Abstract
Microalgae possess the ability to grow and glean nutrients from wastewater; such wastewater-grown biomass can be used as a biofertilizer for crops. The present investigation was undertaken to evaluate two formulations (formulation with unicellular microalgae (MC1) and formulation with filamentous microalgae (MC2); T4 and T5, respectively), prepared using wastewater-grown microalgal biomass, as a biofertilizer (after mixing with vermiculite/compost as a carrier) in wheat crop (Triticum aestivum L. HD2967) under controlled conditions. The highest values of available nitrogen (N), phosphorus (P), and potassium (K) in soil and nitrogen-fixing potential were recorded in treatment T5 (75 % N + full-dose PK + formulation with filamentous microalgae (MC2). Microbial biomass carbon was significantly enhanced by 31.8–67.0 % in both the inoculated treatments over control (recommended dose of fertilizers), with highest values in T4 (75 % N + full-dose PK + formulation with unicellular microalgae (MC1)). Both the microalgal formulations significantly increased the N, P, and K content of roots, shoots, and grains, and the highest total N content of 3.56 % in grains was observed in treatment T5. At harvest stage, the treatments inoculated with microalgal formulations (T4 and T5) recorded a 7.4–33 % increase in plant dry weight and up to 10 % in spike weight. The values of 1000-grain weight showed an enhancement of 5.6–8.4 %, compared with T1 (recommended doses of fertilizers). A positive correlation was observed between soil nutrient availability at mid crop stage and plant biometrical parameters at harvest stage. This study revealed the promise of such microalgal consortia as a biofertilizer for 25 % N savings and improved yields of wheat crop.
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References
Antolin MC, Pascual I, Garcia C, Polo A, Sanchez-Diaz M (2005) Growth, yield and solute content of barley in soils treated with sewage sludge under semiarid Mediterranean conditions. Field Crop Res 94:224–237
Babu S, Prasanna R, Bidyarani N, Singh R (2015) Analysing the colonisation of inoculated cyanobacteria in wheat plants using biochemical and molecular tools. J Appl Phycol 27:327–338
Bashan Y (1998) Inoculants of plant growth promoting bacteria for use in agriculture. Biotechnol Adv 16:729–770
Bhatnagar A, Bhatnagar M, Chinnasamy S, Das KC (2010) Chlorella minutissima—a promising fuel alga for cultivation in municipal wastewaters. Appl Biochem Biotechnol 161:523–536
Cabanelas ITD, Ruiz J, Arbib Z, Chinalia FA et al (2013) Comparing the use of different domestic wastewaters for coupling microalgal production and nutrient removal. Bioresour Technol 131:429–436
Chaudhary V, Prasanna R, Nain L et al (2012) Bioefficacy of novel cyanobacteria-amended formulations in suppressing damping off disease in tomato seedlings. World J Microbiol Biotechnol 28:3301–3310
Colica G, Li H, Rossi F, Li D, Liu Y, Philippis RD (2014) Microbial secreted exopolysaccharides affect the hydrological behavior of induced biological soil crusts in desert sandy soils. Soil Biol Biochem 68:62–70
de-Bashan LE, Bashan Y (2004) Recent advances in removing phosphorus from wastewater and its future use as fertilizer (1997–2003). Water Res 38:4222–4246
de-Bashan LE, Hernandez J, Morey T, Bashan Y (2004) Microalgae growth-promoting bacteria as “helpers” for microalgae: a novel approach for removing ammonium and phosphorus from municipal wastewater. Water Res 38:466–474
Faheed FA, Fattah ZA (2008) Effect of Chlorella vulgaris as bio-fertilizer on growth parameters and metabolic aspects of lettuce plant. J Agric Soc Sci 4:165–169
Fernandez JM, Plaza C, Garcia-Gil JC, Polo A (2009) Biochemical properties and barley yield in a semiarid Mediterranean soil amended with two kinds of sewage sludge. Appl Soil Ecol 42:18–24
Gantar M, Kerby NW, Rowell P, Obreht Z (1991) Colonization of wheat (Triticum vulgare L.) by N2-fixing cyanobacteria: I. A survey of soil cyanobacterial isolates forming associations with roots. New Phytol 118:477–483
Gatica J, Cytryn E (2013) Impact of treated wastewater irrigation on antibiotic resistance in soil microbiome. Environ Sci Pollut Res 20:3529–3538
Grotz N, Guerinot ML (2006) Molecular aspects of Cu, Fe, Zn homeostasis in plants. Biochem Biophys Acta 1763:595–608
Han HS, Supanjani, Lee KD (2006) Effect of co-inoculation with phosphate and potassium solubilizing bacteria on mineral uptake and growth of pepper and cucumber. Plant Soil Environ 52:130–136
Hegazi AZ, Mostafa SSM, Ahmed HMI (2010) Influence of different cyanobacterial application methods on growth and seed production of common bean under various levels of mineral nitrogen fertilization. Nat Sci 8:183–194
Hogh-Jense H, Pedersen MB (2003) Morphological plasticity by crop plants and their potassium use efficiency. J Plant Nutr 26:969–984
Hussain A, Husnain S (2011) Phytostimulation and biofertilization in wheat by cyanobacteria. J Ind Microbiol Biotechnol 38:85–92
Jackson ML (1958) Soil chemical analysis. Prentice Hall, New Jersey, p 498
Jaga PK, Patel Y (2012) An overview of fertilizers consumption in India: determinants and outlook for 2020—a review. Int J Sci Eng Technol 1:285–291
Jenkinson DS, Powlson DS (1976) The effects of biocidal treatment on metabolism in soil—V. A method for measuring soil biomass. Soil Biol Biochem 8:209–213
Junk A (2001) Root hairs and the acquisition of plant nutrients from soil. J Plant Nutr Soil Sci 64:121–129
Karthikeyan N, Prasanna R, Nain L, Kaushik BD (2007) Evaluating the potential of plant growth promoting cyanobacteria as inoculants for wheat. Eur J Soil Biol 43:23–30
Karthikeyan N, Prasanna R, Sood A, Jaiswal P, Nayak S, Kaushik BD (2009) Physiological characterization and electron microscopic investigations of cyanobacteria associated with wheat rhizosphere. Folia Microbiol 54:43–51
Kaushik BD (1998) Use of cyanobacterial biofertilizer in rice cultivation: a technology improvement. In: Subramanian G, Kaushik BD, Venkataraman GS (eds) Cyanobacterial biotechnology. Science Publisher Inc, USA, pp 211–222
Kizilkaya R, Bayrakh B (2005) Effects of N-enriched sewage sludge on soil enzyme activities. Appl Soil Ecol 30:192–202
Lakaniemi A, Intihar VM, Tuovinen OH, Puhakka JA (2012) Growth of Chlorella vulgaris and associated bacteria in photobioreactors. Microb Biotechnol 5:69–78
Lata, Saxena AK, Tilak KVBR (2002) Biofertilizers to augment soil fertility and crop production. In: Krishna KR (ed) Soil fertility and crop production. Oxford and IBH Publishing Co Pvt Ltd, New Delhi, pp 279–312
Latare AM, Kumar O, Singh SK, Gupta A (2014) Direct and residual effect of sewage sludge on yield, heavy metals content and soil fertility under rice–wheat system. Ecol Eng 69:17–24
Lavakush, Yadav J, Verma JP, Jaiswal DK, Kumar A (2014) Evaluation of PGPR and different concentration of phosphorus level on plant growth, yield and nutrient content of rice (Oryza sativa). Ecol Eng 62:123–128
Manjunath M, Prasanna R, Sharma P, Nain L, Singh R (2011) Developing PGPR consortia using novel genera Providencia and Alcaligenes along with cyanobacteria for wheat. Arch Agron Soil Sci 57:873–887
Maqubela MP, Mnkeni PNS, Issa OM, Pardo MT, Acqui LPD (2009) Nostoc cyanobacterial inoculation in South African agricultural soils enhances soil structure, fertility, and maize growth. Plant Soil 315:79–92
Markou G, Georgakakis D (2011) Cultivation of filamentous cyanobacteria (blue-green algae) in agro-industrial wastes and wastewaters: a review. Appl Energy 88:3389–3401
Mazor G, Kidron GJ, Vonshak A, Abeliovich A (1996) The role of cyanobacterial exopolysaccharides in structuring desert microbial crusts. FEMS Microbiol Ecol 21:121–130
McColl RHS (1975) Availability of soil and sediment phosphorus to a planktonic alga. N Z J Mar Freshw Res 9:169–182
Mondal S, Singh RD, Patra AK, Dwivedi BS (2015) Changes in soil quality in response to short-term application of municipal sewage sludge in a Typic Haplustept under cowpea-wheat cropping system. Environ Nanotechnol Monit Manag. doi:10.1016/j.enmm.2014.12.001
Motsara MR, Bhattacharya P, Srivastava B (1995) Biofertilizer—technology, marketing and usage: a source book-cum-glossary. Fertilizer Development and Consultation Organization, New Delhi, p 183
Motta SR, Maggiore T (2013) Evaluation of nitrogen management in maize cultivation grows on soil amended with sewage sludge and urea. Eur J Agron 45:59–67
Nain L, Rana A, Joshi M et al (2010) Evaluation of synergistic effects of bacterial and cyanobacterial strains as biofertilizers for wheat. Plant Soil 331:217–230
Natesan R, Shanmugasundaram S (1989) Extracellular phosphate solubilization by the cyanobacterium Anabaena ARM310. J Biosci 14:203–208
Nieves-Cordones M, Aleman F, Martinez V, Rubio F (2014) K+ uptake in plant roots. The systems involved their regulation and parallels in other organisms. J Plant Physiol 171:688–695
Olsen SR, Cole CV, Watanabe FS, Dean LA (1954) Estimation of available phosphorus in soils by extraction with sodium bicarbonate. US Department of Agriculture, Washington DC, Circ No. 939
Owamah HI, Enaboifo MA, Izinyon OC (2014) Treatment of wastewater from raw rubber processing industry using water lettuce macrophyte pond and the reuse of its effluent as biofertilizer. Agric Water Manag 146:262–269
Parmar P, Sindhu SS (2013) Potassium solubilization by rhizosphere bacteria: influence of nutritional and environmental conditions. J Microbiol Res 3:25–31
Pittman JK, Dean AP, Osundeko O (2011) The potential of sustainable algal biofuel production using wastewater resources. Bioresour Technol 102:17–25
Prasad R, Shivay YS, Kumar D, Sharma SN (2006) Learning by doing exercises in soil fertility (a practical manual for soil fertility). Division of Agronomy, Indian Agricultural Research Institute, New Delhi, p 68
Prasanna R, Jaiswal P, Kaushik BD (2008) Cyanobacteria as potential options for environmental sustainability—promises and challenges. Indian J Microbiol 48:89–94
Prasanna R, Joshi M, Rana A, Shivay YS, Nain L (2012a) Influence of co-inoculation of bacteria-cyanobacteria on crop yield and C–N sequestration in soil under rice crop. World J Microbiol Biotechnol 28:1223–1235
Prasanna R, Nain L, Pandey AK, Saxena AK (2012b) Microbial diversity and multidimensional interactions in the rice ecosystem. Arch Agron Soil Sci 58:723–744
Prasanna R, Kumar A, Babu S et al (2013) Deciphering the biochemical spectrum of novel cyanobacterium-based biofilms for use as inoculants. Biol Agric Hortic 29:145–158
Prasanna R, Babu S, Bidyarani N et al (2014) Prospecting cyanobacteria-fortified composts as plant growth promoting and biocontrol agents in cotton. Exp Agric 51:42–65
Rai AN, Soderback E, Bergman B (2000) Cyanobacterial plant symbioses. New Phytol 147:449–481
Rana A, Joshi M, Prasanna R, Shivay YS, Nain L (2012) Biofortification of wheat through inoculation of plant growth promoting rhizobacteria and cyanobacteria. Eur J Soil Biol 50:118–126
Renuka N (2015) Microalgal diversity, nutrient removal potential and utilization of biomass from sewage wastewater. PhD thesis, Panjab University, India, p 252
Renuka N, Sood A, Ratha SK, Prasanna R, Ahluwalia AS (2013a) Evaluation of microalgal consortia for treatment of primary treated sewage effluent and biomass production. J Appl Phycol 25:1529–1537
Renuka N, Sood A, Ratha SK, Prasanna R, Ahluwalia AS (2013b) Nutrient sequestration, biomass production by microalgae and phytoremediation of sewage wastewater. Int J Phytoremediation 15:789–800
Renuka N, Sood A, Prasanna R, Ahluwalia AS (2014) Influence of seasonal variation in water quality on the microalgal diversity of sewage wastewater. S Afr J Bot 90:137–145
Renuka N, Sood A, Prasanna R, Ahluwalia AS (2015) Phycoremediation of wastewaters: a synergistic approach using microalgae for bioremediation and biomass generation. Int J Environ Sci Technol 12:1443–1460
Savci S (2012) An agricultural pollutant: chemical fertilizer. Int J Environ Sci Dev 3:77–80
Sharma SB, Sayyed R, Trivedi MH, Gobi TA (2013) Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. SpringerPlus 2:587
Sheng XF, He LH (2006) Solubilization of potassium-bearing minerals by a wild type strain of Bacillus edaphicus and its mutants and increased potassium uptake by wheat. Can J Microbiol 52:66–72
Singh JK, Pandey VM, Singh DP (2011) Efficient soil microorganisms: a new dimension for sustainable agriculture and environmental development. Agric Ecosyst Environ 140:339–353
Sood A, Singh PK, Kumar A, Singh R, Prasanna R (2011) Growth and biochemical characterization of associations between cyanobionts and wheat seedlings in co-culturing experiments. Biologia 66:104–110
Su Y, Mennerich A, Urban B (2011) Municipal wastewater treatment and biomass accumulation with a wastewater-born and settleable algal–bacterial culture. Water Res 45:3351–3358
Subbiah BV, Asija GL (1956) A rapid procedure for the determination of available nitrogen in soils. Curr Sci 25:259–260
Toha J, Soto M, Contreras S (1991) Removal of faecal coliform in high pH ponds using rapid growth alga biomass. Int J Environ Health Res 1:236–239
Vaishampayan M, Sinha RP, Hader DP, Dey T, Gupta AK, Bhan AK, Rao AL (2001) Cyanobacterial biofertilizers in rice agriculture. Bot Rev 6:453–516
Venkataraman GS (1972) Algal biofertilizers and rice cultivation. Today and Tomorrow, New Delhi, p 75
Vivaldi GA, Camposeo S, Rubino P, Lonigro A (2013) Microbial impacts of different types of municipal wastewaters used to irrigate nectarines in Southern Italy. Agric Ecosyst Environ 181:50–57
Voroney RP, Winter JP, Bayaert RP (1993) Soil microbial biomass C and N. In: Carter MR (ed) Soil sampling and methods of analysis. Lewis, Boca Raton, pp 277–286
Warman PR, Termeer WC (2005) Evaluation of sewage sludge, septic waste and sludge compost applications to corn and forage: yields and N, P and K content of crops and soils. Bioresour Technol 96:955–961
Wigoda N, Moshelion M, Moran N (2014) Is the leaf bundle sheath a “smart flux valve” for K+ nutrition? J Plant Physiol 171:715–722
Yan Y, Hou H, Ren T, Xu Y, Wang Q, Xu W (2013) Utilization of environmental waste cyanobacteria as a pesticide carrier: studies on controlled release and photostability of avermectin. Colloids Surf B 102:341–347
Yasmeen T, Ali Q, Islam F, Noman A, Akram MS, Javed MT (2014) Biologically treated wastewater fertigation induced growth and yield enhancement effects in Vigna radiata L. Agric Water Manag 146:124–130
Zhan J, Sun Q (2012) Diversity of free-living nitrogen-fixing microorganisms in the rhizosphere and non-rhizosphere of pioneer plants growing on wastelands of copper mine tailings. Microbiol Res 167:157–165
Zhang S, White TL, Martinez M, McInroy C, Kloepper JA, Klassen JWW (2010) Evaluation of plant growth-promoting rhizobacteria for control of Phytophthora blight on squash under greenhouse conditions. Biol Control 53:129–135
Zorb C, Senbayram M, Peiter E (2014) Potassium in agriculture—status and perspectives. J Plant Physiol 171:656–669
Acknowledgments
The first author is thankful to the University Grants Commission, New Delhi, for her fellowship. All the authors are thankful to the Department of Botany, Panjab University, Chandigarh, and to the Division of Microbiology, Division of Agronomy, and National Phytotron Facility, ICAR-Indian Agricultural Research Institute, New Delhi, for providing the research facilities to carry out the present investigation.
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Supplementary Fig. 1
(A–F) Correlation between nutrient characteristics at mid crop and plant biometrical parameters at harvest stage. A Soil available N at mid crop and plant dry weight at harvest stage. B Soil available P at mid crop and plant dry weight at harvest stage. C Soil available N at mid crop and Spike weight at harvest stage. D Soil available P at mid crop and spike weight at harvest stage. E Soil available N at mid crop and 1000 grain weight at harvest. F Soil available K at mid crop and 1000 grain weight at harvest (XLS 138 kb)
Supplementary Fig. 2
(A–F) Correlation between shoot nutrient characteristics and plant biometrical parameters at harvest stage. A Shoot N content and straw yield. B Shoot P content and straw yield. C Shoot N content and spike weight. D Shoot P content and spike weight. E Shoot N content and 1000 grain weight. F Shoot P content and 1000 grain weight (XLS 172 kb)
Supplementary Fig. 3
Correlation between (A–C) different plant characteristics at harvest stage. (D–F) Grain nutrient characteristics at harvest stage and soil nutrient characteristics at mid crop stage. A Shoot K content and 1000 grain weight at harvest. B Root N content and straw yield at harvest. C Root N content and plant dry weight at harvest. D Soil available N at mid crop and Grain N content at harvest. E Soil available P at mid crop and Grain P content at harvest. F Soil available K at mid crop and Grain K content at harvest (XLS 213 kb)
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Renuka, N., Prasanna, R., Sood, A. et al. Exploring the efficacy of wastewater-grown microalgal biomass as a biofertilizer for wheat. Environ Sci Pollut Res 23, 6608–6620 (2016). https://doi.org/10.1007/s11356-015-5884-6
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DOI: https://doi.org/10.1007/s11356-015-5884-6