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The Bacterial Flora of the Nickel-Hyperaccumulator Plant Alyssum bertolonii

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Biomanagement of Metal-Contaminated Soils

Part of the book series: Environmental Pollution ((EPOL,volume 20))

Abstract

Recent years have witnessed a considerable growth of microbiological researches in serpentine soils in relation to the presence of hyperaccumulating plants. Nickel-hyperaccumulating plants accumulate huge amounts of heavy metals in shoots, and therefore, provide a specific environment for bacterial populations and in particular for endophytic bacteria. Bacterial endophytes have been studied in many different plant species and in some cases they have been found to promote plant growth or to confer the plant higher tolerance to biotic and abiotic stress. Here, we report the data on presence, composition and possible roles of bacteria associated with Alyssum bertolonii Desv. (Brassicaceae), the first nickel-hyperaccumulator plant discovered endemic to serpentine outcrops of Central Italy. The analysis of both cultivable and total fraction of the soil bacterial community showed a very strong effect of the plant in shaping the community composition. Moreover, the plant harbors a complex and highly variable endophytic bacterial flora with many Ni-resistant strains. Endophytic bacteria were isolated from roots, stems, and leaves of several A. bertolonii plants and populations allowing providing a model of correlation between taxonomic compositions of bacterial communities from different organs, plants, populations, and surrounding soils. Some of the endophytic bacteria tested for plant tissue colonization ability, and for their influence on plant growth and nickel-hyperaccumulation, resulted in increased biomass production and metal accumulation. Ecological and evolutionary implications of such findings are also discussed.

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References

  • 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. Intern J Phytoremed 9:41–52

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Abou-Shanab RA, van Berkum P, Angle JS (2007) 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

    Article  CAS  Google Scholar 

  • Arrigoni PV, Ricceri C, Mazzanti A (1983) La vegetazione serpentinicola del Monte Ferrato di Prato in Toscana. Centro Scienze Naturali Prato, Pistoia

    Google Scholar 

  • Assunção AGL, Bookum WM, Nelissen HJM, Vooijs R, Schat H, Ernst WHO (2003) Differential metal-specific tolerance and accumulation patterns among Thlaspi caerulescens populations originating from different soil types. New Phytologist 159:411–419

    Article  Google Scholar 

  • Assunção AGL, Pieper B, Vromans J, Lindhout P, Aarts MGM, Schat H (2006) Construction of a genetic linkage map of Thlaspi caerulescens and quantitative trait loci analysis of zinc accumulation. New Phytologist 170:21–32

    Article  Google Scholar 

  • Assunção AGL, Bleeker P, Ten Bookum WM, Vooijs R, Schat H (2008) Intraspecific variation of metal preference patterns for hyperaccumulation in Thlaspi caerulescens: evidence from binary metal exposures. Plant Soil 303:289–299

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Barac T, Taghavi S, Borremans B, Provoost A, Oeyen L, Colpaert JV, Vangronsveld J, van der Lelie D (2004) Engineered endophytic bacteria improve phytoremediation of water-soluble, volatile, organic pollutants. Nature Biotechnol 22:583–588

    Article  CAS  Google Scholar 

  • 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. Microbial Ecol 53:306–316

    Article  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. Intern J Phytoremed 11:525–541

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Brooks RR (1983) Biological methods of prospecting for minerals. Wiley, New York

    Google Scholar 

  • Brooks RR (1987) Serpentine and its vegetation. A multidisciplinary approach. Dioscorides Press, Portland

    Google Scholar 

  • Brooks RR, Radford CC (1978) Nickel accumulation by European species of the genus Alyssum. Proc R Soc Lond B 200:217–224

    Article  CAS  Google Scholar 

  • Brooks RR, Morrison RS, Reeves RD, Dudley TR, Akman Y (1979) Hyperaccumulation of nickel by Alyssum Linnaeus (Cruciferae). Proc R Soc Lond B 203:387–403

    Article  CAS  Google Scholar 

  • Chaney RL, Angle JS, Baker AJM, Li Y-M (1998) Method for phytomining of nickel, cobalt and other metals from soils. US Patent, No. 5: 711,784

    Google Scholar 

  • Costacurta A, Vanderleyden J (1995) Synthesis of phytohormones by plant-associated bacteria. Crit Rev Microbiol 21:1–18

    Article  Google Scholar 

  • Danhorn T, Fuqua C (2007) Biofilm formation by plant-associated bacteria. Ann Rev Microbiol 61:401–422

    Article  CAS  Google Scholar 

  • Galardi F, Corrales I, Mengoni A, Pucci S, Barletti L, Arnetoli M, Gabbrielli R, Gonnelli C (2007a) Intra-specific differences in nickel tolerance and accumulation in the Ni-hyperaccumulator Alyssum bertolonii. Environ Exp Bot 60:377–384

    Article  CAS  Google Scholar 

  • Galardi F, Mengoni A, Pucci S, Barletti L, Massi L, Barzanti R, Gabbrielli R, Gonnelli C (2007b) Intra-specific differences in mineral element composition in the Ni-hyperaccumulator Alyssum bertolonii: a survey of populations in nature. Environ Exp Bot 60:50–56

    Article  CAS  Google Scholar 

  • Glick BR (2005) Modulation of plant ethylene levels by the bacterial enzyme ACC deaminase. FEMS Microbiol Lett 251:1–7

    Article  CAS  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

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Jackson RW (2009) Plant pathogenic bacteria: genomics and molecular biology. Caister Academic Press, Norwich

    Google Scholar 

  • Janssen PJ, Van Houdt R, Moors H, Monsieurs P, Morin N, Michaux A, Benotmane MA, Leys N, Vallaeys T, Lapidus A, Monchy S, Médigue C, Taghavi S, McCorkle S, Dunn J, van der Lelie D, Mergeay M (2009) The complete genome sequence of Cupriavidus metallidurans strain CH34, a master survivalist in harsh and anthropogenic environments. PLoS One 5(5):e10433

    Article  Google Scholar 

  • Kruckeberg AR (1954) The ecology of serpentine soils. III. Plant species in relation to serpentine soils. Ecology 35:267–274

    Google Scholar 

  • Kruckeberg AR, Kruckeberg AL (1990) Endemic metallophytes: their taxonomic, genetic and evolutionary attributes. In: Shaw AJ (ed.) Heavy metal tolerance in plants: evolutionary aspects. CRC Press Inc, Boca Raton, pp 301–312

    Google Scholar 

  • Lidstrom ME, Chistoserdova L (2002) Plants in the pink: cytokinin production by Methylobacterium. J Bacteriol 184:1818

    Article  CAS  Google Scholar 

  • Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Lucy M, Reed E, Glick BR (2004) Applications of free living plant growth-promoting rhizobacteria. Antonie Van Leeuwenhoek 86:1–25

    Article  CAS  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. Microbial Ecol 53:123–133

    Article  CAS  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. Intern J Phytoremed 11:251–267

    Article  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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Mengoni A, Grassi E, Barzanti R, Biondi EG, Gonnelli C, Kim CK, Bazzicalupo M (2004) Genetic diversity of bacterial communities of serpentine soil and of rhizosphere of the nickel-hyperaccumulator plant Alyssum bertolonii. Microbial Ecol 48:209–217

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Mengoni A, Schat H, Vangronsveld J (2010) Plants as extreme environments? Ni-resistant bacteria and Ni-hyperaccumulators of serpentine flora. Plant Soil 331:5–16

    Article  CAS  Google Scholar 

  • Minguzzi C, Vergnano Gambi O (1948) Il contenuto di nichel nelle ceneri di Alyssum bertolonii Desv. Memorie Società Toscana di Scienze Naturali 55:49–74

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Pichi Sermolli R (1948) Flora e vegetazione delle serpentine e delle altre ofioliti dell’alta valle del Tevere (Toscana). Webbia 17:1–380

    Google Scholar 

  • Pignatti S (1997) Flora d’Italia, vol 1. Agricole, Bologne

    Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  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

    Article  CAS  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. Antonie Van Leeuwenhoek 83:21–26

    Article  CAS  Google Scholar 

  • Salt DE, Smith RD, Raskin I (1998) Phytoremediation. Ann Rev Plant Physiol Plant Mol Biol 49:643–668

    Article  CAS  Google Scholar 

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

    CAS  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, vol 1, Soil biology. Springer, Berlin/Heidelberg, pp 317–332

    Chapter  Google Scholar 

  • Singh BK, Millard P, Whiteley AS, Murrell JC (2004) Unravelling rhizosphere-microbial interactions: opportunities and limitations. Trends Microbiol 12:386–393

    Article  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

    Google Scholar 

  • Somers E, Vanderleyden J, Srinivasan M (2004) Rhizosphere bacterial signalling: a love parade beneath our feet. Crit Rev Microbiol 30:205–240

    Article  CAS  Google Scholar 

  • Taghavi S, van der Lelie D, Hoffman A, Zhang YB, Walla MD, Vangronsveld J, Newman L, Monchy S (2010) Genome sequence of the plant growth promoting endophytic bacterium Enterobacter sp. 638. PLoS Genet 6(5):e1000943

    Article  Google Scholar 

  • Turner TL, Bourne EC, Von Wettberg EJ, Hu TT, Nuzhdin SV (2010) Population re-sequencing reveals local adaptation of Arabidopsis lyrata to serpentine soils. Nat Genet 42:260–263

    Article  CAS  Google Scholar 

  • Van Rhijn P, Vanderleyden J (1995) The Rhizobium-plant symbiosis. Microbiol Rev 59:124–142

    Google Scholar 

  • Vergnano Gambi O (1992) The distribution and ecology of the vegetation of ultramafic soils in Italy. In: Roberts BA, Proctor J (eds.) The ecology of areas with serpentinized rocks – a world view. Kluwer, Dordrecht, pp 217–247

    Chapter  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Whipps JM, Hand P, Pink D, Bending GD (2008) Phyllosphere microbiology with special reference to diversity and plant genotype. J Appl Microbiol 105:1744–1755

    Article  CAS  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 Phytologist 145:199–210

    Article  CAS  Google Scholar 

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Acknowledgments

This work was partially supported by grants of University of Florence to AM and MB (Contributo di Ateneo anno 2009). FP performed part of his Ph.D. work on A. bertolonii endophytes sponsored by a fellowship of the Italian Ministry of Research and Education (MIUR).

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Authors and Affiliations

  1. Department of Evolutionary Biology, University of Firenze, via Romana 17, I-50125, Florence, Italy

    Alessio Mengoni, Francesco Pini & Marco Bazzicalupo

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  1. Alessio Mengoni
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  2. Francesco Pini
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  3. Marco Bazzicalupo
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Correspondence to Alessio Mengoni .

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Editors and Affiliations

  1. Fac. Agricultural Sciences, Dept. Agricultural Microbiology, Aligarh Muslim University, Aligarh, 202002, India

    Mohammad Saghir Khan

  2. Fac. Agricultural Sciences, Dept. Agricultural Microbiology, Aligarh Muslim University, Aligarh, 202002, India

    Almas Zaidi

  3. , Department of Microbiology, Govind Ballabh Pant University of Agricu, Pantnagar, 263145, India

    Reeta Goel

  4. , Department of Zoology, King Saud University, Riyadh, 11451, Saudi Arabia

    Javed Musarrat

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Mengoni, A., Pini, F., Bazzicalupo, M. (2011). The Bacterial Flora of the Nickel-Hyperaccumulator Plant Alyssum bertolonii . In: Khan, M., Zaidi, A., Goel, R., Musarrat, J. (eds) Biomanagement of Metal-Contaminated Soils. Environmental Pollution, vol 20. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-1914-9_7

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