi S (2006) Endophytic bacteria and their potential application to improve the phytoremediation of contaminated environments. Biotechol Genet Eng Rev 23:175–207

    Article  CAS  Google Scholar 

  • Mendoza-Gamboa EK (2007) Estudio del aislado Bacillus subtillis DAF-1. Su perfil exoenzimático y su acción antibiótica. Tesis de Maestría ENCB-IPN. (Disertation in Spanish)

  • Menna P, Hungria M, Barcellos FG, Bangel EV, Hess PN, Martínez-Romero E (2006) Molecular phylogeny based on the 16S rRNA gene of elite rhizobial strains used in Brazilian commercial inoculants. Syst Appl Microbiol 29:315–332

    Article  CAS  PubMed  Google Scholar 

  • Mohan E, Rajendran K (2014) Effect of plant promoting Microorganisms on quality seedling production on Ferronia elepharum (Curr) in semi arid region of Southern India. Int J Curr Microbiol App Sci 3:103–116

    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 Pollut 180:199–212

    Article  CAS  Google Scholar 

  • Navarro-Noya Y, Jan-Roblero J, González-Chávez MC, Hernández-Gama R, Hernández-Rodríguez CH (2010) Bacterial communities associated with the rhizosphere of pioneer plants (Bahia xylopoda and Viguiera linearis) growing on heavy metals-contaminated soils. Antonie Van Leeuwenhoek 97:335–349

    Article  CAS  PubMed  Google Scholar 

  • Pastor N, Carlier E, Andrés J, Rosas SB, Rovera M (2012) Characterization of rhizosphere bacteria for control of phytophatogenic fungi of tomato. J Environ Manag 95:5332–5337

    Google Scholar 

  • Peralta RM, Ahn C, Gillevet PM (2013) Characterization of soil bacterial community structure and physicochemical properties in created and natural wetlands. Sci Total Environ 443:725–732

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Miranda S, Cabirol N, George-Téllez R, Zamudio-Rivera LS, Fernández FJ (2007) O-CAS, a fast and universal method for siderophore detection. J Microb Methods 70:127–131

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Praveena J, Bhore SJ (2013) Identification of bacterial endophytes associated with traditional medicinal plant Tridax procumbens Linn. Anc Sci Life 32:173–177

    Article  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  CAS  PubMed  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  CAS  PubMed  Google Scholar 

  • Reva ON, Smirnov VV, Pettersson B, Priest FG (2002) Bacillus endophyticus sp. nov., isolated from the inner tissues of cotton plants (Gossypium sp.). Int J Syst Evol Microbiol 52:101–107

    Article  CAS  PubMed  Google Scholar 

  • Rohlf FJ (2000) NTSYS-pc: numerical taxonomy and multivariate analysis system, version 2.2. Exeter Software. Setauket, New York

  • 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 laevigata grown at the edge of mine tailing in Mexico. Arch Microbiol 197:1151–1158

    Article  PubMed  Google Scholar 

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

    Article  PubMed  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/

  • Schloss PD, Handelsman J (2005) Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness. Appl Environ Microbiol 71:1501–1506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shafher SM, Rogers DF (1993) Similarity and distance measures for cellular manufacturing Part II. An extension and comparison. Int J Prod Res 31:1315–1326

    Article  Google Scholar 

  • Sheng XF, Xia JJ, Jiang CY, He LY, Quian M (2008) Characterization of heavy metal-resistant endophytic bacteria from rape (Brassica napus) roots and their potential in promoting the growth and lead accumulation. Environ Pollut 156:1164–1170

    Article  CAS  PubMed  Google Scholar 

  • Shin MN, Shim J, You Y, Myung M, Bang KS, Choa M, Kamala-Kannan S, Oh BT (2012) Characterization of lead resistant endophytic Bacillus sp. MN3-4 and its potential for promoting lead accumulation in metal hyperaccumulator Alnus firma. J Hazard Mater 199–200:314–320

    Article  PubMed  Google Scholar 

  • Šilaver P, Lepš J (2014) Multivariate analysis of ecological data using CANOCO 5. Cambridge University Press, Cambridge

    Google Scholar 

  • Soufiane B, Barzet M, Côté JC (2013) Multilocus sequences analysis of Bacillus thuringiensis serovars navarrensis, bolivia, and vazensis and Bacillus weihenstephanensis reveals a common phylogeny. Antonie Van Leeuwenhoek 103:195–205

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Sun LN, Zhang YF, He LY, Chen ZJ, Wang QY, Quian M, Shen XF (2010) Genetic diversity and characterization of heavy metal-resistant-endophytic bacteria from two copper-tolerant plant species on copper mine wasteland. Biores Technol 101:501–509

    Article  CAS  Google Scholar 

  • Tenorio-Sánchez SA, Rojas-Avelizapa NG, Ibarra JE, Rojas-Avelizapa LI, Cruz-Camarillo R (2010) Characterization of Bacillus thuringensis strain isolated from a highly polychlorinated biphenyls contaminated soils. Tecnologa 3:52–63

    Google Scholar 

  • The Economist (2003) Pocket world in figures. Profile Books Ltd, London

    Google Scholar 

  • Tomova I, Lazarkevich I, Tomova A, Kambourava M, Vasileva-Tonkarva E (2013) Diversity and biosynthetic potential of culturable aerobic heterotrophic bacteria isolated from Magura Cave, Bulgaria. Int J Speoleol 42:65–76

    Article  Google Scholar 

  • Trujillo-Cabrera Y, Ponce-Mendoza A, Vásquez-Murrieta MS, Rivera-Orduña FN, Wang ET (2012) Diverse cellulolytic bacteria isolated from the high humus, alkaline-saline Chinampa soils. Ann Microbiol 63:779–792

    Article  Google Scholar 

  • Vásquez-Murrieta MS, Cruz-Mondragón C, Trujillo-Tapia N, Herrera-Arreola G, Govaerts B, Van Cleemput O, Dendooven L (2006) Nitrous oxide production of heavy metal contaminated soil. Soil Biol Biochem 38:931–940

    Article  Google Scholar 

  • Vinuesa P, Silva C, Loriete MJ, Izaguirre-Mayoral ML, Bedmar EJ, Martínez-Romero E (2005) Molecular systematic of rhizobia based on maximum likelihood and Bayesian phylogenies inferred from rrs, atpD, recA, and nifH sequences and their use in the classification of Sesbonia Microsymbionts from Venezuela wetlands. Syst Appl Microbiol 28:702–716

    Article  CAS  PubMed  Google Scholar 

  • Wang ET, Tan ZY, Guo XW, Rodríguez-Duran R, Boll G, Martínez-Romero E (2006) Diverse endophytic bacteria isolated from a leguminous tree Conzattia multiflora grown in Mexico. Arch Microbiol 186:251–259

    Article  CAS  PubMed  Google Scholar 

  • Wei G, Fan L, Zhu W, Fu Y, Yu J, Tang M (2009) Isolation and characterization of the heavy metal resistant bacteria CCNWRS33-2 isolated from root nodule of Lespedeza cuneata in gold mine tailings in China. J Hazard Mater 162:50–56

    Article  CAS  PubMed  Google Scholar 

  • Williams GP, Gnanadesigan M, Ravikumar S (2012) Biosorption and bio- kinetic studies of halobacterial strains against Ni2+, Al3+ and Hg2+ metal ions. Biores Technol 107:526–529

    Article  Google Scholar 

  • Yang HC, Rosen BP (2016) New mechanism of bacterial arsenic resistance. Biomed J 39:5–13

    Article  PubMed  Google Scholar 

  • Zhang YF, He LY, Che ZJ, Wang QY, Quian M, Sheng XF (2011) Characterization of ACC deaminase-producing endophytic bacteria isolated from copper-tolerant plants and their potential in promoting the growth and copper accumulation of Brassica napus. Chemosphere 87:57–62

    Article  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  CAS  PubMed  Google Scholar 

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Acknowledgments

We thank A. Patiño-Siliciano for identifying the plant samples. This study was funded by the Projects SIP 20130722, 20130828 and 20140124 authorized by IPN. B.R.P. received scholarships support from the CONACyT and PIFI. M.S.V.-M., F.N.R.-O. and E.T.W. appreciate the scholarships of COFAA and EDI-IPN and SNI-CONACyT.

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Communicated by Jorge Membrillo-Hernández.

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Román-Ponce, B., Ramos-Garza, J., Vásquez-Murrieta, M.S. et al. Cultivable endophytic bacteria from heavy metal(loid)-tolerant plants. Arch Microbiol 198, 941–956 (2016). https://doi.org/10.1007/s00203-016-1252-2

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