A preliminary study of the role of bacterial–fungal co-inoculation on heavy metal phytotoxicity in serpentine soil
Mihiri Seneviratne A , Gamini Seneviratne A , H. M. S. P. Madawala B , M. C. M. Iqbal C , Nishanta Rajakaruna D E , Tharanga Bandara F and Meththika Vithanage F G
+ Author Affiliations
- Author Affiliations
A Microbial Biotechnology Unit, Institute of Fundamental Studies, Kandy 20000, Sri Lanka.
B Department of Botany, University of Peradeniya, Sri Lanka.
C Plant Biology Group, Institute of Fundamental Studies, Kandy 20000, Sri Lanka.
D College of the Atlantic, Bar Harbor, ME 04609, USA.
E Unit for Environmental Sciences and Management, North-West University, Potchefstroom, 2520, South Africa.
F Chemical and Environmental Systems Model Research Group, Institute of Fundamental Studies, Kandy 20000, Sri Lanka.
G Corresponding author. Email: meththikavithanage@gmail.com
Australian Journal of Botany 63(4) 261-268 https://doi.org/10.1071/BT14270
Submitted: 15 October 2014 Accepted: 13 February 2015 Published: 17 April 2015
Abstract
This study was conducted to understand the role of bacterial–fungal interactions on heavy metal uptake by Zea mays plants. A pot experiment was conducted for 90 days with Z. mays in serpentine soil inoculated with a Gram-negative bacterium, fungus (Aspergilllus sp.) and both microbes to determine the effects of inoculation on nickel, manganese, chromium and cobalt concentrations in plant tissue and soil. Soil nutrients and soil enzyme activities were measured to determine the effect of inoculations on soil quality. Inoculation of microorganisms increased shoot and root biomass, and the maximum biomass was in the bacterial–fungal inoculation. This could be due to the solubilisation of phosphate and production of indole acetic acid. Although the combination treatment contributed to an increase in heavy metal uptake in Z. mays plants, the lowest translocation was observed in the combination treatment. Moreover, the soil available nitrogen, available phosphorous and total organic carbon content were increased with the microbial inoculation. Similarly, the soil dehydrogenase activity was higher as a result of microbial inoculation, whereas the highest dehydrogenase activity was reported in the combination inoculation. This study confirms the synergistic effect of bacterial–fungal inoculation as a soil-quality enhancer and as a plant-growth promoter in the presence of heavy metals.
Additional keywords: bioremediation, enzyme activity, heavy metal availability, soil quality, synergistic effect.
References
Abou‐Shanab R, Angle J, Delorme T, Chaney R, Van Berkum P, Moawad H, Ghanem K, Ghozlan H (2003) Rhizobacterial effects on nickel extraction from soil and uptake by Alyssum murale. New Phytologist 158, 219–224.| Rhizobacterial effects on nickel extraction from soil and uptake by Alyssum murale.Crossref | GoogleScholarGoogle Scholar |
Achuba F, Peretiemo-Clarke BO (2008) Effect of spent engine oil on soil catalase and dehydrogenase activities. International Agrophysics 22, 1–4.
Ahmad I, Ansari MI, Aqil F (2006) Biosorption of Ni, Cr and Cd by metal tolerant Aspergillus niger and Penicillium sp. using single and multi-metal solution. Indian Journal of Experimental Biology 44, 73–76.
Alexander E (1988) Morphology, fertility and classification of productive soils on serpentinized peridotite in California (USA). Geoderma 41, 337–351.
| Morphology, fertility and classification of productive soils on serpentinized peridotite in California (USA).Crossref | GoogleScholarGoogle Scholar |
Alloway BJ (Ed.) (1995) ‘Heavy metals in soils.’ (Blackie Academic and Professional: London)
Anacker BL (2014) The nature of serpentine endemism. American Journal of Botany 101, 219–224.
| The nature of serpentine endemism.Crossref | GoogleScholarGoogle Scholar | 24509800PubMed |
Anahid S, Yaghmaei S, Ghobadinejad Z (2011) Heavy metal tolerance of fungi. Scientia Iranica 18, 502–508.
| Heavy metal tolerance of fungi.Crossref | GoogleScholarGoogle Scholar |
Anjum NA, Ahmad I, Pereira ME, Duarte AC, Umar S, Khan NA (2012) ‘The plant family Brassicaceae: contribution towards phytoremediation.’ (Springer Science & Business Media: Dordrecht, The Netherlands)
Antibachi D, Kelepertzis E, Kelepertsis A (2012) Heavy metals in agricultural soils of the Mouriki–Thiva area (central Greece) and environmental impact implications. Soil and Sediment Contamination: an International Journal 21, 434–450.
| Heavy metals in agricultural soils of the Mouriki–Thiva area (central Greece) and environmental impact implications.Crossref | GoogleScholarGoogle Scholar |
Barker AV, Pilbeam DJ (2014) ‘Handbook of plant nutrition.’ (CRC Press: Boca Raton, FL)
Belimov A, Hontzeas N, Safronova V, Demchinskaya S, Piluzza G, Bullitta S, Glick B (2005) Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.). Soil Biology & Biochemistry 37, 241–250.
| Cadmium-tolerant plant growth-promoting bacteria associated with the roots of Indian mustard (Brassica juncea L. Czern.).Crossref | GoogleScholarGoogle Scholar |
Brady KU, Kruckeberg AR, Bradshaw H (2005) Evolutionary ecology of plant adaptation to serpentine soils. Annual Review of Ecology Evolution and Systematics 36, 243–266.
| Evolutionary ecology of plant adaptation to serpentine soils.Crossref | GoogleScholarGoogle Scholar |
Brown PH, Welch RM, Cary EE, Checkai RT (1987) Micronutrients: beneficial effects of nickel on plant growth. Journal of Plant Nutrition 10, 2125–2135.
| Micronutrients: beneficial effects of nickel on plant growth.Crossref | GoogleScholarGoogle Scholar |
Burd GI, Dixon DG, Glick BR (1998) A plant growth-promoting bacterium that decreases nickel toxicity in seedlings. Applied and Environmental Microbiology 64, 3663–3668.
Burd GI, Dixon DG, Glick BR (2000) Plant growth-promoting bacteria that decrease heavy metal toxicity in plants. Canadian Journal of Microbiology 46, 237–245.
| Plant growth-promoting bacteria that decrease heavy metal toxicity in plants.Crossref | GoogleScholarGoogle Scholar | 10749537PubMed |
Caldwell BA (2005) Enzyme activities as a component of soil biodiversity: a review. Pedobiologia 49, 637–644.
| Enzyme activities as a component of soil biodiversity: a review.Crossref | GoogleScholarGoogle Scholar |
Casida LE, Klein D, Santoro T (1964) Soil dehydrogenase activity. Soil Science 98, 371–376.
| Soil dehydrogenase activity.Crossref | GoogleScholarGoogle Scholar |
Cataldo D, Maroon M, Schrader L, Youngs V (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid 1. Communications in Soil Science and Plant Analysis 6, 71–80.
| Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid 1.Crossref | GoogleScholarGoogle Scholar |
Chu H, Lin X, Fujii T, Morimoto S, Yagi K, Hu J, Zhang J (2007) Soil microbial biomass, dehydrogenase activity, bacterial community structure in response to long-term fertilizer management. Soil Biology & Biochemistry 39, 2971–2976.
| Soil microbial biomass, dehydrogenase activity, bacterial community structure in response to long-term fertilizer management.Crossref | GoogleScholarGoogle Scholar |
Crossgrove J, Zheng W (2004) Manganese toxicity upon overexposure. NMR in Biomedicine 17, 544–553.
| Manganese toxicity upon overexposure.Crossref | GoogleScholarGoogle Scholar | 15617053PubMed |
Dayan A, Paine A (2001) Mechanisms of chromium toxicity, carcinogenicity and allergenicity: review of the literature from 1985 to 2000. Human and Experimental Toxicology 20, 439–451.
| Mechanisms of chromium toxicity, carcinogenicity and allergenicity: review of the literature from 1985 to 2000.Crossref | GoogleScholarGoogle Scholar | 11776406PubMed |
Dell’Amico E, Cavalca L, Andreoni V (2005) Analysis of rhizobacterial communities in perennial Graminaceae from polluted water meadow soil, and screening of metal‐resistant, potentially plant growth‐promoting bacteria. FEMS Microbiology Ecology 52, 153–162.
| Analysis of rhizobacterial communities in perennial Graminaceae from polluted water meadow soil, and screening of metal‐resistant, potentially plant growth‐promoting bacteria.Crossref | GoogleScholarGoogle Scholar | 16329902PubMed |
Denkhaus E, Salnikow K (2002) Nickel essentiality, toxicity, and carcinogenicity. Critical Reviews in Oncology/Hematology 42, 35–56.
| Nickel essentiality, toxicity, and carcinogenicity.Crossref | GoogleScholarGoogle Scholar | 11923067PubMed |
Gadd GM (2010) Metals, minerals and microbes: geomicrobiology and bioremediation. Microbiology 156, 609–643.
| Metals, minerals and microbes: geomicrobiology and bioremediation.Crossref | GoogleScholarGoogle Scholar | 20019082PubMed |
Gadd GM, Sayer JA (2000) Influence of fungi on the environmental mobility of metals and metalloids. In ‘Environmental microbe–metal interactions’. (Ed. D Lovley) pp. 237–256. (ASM Press: Washington, DC)
Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica 2012,
| Plant growth-promoting bacteria: mechanisms and applications.Crossref | GoogleScholarGoogle Scholar | 24278762PubMed |
Grichko VP, Glick BR (2001) Amelioration of flooding stress by ACC deaminase-containingplant growth-promoting bacteria. Plant Physiology and Biochemistry 39, 11–17.
| Amelioration of flooding stress by ACC deaminase-containingplant growth-promoting bacteria.Crossref | GoogleScholarGoogle Scholar |
Gupta AK, Sinha S (2006) Chemical fractionation and heavy metal accumulation in the plant of Sesamum indicum (L.) var. T55 grown on soil amended with tannery sludge: selection of single extractants. Chemosphere 64, 161–173.
| Chemical fractionation and heavy metal accumulation in the plant of Sesamum indicum (L.) var. T55 grown on soil amended with tannery sludge: selection of single extractants.Crossref | GoogleScholarGoogle Scholar | 16330080PubMed |
Haferburg G, Kothe E (2007) Microbes and metals: interactions in the environment. Journal of Basic Microbiology 47, 453–467.
| Microbes and metals: interactions in the environment.Crossref | GoogleScholarGoogle Scholar | 18072246PubMed |
Hall J (2002) Cellular mechanisms for heavy metal detoxification and tolerance. Journal of Experimental Botany 53, 1–11.
| Cellular mechanisms for heavy metal detoxification and tolerance.Crossref | GoogleScholarGoogle Scholar | 11741035PubMed |
Harrison S, Rajakaruna N (2011) ‘Serpentine: the evolution and ecology of a model system.’ (University of California Press: Berkeley, CA)
Herath H, Rajapaksha AU, Vithanage M, Seneviratne G (2013) Developed fungal–bacterial biofilms as a novel tool for bioremoval of hexavelant chromium from wastewater. Chemistry and Ecology 30, 418–427.
| Developed fungal–bacterial biofilms as a novel tool for bioremoval of hexavelant chromium from wastewater.Crossref | GoogleScholarGoogle Scholar |
Jiang C-y, Sheng X-f, Qian M, Wang Q-y (2008) Isolation and characterization of a heavy metal-resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in promoting plant growth and heavy metal accumulation in metal-polluted soil. Chemosphere 72, 157–164.
| Isolation and characterization of a heavy metal-resistant Burkholderia sp. from heavy metal-contaminated paddy field soil and its potential in promoting plant growth and heavy metal accumulation in metal-polluted soil.Crossref | GoogleScholarGoogle Scholar | 18348897PubMed |
Jones DL, Darrah PR (1994) Role of root derived organic acids in the mobilization of nutrients from the rhizosphere. Plant and Soil 166, 247–257.
| Role of root derived organic acids in the mobilization of nutrients from the rhizosphere.Crossref | GoogleScholarGoogle Scholar |
Kabata-Pendias A (2010) ‘Trace elements in soils and plants.’ (CRC Press: Boca Raton, FL)
Ladd JN (1978) ‘Origin and range of enzymes in soil. In ‘Soil enzymes’. (Ed. RG Burns) pp. 51–96. (Academic Press: London)
Ma Y, Rajkumar M, Freitas H (2009) Improvement of plant growth and nickel uptake by nickel resistant-plant-growth promoting bacteria. Journal of Hazardous Materials 166, 1154–1161.
| Improvement of plant growth and nickel uptake by nickel resistant-plant-growth promoting bacteria.Crossref | GoogleScholarGoogle Scholar | 19147283PubMed |
Ma Y, Rajkumar M, Rocha I, Oliveira RS, Freitas H (2014) Serpentine bacteria influence metal translocation and bioconcentration of Brassica juncea and Ricinus communis grown in multi-metal polluted soils. Frontiers in Plant Science 5,
Madhaiyan M, Poonguzhali S, Sa T (2007) Metal tolerating methylotrophic bacteria reduces nickel and cadmium toxicity and promotes plant growth of tomato (Lycopersicon esculentum L.). Chemosphere 69, 220–228.
| Metal tolerating methylotrophic bacteria reduces nickel and cadmium toxicity and promotes plant growth of tomato (Lycopersicon esculentum L.).Crossref | GoogleScholarGoogle Scholar | 17512031PubMed |
Miranda M, Benedito J, Blanco-Penedo I, López-Lamas C, Merino A, Lopez-Alonso M (2009) Metal accumulation in cattle raised in a serpentine-soil area: relationship between metal concentrations in soil, forage and animal tissues. Journal of Trace Elements in Medicine and Biology 23, 231–238.
| Metal accumulation in cattle raised in a serpentine-soil area: relationship between metal concentrations in soil, forage and animal tissues.Crossref | GoogleScholarGoogle Scholar | 19486833PubMed |
Mishra D, Kar M (1974) Nickel in plant growth and metabolism. Botanical Review 40, 395–452.
| Nickel in plant growth and metabolism.Crossref | GoogleScholarGoogle Scholar |
Neilson S, Rajakaruna N (2012) Roles of rhizospheric processes and plant physiology in applied phytoremediation of contaminated soils using Brassica oilseeds. In ‘The plant family Brassicaceae’. (Eds NA Anjum, I Ahmad, ME Pereira, AC Duarte, S Umar, NA Khan) pp. 313–330. (Springer: Dordrecht, The Netherlands)
Nocito FF, Lancilli C, Crema B, Fourcroy P, Davidian J-C, Sacchi GA (2006) Heavy metal stress and sulfate uptake in maize roots. Plant Physiology 141, 1138–1148.
| Heavy metal stress and sulfate uptake in maize roots.Crossref | GoogleScholarGoogle Scholar | 16698905PubMed |
Panaccione DG, Sheets NL, Miller SP, Cumming JR (2001) Diversity of Cenococcum geophilum isolates from serpentine and non-serpentine soils. Mycologia 93, 645–652.
| Diversity of Cenococcum geophilum isolates from serpentine and non-serpentine soils.Crossref | GoogleScholarGoogle Scholar |
Proctor J, Woodell SR (1975) The ecology of serpentine soils. Advances in Ecological Research 9, 255–366.
| The ecology of serpentine soils.Crossref | GoogleScholarGoogle Scholar |
Rajapaksha AU, Vithanage M, Oze C, Bandara W, Weerasooriya R (2012) Nickel and manganese release in serpentine soil from the Ussangoda Ultramafic Complex, Sri Lanka. Geoderma 189–190, 1–9.
| Nickel and manganese release in serpentine soil from the Ussangoda Ultramafic Complex, Sri Lanka.Crossref | GoogleScholarGoogle Scholar |
Rajkumar M, Freitas H (2008) Influence of metal resistant-plant growth-promoting bacteria on the growth of Ricinus communis in soil contaminated with heavy metals. Chemosphere 71, 834–842.
| Influence of metal resistant-plant growth-promoting bacteria on the growth of Ricinus communis in soil contaminated with heavy metals.Crossref | GoogleScholarGoogle Scholar | 18164365PubMed |
Rajkumar M, Nagendran R, Lee KJ, Lee WH (2005) Characterization of a novel Cr6+ reducing Pseudomonas sp. with plant growth-promoting potential. Current Microbiology 50, 266–271.
| Characterization of a novel Cr6+ reducing Pseudomonas sp. with plant growth-promoting potential.Crossref | GoogleScholarGoogle Scholar | 15886910PubMed |
Richardson AE, Simpson RJ (2011) Soil microorganisms mediating phosphorus availability update on microbial phosphorus. Plant Physiology 156, 989–996.
| Soil microorganisms mediating phosphorus availability update on microbial phosphorus.Crossref | GoogleScholarGoogle Scholar | 21606316PubMed |
Seneviratne G, Thilakaratne R, Jayasekara A, Seneviratne K, Padmathilake K, De Silva M (2009) Developing beneficial microbial biofilms on roots of non legumes: a novel biofertilizing technique. In ‘Microbial strategies for crop improvement’. (Eds MS Khan, A Zaidi, J Musarrat) pp. 51–62. (Springer-Verlag: Berlin Heidelberg)
Shallari S, Schwartz C, Hasko A, Morel J (1998) Heavy metals in soils and plants of serpentine and industrial sites of Albania. The Science of the Total Environment 209, 133–142.
| Heavy metals in soils and plants of serpentine and industrial sites of Albania.Crossref | GoogleScholarGoogle Scholar | 9514035PubMed |
Sheng X-F, Xia J-J (2006) Improvement of rape (Brassica napus) plant growth and cadmium uptake by cadmium-resistant bacteria. Chemosphere 64, 1036–1042.
| Improvement of rape (Brassica napus) plant growth and cadmium uptake by cadmium-resistant bacteria.Crossref | GoogleScholarGoogle Scholar | 16516946PubMed |
Sheng X-F, Xia J-J, Jiang C-Y, He L-Y, Qian M (2008) Characterization of heavy metal-resistant endophytic bacteria from rape (Brassica napus) roots and their potential in promoting the growth and lead accumulation of rape. Environmental Pollution 156, 1164–1170.
| Characterization of heavy metal-resistant endophytic bacteria from rape (Brassica napus) roots and their potential in promoting the growth and lead accumulation of rape.Crossref | GoogleScholarGoogle Scholar | 18490091PubMed |
Smith SE, Read DJ (1996) ‘Mycorrhizal symbiosis.’ (Academic Press: New York)
Southworth D, Tackaberry LE, Massicotte HB (2014) Mycorrhizal ecology on serpentine soils. Plant Ecology & Diversity 7, 445–455.
Srivastava PK, Shenoy BD, Gupta M, Vaish A, Mannan S, Singh N, Tewari SK, Tripathi RD (2012) Stimulatory effects of arsenic-tolerant soil fungi on plant growth promotion and soil properties. Microbes and Environments 27, 477–482.
| Stimulatory effects of arsenic-tolerant soil fungi on plant growth promotion and soil properties.Crossref | GoogleScholarGoogle Scholar | 23047145PubMed |
Vithanage M, Rajapaksha AU, Oze C, Rajakaruna N, Dissanayake C (2014) Metal release from serpentine soils in Sri Lanka. Environmental Monitoring and Assessment 186, 3415–3429.
| Metal release from serpentine soils in Sri Lanka.Crossref | GoogleScholarGoogle Scholar | 24464398PubMed |
Watanabe F, Olsen S (1965) Test of an ascorbic acid method for determining phosphorus in water and NaHCO3 extracts from soil. Soil Science Society of America Journal 29, 677–678.
| Test of an ascorbic acid method for determining phosphorus in water and NaHCO3 extracts from soil.Crossref | GoogleScholarGoogle Scholar |
Weissenhorn I, Leyval C, Belgy G, Berthelin J (1995) Arbuscular mycorrhizal contribution to heavy metal uptake by maize (Zea mays L.) in pot culture with contaminated soil. Mycorrhiza 5, 245–251.
Wenzel W, Bunkowski M, Puschenreiter M, Horak O (2003) Rhizosphere characteristics of indigenously growing nickel hyperaccumulator and excluder plants on serpentine soil. Environmental Pollution 123, 131–138.
| Rhizosphere characteristics of indigenously growing nickel hyperaccumulator and excluder plants on serpentine soil.Crossref | GoogleScholarGoogle Scholar | 12663213PubMed |
Zaidi S, Usmani S, Singh BR, Musarrat J (2006) Significance of Bacillus subtilis strain SJ-101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea. Chemosphere 64, 991–997.
| Significance of Bacillus subtilis strain SJ-101 as a bioinoculant for concurrent plant growth promotion and nickel accumulation in Brassica juncea.Crossref | GoogleScholarGoogle Scholar | 16487570PubMed |
