Skip to main content
Log in

Symbiotic interactions of culturable microbes with the nickel hyperaccumulator Berkheya coddii and the herbivorous insect Chrysolina clathrata

  • Published:
Symbiosis Aims and scope Submit manuscript

Abstract

Chrysolina clathrata is a specialized phytophagous beetle feeding exclusively on the herbaceous nickel hyperaccumulating plant Berkheya coddii. These organisms appear impervious to the toxic levels of nickel in their environment. In the current study we aimed to identify microorganisms that may have symbiotic relationships with these organisms. Culture techniques were used to isolate bacteria and fungi from plants and the faeces of beetles reared under laboratory conditions. The identity of isolates was determined using morphology and molecular techniques. Several genera of filamentous fungi (Alternaria, Aspergillus, Bipolaris, Cladosporium, Epicoccum, Fusarium, and Penicillium), yeasts (Cryptococcus, Meyerozyma, and Rhodotorula), as well as endophytic bacteria (Bacillus and Lysinibacillus) were isolated from the leaves of the plant. We also selectively isolated yeasts (Candida, Cryptococcus, Debaryomyces, Meyerozyma and Wickerhamomyces) from the beetle’s faeces. Subsequently we determined the minimum inhibitory Ni-concentration (MIC) of all isolates. The endophytic bacteria, filamentous fungi and the yeasts Candida intermedia, Cryptococcus flavescens and Meyerozyma guilliermondii, showed notable Ni resistance, while the beetle’s gut seems to select for Ni resistant yeasts.

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
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Ahmad I, Zafar S, Ahmad F (2005) Heavy metal biosorption potential of Aspergillus and Rhizopus sp. isolated from wastewater treated soil. JASEM 9(1):123–126

    Google Scholar 

  • Augustyniak M, Mesjasz-Przybyłowicz J, Nakonieczny M, Dybowska M, Przybyłowicz W, Migula P (2002) Food relations between Chrysolina pardalina and Berkheya coddii– a nickel hyperaccumulator from South-African ultramafic outcrops. Fresenius Environ Bull 11:85–90

    Google Scholar 

  • Augustyniak M, Migula P, Mesjasz-Przybyłowicz J, Tarnawska M, Nakonieczny M, Babczyńska A, Przybyłowicz WJ, Augustyniak MG (2007) Short-term effects of dimethoate on metabolic responses in Chrysolina pardalina (Chrysomelidae) feeding on Berkheya coddii (Asteraceae), a hyperaccumulator of nickel. Environ Pollut 150:218–224

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bhatti FJ, Bhutta AR (2002) Seed-borne pathogens associated with certified seed lots of wheat in Pakistan. Q Sci Vis 8(1):112–115

    Google Scholar 

  • Boyd RS, Martens SN (1992) The raison d’etre for metal hyperaccumulation by plants. In: Baker AJM, Proctor J, Reeves RD (eds) The vegetation of ultramafic (serpentine) soils. Intercept Limited, Andover, Hampshire

    Google Scholar 

  • Boyd RS, Shaw JJ, Martens SN (1994) Nickel hyperaccumulation defends Streptanthus polygaloides (Brassicaceae) against pathogens. Am J Bot 81(3):294–300

    Article  CAS  Google Scholar 

  • Branco S, Ree RH (2010) Serpentine soils do not limit mycorrhizal fungal diversity. PLoS One 5(7):e11757. doi:10.1371/journal.pone.0011757

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Brooks RR, Chambers MF, Nicks LJ, Robinson BH (1998) Phytomining. Trends Plant Sci 3:359–362

    Article  Google Scholar 

  • Brooks RR, Robinson BH (1998) The potential use of hyperaccumulators and other plants for phytomining. In: Brooks RR (ed) Plants that hyperaccumulate heavy metals: Their role in phytoremediation, microbiology, archaeology, mineral exploration and phytomining. CABI Publishing, CAB International, New York, pp 327–356

    Google Scholar 

  • Brooks RR, Robinson BH, Howes AW, Chiarucci A (2001) An evaluation of Berkheya coddii Roessler and Alyssum bertolonii Desv. for phytoremediation and phytomining of nickel. S Afr J Sci 97:558–560

    CAS  Google Scholar 

  • Congeevaram S, Dhanarani S, Park J, Dexilin M, Thamaraiselvi K (2007) Biosorption of chromium and nickel by heavy metal resistant fungal and bacterial isolates. J Hazard Mater 146:270–277

    Article  PubMed  CAS  Google Scholar 

  • Esteve-Zarzoso B, Belloch C, Uruburu F, Querol A (1999) Identification of yeasts by RFLP analysis of the 5.8S rRNA gene and the two ribosomal internal transcribed spacers. Int J Syst Bacteriol 49:329–337

    Article  PubMed  CAS  Google Scholar 

  • Ezzouhri L, Castro E, Moya M, Espinola F, Lairini K (2009) Heavy metal tolerance of filamentous fungi isolated from polluted sites in Tangier. Morocco Afr J Microbiol 3(2):035–048

    CAS  Google Scholar 

  • Fávaro LCL, De Melo FL, Aguilar-Vildoso CI, Araújo WL (2011) Polyphasic analysis of intraspecific diversity in Epicoccum nigrum warrants reclassification into separate. PLoS One. doi:10.1371/journal.pone.0014828

  • Fonseca Á, Inácio J (2006) Phylloplane yeasts. In: Rosa CA, Péter G (eds) The yeast handbook; Biodiversity and ecophysiology of yeasts. Springer-Verlag Berlin, Heidelberg, pp 263–301

    Chapter  Google Scholar 

  • Ganter PF (2006) Yeasts and invertebrate associations. In: Rosa CA, Péter G (eds) The yeast handbook; Biodiversity and ecophysiology of yeasts. Springer-Verlag Berlin, Heidelberg, pp 303–370

    Chapter  Google Scholar 

  • Guillamón JM, Sabaté J, Cano EBJ, Querol A (1998) Rapid identification of wine yeast species based on RFLP analysis of the ribosomal internal transcribes spacer (ITS) region. Arch Microbiol 169:387–392

    Article  PubMed  Google Scholar 

  • Gullan PJ, Cranston PS (2010) The insects-An outline of Entomology, 4th edn. Wiley-Blackwell, Oxford

    Google Scholar 

  • Harris AT, Naidoo K, Nokes J, Walker T, Orton F (2009) Indicative assessment of the feasibility of Ni and Au phytomining in Australia. J Clean Prod 17:194–200

    Article  CAS  Google Scholar 

  • Harrison S, Rajakaruna N (eds) (2011) Serpentine: The evolution and ecology of a model system. University of California Press, London

    Google Scholar 

  • Hatta R, Ito K, Hosakie Y, Tanaka T, Tanaka A, Yamamoto M, Akimitsu K, Tsuge T (2002) A conditionally dispensible chromosome controls host-specific pathogenicity in the fungal plant pathogen Alternaria alternata. Genetics 161(1):59–70

    PubMed  CAS  Google Scholar 

  • Horn BW, Moore GG (2011) Sexual reproduction in aflatoxin-producing Aspergillus nomius. Mycologia 103(1):174–183

    Article  PubMed  Google Scholar 

  • Javier F, Heras-Vazquez L, Mingorance-Cazorla L, Clemente-Jimenez JF, Rodriquez-Vico F (2003) Identification of yeast species from orange fruit and juice by RFLP and sequence analysis of the 5.8S rRNA gene and the two internal transcribed spacers. FEMS Yeast Res 3:3–9

    Google Scholar 

  • Kentner E, Armitage BD, Zeitlin H (1969) A rapid dimethylglyoxime method for the determination of nickel(II) in sea water. Anal Chim Acta 45:343–346

    Article  CAS  Google Scholar 

  • Kidd BN, Kadoo NY, Dombrecht B, Tekeoğlu M, Gardiner DM, Thatcher LF, Aitken EAB, Schenk PM, Manners JM, Kazan K (2011) Auxin signalling and transport promote susceptibility to the root-infecting fungal pathogen Fusarium oxysporum in Arabidopsis. MPMI 24(6):733–748

    Article  PubMed  CAS  Google Scholar 

  • Lodewyckx C, Vangronsveld J, Porteous F, Moore ERB, Taghavi S, Mezgeay M, Van der Lelie D (2002) Endophytic bacteria and their potential application. Crit Rev Plant Sci 21(6):583–606

    Article  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 

  • Manamgoda D, Cai L, Bahkali AH, Chukeatirote E, Hyde KD (2011) Cochliobolus: an overview and current status of species. Fungal Diversity 51:3–42. doi:10.1007/s13225-011-0139-4

    Article  Google Scholar 

  • Mesjasz-Przybylowicz J, Przybylowicz WJ (1999) Phytophagous insects associated with the Ni-hyperaccumulating plant Berkheya coddii (Asteraceae) in Mpumalanga, South Africa. In: Abstracts of the Third International Conference on Serpentine Ecology, Kruger National Park, South Africa, 8

  • Mesjasz-Przybylowicz J, Przybylowicz WJ (2001) Phytophagous insects associated with the Ni-hyperaccumulating plant Berkheya coddii (Asteraceae) in Mpumalanga, South Africa. S Afr J Sci 97:596–598

    CAS  Google Scholar 

  • Mesjasz-Przybylowicz J, Przybylowicz WJ, Pineda CA (2001) Nuclear microprobe studies of elemental distribution in apical leaves of the Ni hyperaccumulator Berkheya coddii. S Afr J Sci 97:591–593

    CAS  Google Scholar 

  • Mesjasz-Przybylowicz J, Przybylowicz W, Ostachowicz B, Augustyniak M, Nakonieczny M, Migula P (2002) Trace elements in the chrysomelid beetle (Chrysolina pardalina) and its Ni-hyperaccumulating host-plant (Berkheya coddii). Frasenius Environ Bull 11:78–84

    Google Scholar 

  • Mesjasz-Przybyłowicz J, Nakonieczny M, Migula P, Augustyniak M, Tarnawska M, Reimold WU, Koeberl C, Przybyłowicz W, Głowacka E (2004) Uptake of cadmium, lead, nickel and zinc from soil and water solutions by the nickel hyperaccumulator Berkheya Coddii. Acta Biol Cracov Bot 46:75–85

    Google Scholar 

  • Michielse CB, Rep M (2009) Pathogen profile update: Fusarium oxysporum. Mol Plant Pathol 10(3):311–324

    Article  PubMed  CAS  Google Scholar 

  • Migula P, Przybylowicz WJ, Mesjasz-Przybylowicz J, Augustyniak M, Nakonieczny M, Glowacka E, Tarnawska M (2007) Micro-PIXE studies of elemental distribution in sap feeding insects associated with Ni hyperaccumulator, Berkheya coddii. Plant Soil 293:197–207

    Article  CAS  Google Scholar 

  • Migula P, Przybylowicz WJ, Nakonieczny M, Augustyniak M, Tarnawska M, Mesjasz-Przybylowicz J (2011) Micro-PIXE studies of Ni-elimination strategies in representatives of two families of beetles feeding on Ni-hyperaccumulating plant Berkheya coddii. X-ray Spectrom 40:194–197

    Article  CAS  Google Scholar 

  • Moradi AB, Siegfried S, Robinson B, Prohaska T, Kaestner A, Oswald SE, Wenzel WW, Schuling R (2010) Mapping of nickel in root cross-sections of the hyperaccumulator plant Berkheya coddii using laser ablation ICP-MS. Environ Exp Bot 69:24–31

    Article  CAS  Google Scholar 

  • Morais PB, Pagnocca FC, Rosa CA (2006) Yeast communities in tropical rain forests in Brazil and other South American ecosystems. In: Rosa CA, Péter G (eds) The yeast handbook; Biodiversity and ecophysiology of yeasts. Springer-Verlag Berlin, Heidelberg

    Google Scholar 

  • Nakonieczny M (2007) Structural and functional adaptations of Chrysolina pardalina (Chrysomelidae; Coleoptera) to development on nickel hyperaccumulator Berkheya coddii (Asteraceae) – a comparative study with Chrysolina herbacea. Wydawnictwo Uniwersytetu Śląskiego, Katowice, Poland

    Google Scholar 

  • Nasini G, Arnone A, Assante G, Bava A, Moricca S, Ragazzi A (2004) Secondary mould metabolites of Cladosporium tenuissimum a hyperparasite of rust fungi. Phytochem 65:2107–2111

    Article  CAS  Google Scholar 

  • Nguyen NH, Suh S, Blackwell M (2007) Five novel Candida species in insect-associated yeast clades isolated from Neuroptera and other insects. Mycologia 99(6):842–858

    Article  PubMed  CAS  Google Scholar 

  • Nicholson JK, Holmes E, Kinross J, Burcelin R, Gibson G, Jia W, Pettersson S (2012) Host-gut microbiota metabolic interactions. Science 336(6086):1262–1267

    Article  PubMed  CAS  Google Scholar 

  • O’Donnell J, Dickinson CH (1980) Pathogenicity of Alternaria and Cladosporium isolates on Phaseolus. Trans Br Mycol Soc 74(2):731–738

    Google Scholar 

  • Orlowska E, Mesjasz-Przybylowicz J, Przybylowicz WJ, Turnau K (2008) Nuclear microprobe studies of elemental distribution in mycorrhizal and non-mycorrhizal roots of Ni-hyperaccumulator Berkheya coddii. X-Ray Spectrom 37:129–132

    Article  CAS  Google Scholar 

  • Orłowska E, Przybyłowicz W, Orłowski D, Turnau K, Mesjasz-Przybyłowicz J (2011) The effect of mycorrhiza on the growth and elemental composition of Ni-hyperaccumulating plant Berkheya coddii Roessler. Environ Pollut 159(12):3730–3738

    Article  PubMed  Google Scholar 

  • Padmavathy V (2008) Biosorption of nickel(II) ions by baker’s yeast: Kinetic, thermodynamic and desorption studies. Bioresource Technol 99:3100–3109

    Article  CAS  Google Scholar 

  • Reissinger A, Vilich V, Sikora RA (2001) Detection of fungi in planta: effectiveness of surface sterilization methods. Mycol Res 105(5):563–566

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Rascio N, Navari-Izzo F (2011) Heavy metal hyperaccumulating plants: How and why do they do it? And what makes them so interesting? Plant Sci 180:169–181

    Article  PubMed  CAS  Google Scholar 

  • Robinson BH, Brooks RR, Howes AW, Kirkman JH, Gregg PEH (1997) The potential of the high-biomass nickel hyperaccumulator Berkheya coddii for phytoremediation and phytomining. J Geochem Explor 60:115–126

    Article  CAS  Google Scholar 

  • Robinson BH, Brooks RR, Clothier BE (1999) Soil amendments affecting nickel and cobalt uptake by Berkheya coddii: potential use for phytomining and phytoremediation. Ann Bot 84:689–694

    Article  CAS  Google Scholar 

  • Robinson BH, Lombi E, Zhao FJ, McGrath SP (2003) Uptake and distribution of nickel and other metals in the hyperaccumulator Berkheya coddii. New Phytol 158:279–285

    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 

  • Saxena P, Bhattacharyya AK, Mathur N (2006) Nickel tolerance and accumulation by filamentous fungi from sludge of metal finishing industry. Geomicrobiol J 23(5):333–340

    Article  CAS  Google Scholar 

  • Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686

    Article  PubMed  Google Scholar 

  • Sugawara F, Strobel G, Fisher LE, Van Duyne GD, Clardy J (1985) Bipolaroxin, a selective phytotoxin produced by Bipolaris cynodontis. Proc Natl Acad Sci 82:8291–8294

    Article  PubMed  CAS  Google Scholar 

  • Suh SO, McHugh JV, Pollock DD, Blackwell M (2004) The beetle gut: a hyperdiverse source of novel yeasts. Mycol Res 109(3):261–265

    Article  Google Scholar 

  • Suh SO, Nguyen NH, Blackwell M (2008) Yeasts isolated from plant-associated beetles and other insects: seven novel Candida species near Candida albicans. FEMS Yeast Res 8:88–102

    Article  PubMed  CAS  Google Scholar 

  • Temuujin U, Kim J, Kim J, Lee B, Kang H (2011) Identification of novel pathogenicity-related cellulase genes in Xanthomonas oryzae pv. Oryzae Physiol Mol Plant Pathol 76:152–157

    Article  CAS  Google Scholar 

  • Turnau K, Mesjasz-Przybylowicz J (2003) Arbuscular mycorrhiza of Berkheya coddii and other Ni-hyperaccumulating members of Asteraceae from ultramafic soils in South Africa. Mycorrhiza 13:185–190

    Article  PubMed  Google Scholar 

  • Vadkertiová R, Sláviková E (2006) Metal tolerance of yeasts isolated from water, soil and plant environments. J Basic Microbiol 46(2):145–152

    Article  PubMed  Google Scholar 

  • Vega FE, Posada F, Peterson SW, Gianfagna TJ, Chaves F (2006) Penicillium species endophytic in coffee plants and ochratoxin A production. Mycologia 98(1):31–42

    Article  PubMed  CAS  Google Scholar 

  • Vreulink J-M, Stone W, Botha A (2010) Effects of small increases in copper levels on culturable basidiomycetous yeasts in low-nutrient soils. J App Microbiol 109:1411–1421

    Article  CAS  Google Scholar 

  • Wahid PA, Kalmalam NV, Jayasree S (1985) Determination of Phosphorus-32 in Wet-digested Plant Leaves by Cerenkov Counting. Int J Radiat App Isot 36(4):323–324

    Article  CAS  Google Scholar 

  • White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In. Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds.) PCR Protocols, San Diego Academic Press, p. 482

  • Winder RS, Van Dyke CG (1990) The pathogenicity, virulence and biocontrol potential of two Bipolaris species on Johnsongrass (Sorghum halepense). Weed Sci 38(1):89–94

    Google Scholar 

  • Xiao X, Luo S, Zeng G, Wei W, Wan Y, Chen L, Guo H, Cao Z, Yang L, Chen J, Xi Q (2010) Biosorption of cadmium by endophytic fungus (EF) Microsphaeropsis sp. LSE10 isolated from cadmium hyperaccumulator Solanum nigrum L. Bioresource Technol 101:1668–1674

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Alfred Botha.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Postma, F., Mesjasz-Przybyłowicz, J., Przybyłowicz, W. et al. Symbiotic interactions of culturable microbes with the nickel hyperaccumulator Berkheya coddii and the herbivorous insect Chrysolina clathrata . Symbiosis 58, 209–220 (2012). https://doi.org/10.1007/s13199-012-0217-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13199-012-0217-8

Keywords

Navigation