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Plants as extreme environments? Ni-resistant bacteria and Ni-hyperaccumulators of serpentine flora

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Abstract

During recent years there has been an increasing interest in the bacterial communities occurring in unusual, often extreme, environments. On serpentine outcrops around the world, a high diversity of plant species showing the peculiar features of metal hyperaccumulation is present. These metal hyperaccumulators have received much attention for their potential biotechnological exploitation in phytoremediation processes, but also as unusual, extreme habitats for the associated bacterial flora, which could reveal novel details concerning bacterial adaptation. This paper will briefly focus on the research topics that have been addressed to date on bacteria associated with serpentine plants and aims to provide a state of the art and to present possible future directions for research which could lead to new insights on microbial adaptation and evolution, and potentially applied in technologies for sustainable use and remediation of contaminated land.

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References

  • Abou-Shanab RA, Angle JS, Delorme TA, Chaney RL, van Berkum P, Moawad H, Ghanem K, Ghozlan HA (2003a) Rhizobacterial effects on nickel extraction from soil and uptake by Alyssum murale. New Phytol 158:219–224

    CAS  Google Scholar 

  • Abou-Shanab RI, Delorme TA, Angle JS, Chaney RL, Ghanem K, Moawad H, Ghozlan HA (2003b) Phenotypic characterization of microbes in the rhizosphere of Alyssum murale. Int J Phytorem 5:367–379

    CAS  Google Scholar 

  • Abou-Shanab RAI, Angle JS, Chaney RL (2006) Bacterial inoculants affecting nickel uptake by Alyssum murale from low, moderate and high Ni soils. Soil Biol Biochem 38:2882–2889

    CAS  Google Scholar 

  • Abou-Shanab RA, van Berkum P, Angle JS (2007a) Heavy metal resistance and genotypic analysis of metal resistance genes in gram-positive and gram-negative bacteria present in Ni-rich serpentine soil and in the rhizosphere of Alyssum murale. Chemosphere 68:360–367

    CAS  PubMed  Google Scholar 

  • Abou-Shanab RAI, Angle JS, van Berkum P (2007b) Chromate-tolerant bacteria for enhanced metal uptake by Eichornia crassipes (Mart.). Int J Phytorem 9:91–105

    CAS  Google Scholar 

  • Abou-Shanab RA, Ghanem K, Ghanem N, Al-Kolaibe A (2008) The role of bacteria on heavy-metal extraction and uptake by plants growing on multi-metal-contaminated soils. W J Microbiol Biotechnol 24:253–262

    CAS  Google Scholar 

  • Aboudrar W, Schwartz C, Benizri E, Morel JL, Boularbah A (2007) Soil microbial diversity as affected by the rhizosphere of the hyperaccumulator Thlaspi caerulescens under natural conditions. Int J Phytorem 9:41–52

    CAS  Google Scholar 

  • Andersson AF, Lindberg M, Jakobsson H, Backhed F, Nyren P, Engstrand L (2008) Comparative analysis of human gut microbiota by barcoded pyrosequencing. PLoS ONE 3:e2836

    PubMed  Google Scholar 

  • Anderson TR, Howes AW, Slatter K, Dutton MF (1997) Studies on the nickel hyperaccumulator Berkheya coddii. In: Jaffré T, Reeves RD, Becquer T (eds) The ecology of ultramafic and metalliferous areas, Centre ORSTOM de Noumea, New Caledonia, pp. 261–266

  • Baker AJM, Proctor J, van Balgooy MMJ, Reeves RD (1992) Hyperaccumulation of nickel by the flora of the ultramafics of Palawan, Republic of the Philippines. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic (Serpentine) soils, intercept, GB-Andover, pp 291–304

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

    CAS  PubMed  Google Scholar 

  • Batianoff GN, Reeves RD, Specht RL (1990) Stackhousia tryonii Bailey: a nickel-accumulating serpentine-endemic species of Central Queensland. Aust J Bot 38:121–130

    CAS  Google Scholar 

  • Becerra-Castro C, Monterroso C, García-Lestón M, Prieto-Fernández A, Acea MJ, Kidd PS (2009) Rhizosphere microbial densities and trace metal tolerance of the Nickel hyperaccumulator Alyssum serpyllifolium subsp. lusitanicum. Int J Phytorem 11:525–541

    CAS  Google Scholar 

  • Berglund ABN, Dahlgren S, Westerbergh A (2004) Evidence for parallel evolution and site-specific selection of serpentine tolerance in Cerastium alpinum during the colonization of Scandinavia. New Phytol 161:199–209

    CAS  Google Scholar 

  • Bernal MP, McGrath SP, Miller AJ, Baker AJM (1994) Comparison of the chemical changes in the rhizosphere of the Nickel hyperaccumulator Alyssum murale with the non-accumulator Raphanus sativus. Plant Soil 164:251–259

    CAS  Google Scholar 

  • Boyd RS, Davis MA, Wall MA, Balkwill K (2002) Nickel defends the South African hyperaccumulator Senecio coronatus (Asteraceae) against Helix aspersa (Mollusca: Pulmonidae). Chemoecology 12:91–97

    CAS  Google Scholar 

  • Boyd RS (2007) The defense hypothesis of elemental hyperaccumulation: status, challenges and new directions. Plant Soil 293:153–176

    CAS  Google Scholar 

  • Brady KU, Kruckeberg AR, Bradshaw HD (2005) Evolutionary ecology of plant adaptation to serpentine soils. Ann Rev Ecol Evol Syst 36:243–266

    Google Scholar 

  • Brooks RR (1987) Serpentine and its vegetation. A multidisciplinary approach. Dioscorides Press, 9999 S.W. Wilshire, Portland, OR 97225, pp. 454

  • Chaintreuil C, Rigault F, Moulin L, Jaffre T, Fardoux J, Giraud E, Dreyfus B, Bailly X (2007) Nickel resistance determinants in Bradyrhizobium strains from nodules of the endemic New Caledonia legume Serianthes calycina. Appl Environ Microbiol 73:8018–8022

    CAS  PubMed  Google Scholar 

  • Chaney RL, Angle JS, McLntosh MS, Reeves RD, Li YM, Brewer EP, Chen KY, Roseberg RJ, Perner H, Synkowski EC, Broadhurst CL, Wang S, Baker AJM (2005) Using hyperaccumulator plants to phytoextract soil Ni and Cd. Zeitschrift Fur Naturforschung C-a Journal of Biosciences 60:190–198

    CAS  Google Scholar 

  • Chaney RL, Angle JS, Broadhurst CL, Peters CA, Tappero RV, Sparks DL (2007) Improved understanding of hyperaccumulation yields commercial phytoextraction and phytomining technologies. J Environ Qual 36:1429–1443

    CAS  PubMed  Google Scholar 

  • Chiarucci A, Robinson BH, Bonini I, Petit D, Brooks RR, De Dominicis V (1998) Vegetation of tuscan ultramafic soils in relation to edaphic and physical factors. Folia Geobot 33:113–131

    Google Scholar 

  • Doty SL (2008) Enhancing phytoremediation through the use of transgenics and endophytes. New Phytol 179:318–333

    CAS  PubMed  Google Scholar 

  • Droege M, Hill B (2008) The genome sequencer FLX system—longer reads, more applications, straight forward bioinformatics and more complete data sets. J Biotechnol 136:3–10

    CAS  PubMed  Google Scholar 

  • Freeman JL, Persans MW, Nieman K, Albrecht C, Peer W, Pickering IJ, Salt DE (2004) Increased glutathione biosynthesis plays a role in nickel tolerance in Thlaspi nickel hyperaccumulators. Plant Cell 16:2176–2191

    CAS  PubMed  Google Scholar 

  • Gevers D, Cohan FM, Lawrence JG, Spratt BG, Coenye T, Feil EJ, Stackebrandt E, Van de Peer Y, Vandamme P, Thompson FL, Swings J (2005) Opinion: re-evaluating prokaryotic species. Nat Rev Microbiol 3:733–739

    CAS  PubMed  Google Scholar 

  • Grass G, Fan B, Rosen BP, Lemke K, Schlegel HG, Rensing C (2001) NreB from Achromobacter xylosoxidans 31A is a nickel-induced transporter conferring nickel resistance. J Bacteriol 183:2803–2807

    CAS  PubMed  Google Scholar 

  • Gremion F, Chatzinotas A, Harms H (2003) Comparative 16S rDNA and 16S rRNA sequence analysis indicates that Actinobacteria might be a dominant part of the metabolically active bacteria in heavy metal-contaminated bulk and rhizosphere soil. Environ Microbiol 5:896–907

    CAS  PubMed  Google Scholar 

  • Hahm D-H, Yeon M-J, Ko W-M, Lee E-J, Lee H-J, Shim I-S, Kim H-Y (2002) Characterization of the Nickel resistance gene from Legionella pneumophila: attenuation of Nickel resistance by ppk (polyphosphate kinase) disruption in Escherichia coli. J Microbiol Biotechnol 12:114–120

    CAS  Google Scholar 

  • Haines BJ (2002) Zincophilic root foraging in Thlaspi caerulescens. New Phytologist 155:363–372

    Google Scholar 

  • Hardoim PR, van Overbeek LS, Elsas JDV (2008) Properties of bacterial endophytes and their proposed role in plant growth. Trends in Microbiol 16:463–471

    CAS  Google Scholar 

  • Hurek T, Reinhold-Hurek B (2003) Azoarcus sp. strain BH72 as a model for nitrogen-fixing grass endophytes. J Biotechnol 106:169–178

    CAS  PubMed  Google Scholar 

  • Idris R, Trifonova R, Puschenreiter M, Wenzel WW, Sessitsch A (2004) Bacterial communities associated with flowering plants of the Ni hyperaccumulator Thlaspi goesingense. Appl Environ Microbiol 70:2667–2677

    CAS  PubMed  Google Scholar 

  • Idris R, Kuffner M, Bodrossy L, Puschenreiter M, Monchy S, Wenzel WW, Sessitsch A (2006) Characterization of Ni-tolerant methylobacteria associated with the hyperaccumulating plant Thlaspi goesingense and description of Methylobacterium goesingense sp nov. Syst Appl Microbiol 29:634–644

    CAS  PubMed  Google Scholar 

  • Ingle RA, Fricker MD, Smith JAC (2008) Evidence for nickel/proton antiport activity at the tonoplast of the hyperaccumulator plant Alyssum lesbiacum. Plant Biol 10:746–753

    CAS  PubMed  Google Scholar 

  • Kaneko T, Sato S, Kotani H, Tanaka A, Asamizu E, Nakamura Y, Miyajima N, Hirosawa M, Sugiura M, Sasamoto S, Kimura T, Hosouchi T, Matsuno A, Muraki A, Nakazaki N, Naruo K, Okumura S, Shimpo S, Takeuchi C, Wada T, Watanabe A, Yamada M, Yasuda M, Tabata S (1996) Sequence analysis of the genome of the unicellular Cyanobacterium Synechocystis sp. strain PCC6803. II. sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res 3:109–136

    CAS  PubMed  Google Scholar 

  • Kazakou E, Dimitrakopoulos PG, Baker AJM, Reeves RD, Troumbis AY (2008) Hypotheses, mechanisms and trade-offs of tolerance and adaptation to serpentine soils: from species to ecosystem level. Biol Rev 83:495–508

    CAS  PubMed  Google Scholar 

  • Keijser BJ, Zaura E, Huse SM, van der Vossen JM, Schuren FH, Montijn RC, ten Cate JM, Crielaard W (2008) Pyrosequencing analysis of the oral microflora of healthy adults. J Dental Res 87:1016–1020

    CAS  Google Scholar 

  • Konstantinidis KT, Ramette A, Tiedje JM (2006) The bacterial species definition in the genomic era. Phil Trans Royal Soc B 361:1929–1940

    Google Scholar 

  • Kupper H, Lombi E, Zhao FJ, Wieshammer G, McGrath SP (2001) Cellular compartmentation of nickel in the hyperaccumulators Alyssum lesbiacum, Alyssum bertolonii and Thlaspi goesingense. J Exp Bot 52:2291–2300

    CAS  PubMed  Google Scholar 

  • Lebeau T, Braud A, Jézéquel K (2008) Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils: a review. Environ Pollut 153:497–522

    CAS  PubMed  Google Scholar 

  • Lee Y-K, Chang H-H, Lee H-J, Park H, Lee K-H, Joe M-H (2006) Isolation of a novel plasmid, pNi15, from Enterobacter sp. Ni15 containing a nickel resistance gene. FEMS Microbiol Lett 257:177–181

    CAS  PubMed  Google Scholar 

  • Lefèbvre C, Vernet P (1990) Microevolutionary processes on contaminated deposits. In: Shaw AJ (ed) Heavy metal tolerance in plants: evolutionary aspects. CRC Press Inc, Boca Raton, pp 286–297

    Google Scholar 

  • Li WC, Ye ZH, Wong MH (2007) Effects of bacteria an enhanced metal uptake of the Cd/Zn-hyperaccumulating plant, Sedum alfredii. J Exp Bot 58:4173–4182

    CAS  PubMed  Google Scholar 

  • Liesegang H, Lemke K, Siddiqui RA, Schlegel HG (1993) Characterization of the inducible nickel and cobalt resistance determinant cnr from pMOL28 of Alcaligenes eutrophus CH34. J Bacteriol 175:767–778

    CAS  PubMed  Google Scholar 

  • Lipman CB (1926) The bacterial flora of serpentine soils. J Bacteriol 12:315–318

    CAS  PubMed  Google Scholar 

  • Liu F, Tang Y, Du R, Yang H, Wu Q, Qiu R (2009) Root foraging for zinc and cadmium requirement in the Zn/Cd hyperaccumulator plant Sedum alfredii. Plant Soil. doi:10.1007/s11104-009-0060-8

    Google Scholar 

  • Lodewyckx C, Taghavi S, Mergeay M, Vangronsveld J, Clijsters H, van der Lelie D (2001) The effect of recombinant heavy metal-resistant endophytic bacteria on heavy metal uptake by their host plant. Int J Phytorem 3:173–187

    CAS  Google Scholar 

  • Lodewyckx C, Mergeay M, Vangronsveld J, Clijsters H, van der Lelie D (2002a) Isolation, characterization, and identification of bacteria associated with the zinc hyperaccumulator Thlaspi caerulescens subsp calaminaria. Int J Phytorem 4:101–115

    CAS  Google Scholar 

  • Lodewyckx C, Vangronsveld J, Porteous F, Moore ERB, Taghavi S, Mezgeay M, van der Lelie D (2002b) Endophytic bacteria and their potential applications. Crit Rev Plant Sci 21:583–606

    Google Scholar 

  • Marrero J, Auling G, Coto O, Nies DH (2007) High-level resistance to cobalt and nickel but probably no transenvelope efflux: metal resistance in the cuban Serratia marcescens strain C-1. Microb Ecol 53:123–133

    CAS  PubMed  Google Scholar 

  • Mastretta C, Taghavi S, van der Lelie D, Mengoni A, Galardi F, Gonnelli C, Barac T, Boulet J, Weyens N, Vangronsveld J (2009) Endophytic bacteria from seeds of Nicotiana tabacum can reduce cadmium phytotoxicity. Int J Phytorem 11:251–267

    CAS  Google Scholar 

  • McNear DH, Chaney RL, Sparks DL (2007) The effects of soil type and chemical treatment on nickel speciation in refinery enriched soils: a multi-technique investigation. Geochim Cosmochim Acta 71:2190–2208

    CAS  Google Scholar 

  • Mengoni A, Barzanti R, Gonnelli C, Gabbrielli R, Bazzicalupo M (2001) Characterization of nickel-resistant bacteria isolated from serpentine soil. Environ Microbiol 3:691–698

    CAS  PubMed  Google Scholar 

  • Mengoni A, Gonnelli C, Brocchini E, Galardi F, Pucci S, Gabbrielli R, Bazzicalupo M (2003a) Chloroplast genetic diversity and biogeography in the serpentine endemic Ni-hyperaccumulator Alyssum bertolonii. New Phytol 157:349–356

    Google Scholar 

  • Mengoni A, Gonnelli C, Hakvoort HWJ, Galardi F, Bazzicalupo M, Gabbrielli R, Schat H (2003b) Evolution of copper-tolerance and increased expression of a 2b-type metallothionein gene in Silene paradoxa L. populations. Plant Soil 257:451–457

    CAS  Google Scholar 

  • Mengoni A, Baker AMJ, Bazzicalupo M, Reeves RD, Adigüzel N, Chianni E, Galardi F, Gabbrielli R, Gonnelli C (2003c) Evolutionary dynamics of nickel hyperaccumulation in Alyssum revealed by ITS nrDNA analysis. New Phytol 159:691–699

    CAS  Google Scholar 

  • Mengoni A, Pini F, Shu W-S, Huang L-N, Bazzicalupo M (2009) Plant-by-plant variations of leaf-associated bacterial communities in the nickel-hyperaccumulator Alyssum bertolonii Desv. Microb Ecol 58:660–667

    CAS  PubMed  Google Scholar 

  • Mergeay M, Houba C, Gerits J (1978) Extrachromosomal inheritance controlling resistance to cadmium, cobalt, and zinc ions: evidence from curing in a Pseudomonas. Arch Int Physiol Biochim 86:440–441

    CAS  PubMed  Google Scholar 

  • Mergeay M, Monchy S, Vallaeys T, Auquier V, Benotmane A, Bertin F, Taghavi S, Dunn J, van der Lelie D, Wattiez R (2003) Ralstonia metallidurans, a bacterium specifically adapted to toxic metals: towards a catalogue of metal-responsive genes. FEMS Microbiol Rev 27:385–410

    CAS  PubMed  Google Scholar 

  • Mergeay M, Monchy S, Janssen P, Houdt R, Leys N (2009) Megaplasmids in Cupriavidus genus and metal resistance. In: Schwartz E (ed) Microbial megaplasmids. Springer Berlin, Heidelberg, pp 209–238

    Google Scholar 

  • Mirete S, de Figueras CG, Gonzalez-Pastor JE (2007) Novel nickel resistance genes from the rhizosphere metagenome of plants adapted to acid mine drainage. Appl Environ Microbiol 73:6001–6011

    CAS  PubMed  Google Scholar 

  • Mongodin EF, Shapir N, Daugherty SC, DeBoy RT, Emerson JB, Shvartzbeyn A, Radune D, Vamathevan J, Riggs F, Grinberg V, Khouri H, Wackett LP, Nelson KE, Sadowsky MJ (2006) Secrets of Soil Survival Revealed by the Genome Sequence of Arthrobacter aurescens TC1. PLOS Genetics 2:e214

    PubMed  Google Scholar 

  • Moore FP, Barac T, Borrernans B, Oeyen L, Vangronsveld J, van der Lelie D, Campbell CD, Moore ERB (2006) Endophytic bacterial diversity in poplar trees growing on a BTEX-contaminated site: the characterisation of isolates with potential to enhance phytoremediation. Syst Appl Microbiol 29:539–556

    CAS  PubMed  Google Scholar 

  • Newman LA, Reynolds CM (2005) Bacteria and phytoremediation: new uses for endophytic bacteria in plants. Trends Biotechnol 23:6–8

    CAS  PubMed  Google Scholar 

  • Nies DH (2000) Heavy metal-resistant bacteria as extremophiles: molecular physiology and biotechnological use of Ralstonia sp CH34. Extremophiles 4:77–82

    CAS  PubMed  Google Scholar 

  • Oline DK (2006) Phylogenetic comparisons of bacterial communities from serpentine and nonserpentine soils. Appl Environ Microbiol 72:6965–6971

    CAS  PubMed  Google Scholar 

  • Pace NR (2009) Problems with “Procaryote”. J Bacteriol 191: 2008–2010

    CAS  PubMed  Google Scholar 

  • Pal A, Wauters G, Paul AK (2007) Nickel tolerance and accumulation by bacteria from rhizosphere of nickel hyperaccumulators in serpentine soil ecosystem of Andaman, India. Plant Soil 293:37–48

    CAS  Google Scholar 

  • Park JE, Schlegel HG, Rhie HG, Lee HS (2004) Nucleotide sequence and expression of the ncr nickel and cobalt resistance in Hafnia alvei 5-5. Int Microbiol 7:27–34

    CAS  PubMed  Google Scholar 

  • Park JS, Lee SJ, Rhie HG, Lee HS (2008) Characterization of a chromosomal nickel resistance determinant from Klebsiella oxytoca CCUG 15788. J Microbiol Biotechnol 18:1040–1043

    CAS  PubMed  Google Scholar 

  • Perrier N, Colin F, Jaffré T, Ambrosi J-P, Rose J, Bottero J-Y (2004) Nickel speciation in Sebertia acuminata, a plant growing on a lateritic soil of New Caledonia. C R Geosciences 336:567–577

    CAS  Google Scholar 

  • Puschenreiter M, Schnepf A, Millan IM, Fitz WJ, Horak O, Klepp J, Schrefl T, Lombi E, Wenzel WW (2005) Changes of Ni biogeochemistry in the rhizosphere of the hyperaccumulator Thlaspi goesingense. Plant Soil 271:205–218

    CAS  Google Scholar 

  • Quince C, Curtis TP, Sloan WT (2008) The rational exploration of microbial diversity. ISME J 2:997–1006

    CAS  PubMed  Google Scholar 

  • Rajakaruna N, Baldwin BG, Chan R, Desrochers AM, Bohm BA, Whitton J (2003) Edaphic races and phylogenetic taxa in the Lasthenia californica complex (Asteraceae: Heliantheae): an hypothesis of parallel evolution. Mol Ecol 12:1675–1679

    PubMed  Google Scholar 

  • Rajkumar M, Freitas H (2008a) Effects of inoculation of plant-growth promoting bacteria on Ni uptake by Indian mustard. Biores Technol 99:3491–3498

    CAS  Google Scholar 

  • Rajkumar M, Freitas H (2008b) Influence of metal resistant-plant growth-promoting bacteria on the growth of Ricinus communis in soil contaminated with heavy metals. Chemosphere 71:834–842

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Rajkumar M, Ae N, Freitas H (2009b) Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere 77:153–160

    CAS  Google Scholar 

  • Reddy PM, Ladha JK, So RB, Hernandez RJ, Ramos MC, Angeles OR, Dazzo FB, de Bruijn FJ (1997) Rhizobial communication with rice roots: induction of phenotypic changes, mode of invasion and extent of colonization. Plant Soil 194:81–98

    CAS  Google Scholar 

  • Reeves RD, Baker AJM, Borhidi A, Berazaìn R (1999) Nickel hyperaccumulation in the serpentine flora of Cuba. Ann Bot 83:29–38

    CAS  Google Scholar 

  • Rosenblueth M, Martinez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant-Microbe Int 19:827–837

    CAS  Google Scholar 

  • Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278:1–9

    CAS  PubMed  Google Scholar 

  • Sagner S, Kneer R, Wanner G, Cosson JP, Deus-Neumann B, Zenk MH (1998) Hyperaccumulation, complexation and distribution of nickel in Sebertia acuminata. Phytochemistry 47:339–347

    CAS  PubMed  Google Scholar 

  • Saintpierre D, Amir H, Pineau R, Sembiring L, Goodfellow M (2003) Streptomyces yatensis sp nov., a novel bioactive streptomycete isolated from a New-Caledonian ultramafic soil. Anton Leeuw Int J G 83:21–26

    CAS  Google Scholar 

  • Sauge-Merle S, Cuiné S, Carrier P, Lecomte-Pradines C, Luu D-T, Peltier G (2003) Enhanced toxic metal accumulation in engineered bacterial cells expressing Arabidopsis thaliana phytochelatin synthase. Appl Environ Microbiol 69:490–494

    CAS  PubMed  Google Scholar 

  • Schlegel HG, Cosson JP, Baker AJM (1991) Nickel-hyperraccumulating plants provide a niche for nickel-resistant bacteria. Bot Acta 104:18–25

    CAS  Google Scholar 

  • Schmidt T, Schlegel HG (1989) Nickel and cobalt resistance of various bacteria isolated from soil and highly polluted domestic and industrial wastes. FEMS Microbiol Lett 62:315–328

    CAS  Google Scholar 

  • Schmidt T, Schlegel HG (1994) Combined nickel-cobalt-cadmium resistance encoded by the ncc locus of Alcaligenes xylosoxidans 31A. J Bacteriol 176:7045–7054

    CAS  PubMed  Google Scholar 

  • Schwartz C, Morel JL, Saumier S, Whiting SN, Baker AJM (1999) Root development of the Zinc-hyperaccumulator plant Thlaspi caerulescens as affected by metal origin, content and localization in soil. Plant Soil 208:103–115

    CAS  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Selosse MA, Baudoin E, Vandenkoornhuyse P (2004) Symbiotic microorganisms, a key for ecological success and protection of plants. Comptes Rendus Biol 327:639–648

    Google Scholar 

  • Sessitsch A, Puschenreiter M (2008) Endophytes and rhizosphere bacteria of plants growing in heavy metal-containing soils. In: Dion P, Nautiyal CS (eds) Microbiology of extreme soils. Soil biology 1. Springer-Verlag, Berlin Heidelberg

    Google Scholar 

  • Shallari S, Echevarria G, Schwartz C, Morel JL (2001) Availability of nickel in soils for the hyperaccumulator Alyssum murale Waldst. & Kit. S Afr J Sci 97:568–570

    CAS  Google Scholar 

  • Smart KE, Kilburn MR, Salter CJ, Smith JAC, Grovenor CRM (2007) NanoSIMS and EPMA analysis of nickel localisation in leaves of the hyperaccumulator plant Alyssum lesbiacum. Int J Mass Spectrom 260:107–114

    CAS  Google Scholar 

  • Staley JT (2006) The bacterial species dilemma and the genomic-phylogenetic species concept. Phil Trans Royal Soc B 361:1899–1909

    Google Scholar 

  • Stoppel R, Schlegel HG (1995) Nickel-resistant bacteria from anthropogenically Nickel-polluted and naturally Nickel-percolated ecosystems. Appl Environ Microbiol 61:2276–2285

    CAS  PubMed  Google Scholar 

  • Stoppel RD, Meyer M, Schlegel HG (1995) The nickel resistance determinant cloned from the enterobacterium Klebsiella oxytoca: conjugational transfer, expression, regulation and DNA homologies to various nickel-resistant bacteria. Biometals 8:70–79

    CAS  PubMed  Google Scholar 

  • Tian J, Wu N, Li J, Liu Y, Guo J, Yao B, Fan Y (2007) Nickel-resistant determinant from Leptospirillum ferriphilum. Appl Environ Microbiol 73:2364–2368

    CAS  PubMed  Google Scholar 

  • Valls M, de Lorenzo V (2002) Exploiting the genetic and biochemical capacities of bacteria for the remediation of heavy metal pollution. FEMS Microbiol Rev 26:327–338

    CAS  PubMed  Google Scholar 

  • Vekemans X, Lefèbvre C (1997) On the evolution of heavy-metal tolerant populations in Armeria maritima: evidence from allozyme variation and reproductive barriers. J Evol Biol 10:175–191

    Google Scholar 

  • von Rozycki T, Nies DH (2008) Cupriavidus metallidurans: evolution of a metal-resistant bacterium. Anton Leeuw Int J G 96:115–139

    Google Scholar 

  • Weyens N, van der Lelie D, Taghavi S, Vangronsveld J (2009a) Phytoremediation: plant-endophyte partnerships take the challenge. Curr Op Biotechnol 20:248–254

    CAS  Google Scholar 

  • Weyens N, van der Lelie D, Taghavi S, Newman L, Vangronsveld J (2009b) Exploiting plant-microbe partnerships for improving biomass production and remediation. Trends Biotechnol. doi:10.1016/j.tibtech.2009.07.006

    Google Scholar 

  • Whiting SN, Leake JR, McGrath SP, Baker AJM (2000) Positive responses to Zn and Cd by roots of the Zn and Cd hyperaccumulator Thlaspi caerulescens. New Phytol 145:199–210

    CAS  Google Scholar 

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Acknowledgments

We are grateful to two anonymous referees for critical reading and improvement of the manuscript.

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Authors and Affiliations

  1. Department of Evolutionary Biology, University of Firenze, I-50125, Firenze, Italy

    Alessio Mengoni

  2. Institute of Molecular and Cellular Biology, Faculty of Earth and Life Sciences, Vrije Universiteit Amsterdam, De Boelelaan 1085, 1081 HV, Amsterdam, The Netherlands

    Henk Schat

  3. Centre for Environmental Sciences, Environmental Biology, Hasselt University, Agoralaan, building D, B-3590, Diepenbeek, Belgium

    Jaco Vangronsveld

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  1. Alessio Mengoni
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Correspondence to Alessio Mengoni.

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Mengoni, A., Schat, H. & Vangronsveld, J. Plants as extreme environments? Ni-resistant bacteria and Ni-hyperaccumulators of serpentine flora. Plant Soil 331, 5–16 (2010). https://doi.org/10.1007/s11104-009-0242-4

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  • DOI: https://doi.org/10.1007/s11104-009-0242-4

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