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

Plant and Soil

Volumn 331, Issue 1, 2010, Pages 5-16

  Mengoni, Alessio ^a   Schat, Henk ^b   Vangronsveld, Jaco ^c  

^a UNIVERSITY OF FLORENCE   (Italy)

^b VU UNIVERSITY AMSTERDAM   (Netherlands)

^c HASSELT UNIVERSITY   (Belgium)

Author keywords

Bacterial communities; Heavy metals; Hyperaccumulators; Nickel resistance; Serpentine soil

Indexed keywords

ADAPTIVE RADIATION; BIOTECHNOLOGY; EXPLOITATION; HYPERACCUMULATION; MICROBIAL COMMUNITY; NICKEL; PHYTOREMEDIATION; SERPENTINE; SOIL POLLUTION; SPECIES DIVERSITY;

BACTERIA (MICROORGANISMS);

EID: 77952424792     PISSN: 0032079X     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11104-009-0242-4     Document Type: Review

References (106)

1. 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.
2. 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.
3. 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.
4. 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.
5. 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.
6. 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.
7. 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.
8. 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.
9. 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.
10. 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.
11. 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.
12. 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.
13. 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.
14. 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.
15. 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.
16. 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.
17. Boyd RS (2007) The defense hypothesis of elemental hyperaccumulation: status, challenges and new directions. Plant Soil 293: 153-176.
18. Brady KU, Kruckeberg AR, Bradshaw HD (2005) Evolutionary ecology of plant adaptation to serpentine soils. Ann Rev Ecol Evol Syst 36: 243-266.
19. Brooks RR (1987) Serpentine and its vegetation. A multidisciplinary approach. Dioscorides Press, 9999 S. W. Wilshire, Portland, OR 97225, pp. 454.
20. 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.
21. 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.
22. 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.
23. 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.
24. Doty SL (2008) Enhancing phytoremediation through the use of transgenics and endophytes. New Phytol 179: 318-333.
25. 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.
26. 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.
27. 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.
28. 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.
29. 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.
30. 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.
31. Haines BJ (2002) Zincophilic root foraging in Thlaspi caerulescens. New Phytologist 155: 363-372.
32. 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.
33. Hurek T, Reinhold-Hurek B (2003) Azoarcus sp. strain BH72 as a model for nitrogen-fixing grass endophytes. J Biotechnol 106: 169-178.
34. 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.
35. 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.
36. 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.
37. 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.
38. 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.
39. 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.
40. Konstantinidis KT, Ramette A, Tiedje JM (2006) The bacterial species definition in the genomic era. Phil Trans Royal Soc B 361: 1929-1940.
41. 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.
42. Lebeau T, Braud A, Jézéquel K (2008) Performance of bioaugmentation-assisted phytoextraction applied to metal contaminated soils: a review. Environ Pollut 153: 497-522.
43. 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.
44. 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.
45. 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.
46. 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.
47. Lipman CB (1926) The bacterial flora of serpentine soils. J Bacteriol 12: 315-318.
48. 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.
49. 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.
50. 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.
51. 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.
52. 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.
53. 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.
54. 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.
55. 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.
56. 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.
57. 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.
58. 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.
59. 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.
60. 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.
61. 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.
62. 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.
63. 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.
64. 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.
65. 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.
66. Newman LA, Reynolds CM (2005) Bacteria and phytoremediation: new uses for endophytic bacteria in plants. Trends Biotechnol 23: 6-8.
67. Nies DH (2000) Heavy metal-resistant bacteria as extremophiles: molecular physiology and biotechnological use of Ralstonia sp CH34. Extremophiles 4: 77-82.
68. Oline DK (2006) Phylogenetic comparisons of bacterial communities from serpentine and nonserpentine soils. Appl Environ Microbiol 72: 6965-6971.
69. Pace NR (2009) Problems with "Procaryote". J Bacteriol 191: 2008-2010.
70. 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.
71. 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.
72. 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.
73. 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.
74. 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.
75. Quince C, Curtis TP, Sloan WT (2008) The rational exploration of microbial diversity. ISME J 2: 997-1006.
76. 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.
77. Rajkumar M, Freitas H (2008a) Effects of inoculation of plant-growth promoting bacteria on Ni uptake by Indian mustard. Biores Technol 99: 3491-3498.
78. 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.
79. 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.
80. Rajkumar M, Ae N, Freitas H (2009b) Endophytic bacteria and their potential to enhance heavy metal phytoextraction. Chemosphere 77: 153-160.
81. 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.
82. Reeves RD, Baker AJM, Borhidi A, Berazaìn R (1999) Nickel hyperaccumulation in the serpentine flora of Cuba. Ann Bot 83: 29-38.
83. Rosenblueth M, Martinez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant-Microbe Int 19: 827-837.
84. Ryan RP, Germaine K, Franks A, Ryan DJ, Dowling DN (2008) Bacterial endophytes: recent developments and applications. FEMS Microbiol Lett 278: 1-9.
85. 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.
86. 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.
87. 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.
88. Schlegel HG, Cosson JP, Baker AJM (1991) Nickel-hyperraccumulating plants provide a niche for nickel-resistant bacteria. Bot Acta 104: 18-25.
89. 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.
90. Schmidt T, Schlegel HG (1994) Combined nickel-cobalt-cadmium resistance encoded by the ncc locus of Alcaligenes xylosoxidans 31A. J Bacteriol 176: 7045-7054.
91. 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.
92. 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.
93. Selosse MA, Baudoin E, Vandenkoornhuyse P (2004) Symbiotic microorganisms, a key for ecological success and protection of plants. Comptes Rendus Biol 327: 639-648.
94. 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.
95. 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.
96. 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.
97. Staley JT (2006) The bacterial species dilemma and the genomic-phylogenetic species concept. Phil Trans Royal Soc B 361: 1899-1909.
98. Stoppel R, Schlegel HG (1995) Nickel-resistant bacteria from anthropogenically Nickel-polluted and naturally Nickel-percolated ecosystems. Appl Environ Microbiol 61: 2276-2285.
99. 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.
100. 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.
101. 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.
102. 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.
103. von Rozycki T, Nies DH (2008) Cupriavidus metallidurans: evolution of a metal-resistant bacterium. Anton Leeuw Int J G 96: 115-139.
104. Weyens N, van der Lelie D, Taghavi S, Vangronsveld J (2009a) Phytoremediation: plant-endophyte partnerships take the challenge. Curr Op Biotechnol 20: 248-254.
105. 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.
106. 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.