Research Article

The Role of Cyanobacteria in Availability of Major Plant Nutrients and Soil Organic Matter to Rice Crop under Saline Soil Condition

Zakirullah Jan1, Shamsher Ali1*, Tariq Sultan2, Wasiullah1 and Wiqar Ahmad1

1Department of Soil & Environmental Sciences, Amir Muhammad Khan Campus, Mardan, The University of Agriculture Peshawar-Pakistan; 2Soil Biology and Biochemistry laboratory, National Agriculture Research Center, Islamabad, Pakistan.

Received | July 12, 2017; Accepted | September 16, 2017; Published | October 27, 2017

*Correspondence | Shamsher Ali, Amir Muhammad Khan Campus, Mardan, The University of Agriculture Peshawar-Pakistan; Email: shamsherali@aup.edu.pk

Citation | Jan, Z. , S. Ali, T. Sultan, Wasiullah and W. Ahmad. 2017. The role of cyanobacteria on availability of major plant nutrients and soil organic matter to rice crop under saline soil condition. Sarhad Journal of Agriculture, 33(4): 566-572.

DOI | http://dx.doi.org/10.17582/journal.sja/2017/33.4.566.572

Keywords | Cyanobacteria, Saline soil, Major plant nutrients, Soil organic matter, Rice crop

Introduction

There are various types of constrains to crop production in the field of agriculture in the world, particularly in Pakistan. One of them is salt affected soils. The increase of salt concentration in the soils usually causes both sodicity and salinity and pose a main threat to various crops cultivation in arid and semi-arid regions of the Pakistan (Ashraf and Khan, 1994). In these regions precipitation is not sufficient to percolate salts and sodium ions out of the root zone. These salts are greatly responsible for declining the cultivated land worldwide. Globally, irrigated land covers about 310 million hectares (m ha), an estimated 20% of it is salt affected (62 m ha) (Qadir et al., 2014). In Pakistan, total geographical area is 79.6 m ha, out of which only 25 % (19.82 m ha) is under cultivation. The whole country has more than 6.30 m ha salt affected land (Alam et al., 2000). Also, salinity is a major constrain in both irrigated and un-irrigated agriculture (Mujeeb and Diaz, 2002). In arid and semi-arid regions, fertilization and use of brackish water for irrigation purposes build up root zone salinity (Villa et al., 2003). Osmotic stress, specific ion toxicity and disturbance of nutrients are the dangerous effects of salinity on plants (Qayyum et al., 2007).

The application of N, P and K and other essential nutrients from various sources to saline soil can reduce the stress of salts and increase salt tolerance of various crops. Imbalance nutrition due to impaired uptake and transport of essential plant nutrients under saline condition is well documented in crops leading to diminished plant growth and production (Shahzad et al., 2012; Qu et al., 2012). Crop growth is severely affected by N-deficiency under salinity (Shahzad et al., 2012)

Different types of micro-organisms are used for increasing crop production, number of plants, improvement and availability of essential plant nutrients and microbial activity under saline soils. In microbes, cyanobacteria can easily survive in saline conditions and high pH (Verma and Abrol, 1980). Cyanobacteria may increase the soil fertility by different methods like secretion of harmons, acids, enzymes which when added to a soil, dissolve the fixed and unavailable nutrients. It also controls the nutrient loss through run-off, de-nitrification and leaching. Potassium is first accumulated by cyanobacteria from the saline medium by K+ up taking system (Reed and Stewart, 1985). The native cyanobacteria of soil, over a period of time improve the soil physical and chemical properties (Kaushik and Subhashini, 1985). Cyanobacteria significantly solubilize and make available the soil phosphorus and sulfur (Hashem, 2001). Cyanobacteria secrete different type of chemicals which can make available the soil plant nutrients like P, K and S in saline ecosystem (Singh, 1961). The cyanobacteria also help in decreasing soil pH (Elayarajan, 2002; Prabu and Udayasoorian, 2007), electrical conductivity (Prabu and Udayasoorian, 2007) and improve the soil aggregation i.e soil structure (Rogers and Burns, 1994; Rai et al., 2006).

Due to the above mentioned facts present experiment was designed to assess the role of cyanobacteria on some major plant nutrients availability and resultant improvement in soil organic matter under saline soil conditions.

Materials and Methods

An experiment in pots was carried out with the aim to assess the role of different strains of cyanobacteria in improvement of major plant nutrients, soil organic matter content and rice production under saline soil condition at the National Agricultural Research Center (NARC) Islamabad during summer 2016. The experimental pots were arranged in completely randomized design (CRD) with three replications. Each pot was induced with salinity of 7.0 dS m-1. Five different locally identified strains of cyanobacteria i.e Oscillatory-MMF-1 (Oscillatoria princeps), Leptolyngbaya-MMF-2 (Lyngbya mucicola), Leptolyngbaya- MMF-3 (Lyngbya Phormidium), Gloeobacter-MMF-4 (Gloeocapsa) and Microcoleus-MMF-5 (Cryophilus) were collected from the Laboratory of Microbiology and Genetics, University of Punjab, Lahore and further multiplied for mass production in the Laboratory of Soil Biology and Biochemistry, National Agricultural Research Center, Islamabad. These five strains of cyanobacteria and a control (no strains) (a total of 6 treatments) were used to treat the pots with 7.0 dS m-1 induced saline soil.

Solution method was used for the application of cyanobacteria. In this method, the required amount of cyanobacteria was dissolved in one-liter water and applied to particular pot. Recommended rate (20 kg ha-1) of cyanobacteria of each strain was applied (Roger, 1991). No organic and chemical fertilizers were applied. Five seedlings of rice (Kainat, smooth cv.) crop from the nursery were transplanted to each pot on 18th August 2016 for their growth and development. The rice in all pots was flooded from transplanting to harvesting. All the cultural practices were applied during the growth period in green house and temperature ranged from 30-38 °C. Rice crop growth was maintained for about 3 months and harvested on October 30, 2016 and data on different rice parameter were collected.

The pre-sowing composite soil and post-harvest soil samples were obtained for analysis of various physicochemical properties of soil according to the standard methods/procedures in the laboratory of Soil Biology and Biochemistry, National Agriculture Research Center, Islamabad. Soil NO3-N, P and K were determined using ammonium bicarbonate-diethylene triamine pentaacetic acid extractable (AB-DTPA ext.) solution by the method of Soltanpour and Schwab (1977) and soil Ca++ and Mg++ by Atomic Absorption using the procedure of Richards (1954). Soil organic matter was determined by the method of Nelson and Sommer (1996).

Characterization of the pre-sowing soil

The analysis of pre-sowing soil sample was done before starting of the experiment, to determine the physiochemical properties of soil i.e. electrical conductivity, pH (McLean, 1982), organic matter, calcium, magnesium, texture, nitrogen, phosphorus and potassium (Ryan et al., 2013). The soil texture of the experimental soil was silt loam in nature, alkaline in reaction and having less organic matter content (Table 1).

Table 1: Physio-chemical properties of soil.

The collected data were statistically analyzed by ANOVA method of Completely Randomized Design procedure using Statistix 8.1 Package. The probability level for LSD test i.e 5 % level of significance was used to distinguish between the means (Steel and Torrie, 1980).

Results and Discussion

AB-DTPA extractable soil nitrate-nitrogen (NO3-N)

Statistical analysis of the data on soil NO3-N showed that differences between the mean values were significant (p ≤ 0.05) (Table 2). The highest amount of soil NO3-N (3.53 mg kg-1) was recorded in MMF-4 Gloeobacter strain followed by MMF-1 Oscillatoria (3.27 mg kg-1) which is statistically at par with each other. In control the lowest amount of NO3-N (162 mg kg-1) was observed as compared to other treatments (Table 2). Among the strains, the low content of nitrate-N (2.83 mg kg-1) was noted in MMF-3 Leptolyngbaya. The data of MMF-2 and MMF-5 are statistically similar. These results are supported by previous findings of Roger and Kulasooriya (1980), Metting (1990), Apte (1992); (1993), Lange et al. (1994), Aziz and Hashem (2003) and Wafaa et al. (2013). The researchers reported that cyanobacteria have ability to accumulate soil NO3−, NH4+ and P from other source and further release these ions in soil.

AB-DTPA extractable soil P

Statistical analysis of the data on soil P (Table 2) showed that the treatments means were significantly different (p < 0.05). The maximum amount of P (2.79 mg kg-1) was recorded in MMF-4 treatment followed by MMF-1 treatment (2.67 mg kg-1). MMF-2 treatment was (2.64 mg kg-1). The lowest value of P (1.59 mg kg-1) was measured in control. These findings are in accordance with Roychoudhury et al. (1985), Roychoudhury and Kaushik (1989), Hashem (2001) and Wafaa et al. (2013). These scientists reported that the application of cyanobacteria increased the availability of P, S and solubilized the unavailable rock phosphate and made it available to plants.

AB-DTPA extractable soil K+

Data on soil potassium showed that the treatments mean values of K+ were significantly (p < 0.05) different from one another (Table 2). The maximum amount of potassium (296 mg kg-1) was noted in MMF-4 treatment followed by MMF-5 treatment (283 mg kg-1). The treatments MMF-1, MMF-2 and MMF-3 were statistically at par with one another. The lowest value of potassium (226 mg kg-1) was recorded in control. These results are supported by the work of Reed and Stewart (1985), Matsuda et al. (2004) and Wafaa et al. (2013). They reported that cyanobacteria accumulate the potassium from medium by their uptake system and prepare glutamate compound thus K+ ions concentration increase in cytoplasm and by efflux of water.

Soil organic matter content (SOM)

Data on soil organic matter (Table 2) showed that the treatments mean values were significantly (p <0.05) different. The maximum amount of soil organic matter (5.4 g kg-1) was measured in MMF-4 treatment followed by MMF-2 treatment (4.9 g kg-1). The lowest amount of soil organic matter (1.4 g kg-1) was recorded in control. MMF-1 treatment (3.5 g kg-1) and MMF-5 treatment (3.3 g kg-1) was statistically similar. This might be due to the further growth of cyanobacteria (Heterotrophic one producing biomass) in the flooded pots and also due to the secretion of exudates from cyanobacteris, roots of rice. The cyanobacteria also make the environment favorable for the root growth in saline soil by producing more biomass, due to which the organic matter was improved. These results were supported by De and Sulaiman (1950), Kannaiyan and Pandiyarajan (1992), Rogers and Burns (1994), Apte and Thomas (1997), Prabu and Udayasoorian (2007) and Wafaa et al. (2013).

Table 2: AB-DTPA extractable NO3-N, P, K+ (mg kg-1) and soil organic matter (g Kg-1) of saline soil as influenced by application of different strains of cyanobacteria

Data on Ca+2 & Mg+2 were presented in Table 3. The analysis of variance indicated that the treatments means were significant (p <0.05). The maximum amount of Ca+2 (944 mg kg-1) was measured in MMF-4 treatment followed by MMF-2 treatment (910 mg kg-1). MMF-3 treatment (892 mg kg-1) and MMF-5 treatment (829 mg kg-1) were statistically different from each other. The lowest concentration of Ca+2 (715 mg kg-1) was noted in control. The analysis of magnesium showed that highest concentration of magnesium (358 mg kg-1) was recorded in MMF-4 treatment and MMF-2 treatment (341 mg kg-1). The lowest amount of magnesium (277 mg kg-1) was measured in control treatment. These results are similar to Shehata and Whitton (1982), Keurson et al. (1984), Singh (1985), Smith et al. (1987) and Pandey et al. (1996).

Plant dry weight (g pot-1)

Data on the plant dry weight (Table 3) revealed that the treatment mean values were significantly (p < 0.05) different from one another. The maximum dry weight (25 g pot-1) was measured in MMF-4 treatment and followed by MMF-3 treatment (24 g pot-1) which was statistically at par with each other. The rest of treatments were statistically similar. The minimum dry weight was recorded in control (18 g pot-1). These results are in accordance with the findings of Pendleton and Warren (1995) and Aziz and Hashem (2004).

Table 3: Calcium, magnesium (mg kg-1) of saline soil and plant dry weight (g pot-1) as influenced by different strains of cyanobacteria.

Alam, S.M., R. Ansari and M.A. Khan. 2000. Pakistan salt affected soil survey. Nuclear Institute of Agriculture Tando Jam, Pakistan. May 2000. Pp. 08 -21.

Apte, S.K. 1992. Molecular biology of cyanobacterial nitrogen fixation: recent advances. Indian J. Microbiol. 32(1):103–126.

Apte, S.K. and J. Thomas. 1997. Possible amelioration of coastal soil salinity using halo tolerant nitrogenfixing cyanobacteria. Plant Soil. 189:205–211. https://doi.org/10.1023/A:1004291830391

Ashraf, M. and A.H. Khan. 1994. Solute accumulation and growth of sorghum grown under NaCl and Na2SO4: Salinity stress. Sci. Int. 6:337-349.

Aziz, M.A. and M.A. Hashem. 2003. Role of cyanobacteria in improving fertility of saline soil. Pak. J. Biol. Sci. 6(4):1751–1752.

De, P.K. and M. Sulaiman. 1950. The influence of algal growth in the rice fields on the yield of crops. Indian J. Agric. Sci. 20:327–342.

Elayarajan, M. 2002. Land application of treated paper board mill effluent on soil- water-plant ecosystem (Soil Science). Coimbatore, TNAU, Ph.D. Thesis.

Hashem, M.A. 2001. Role of blue-green algal inoculum for improving soil fertility and reclaiming salinity of soil. Research report. BARC Dhaka, Bangladesh. Pp. 2.

Kannaiyan, S. And K. Pandiyarajan. 1992. The use of saline tolerance cyanobacteria for salt affected lands. In: Proceedings of the international symposium on strategies for utilizing salt affected lands. Bangkok, Thailand. Pp. 394–404.

Kaushik, B.D., and D. Subhashini. 1985. Amelioration of salt affected soil with blue green algae II, Improvement in soil properties. Proc. Indian Nat. Sci. Acad. B51: 386-389.

Keurson, G.W., J.A. Miernyk and K. Budd. 1984. Evidence for the occurrence of, and possible physiological role for, cyanobacterial calmodulin. Plant Physiol 75:222–224. https://doi.org/10.1104/pp.75.1.222

Lange, O.L., A. Meyer, H. Zellner and U. Heber. 1994. Photosynthesis and water relations of lichen soil-crusts: field measurements in the coastal fog zone of the Namib Desert. Funct. Ecol. 8:253–264. https://doi.org/10.2307/2389909

Matsuda. N., H. Kobayashi, H. Katoh, T. Ogawa, L. Futatsugi, T. Nakamura, P.E. Bakker and N. Uozumi. 2004. Na+-dependent K+ uptake Ktr system from the cyanobacterium Synechocystis sp. PCC 6803 and its role in the early phases of cell adaptation to hyperosmotic shock. J. Biol. Chem. 52:52–62.

McLean, E.O. 1982. Soil pH and lime requirement. In: Page, A.L., R.H. Miller and D.R. Keeney (eds.) Methods of soil analysis. Part 2: Chemical and micro-biological properties. (2nd Ed.). American Society of Agronomy. Pp. 199-223.

Metting, B. 1990. Microalgae applications in agriculture. Dev. Ind. Microbiol. 31:265–270.

Mujeeb-Kazi, A. and J.L. Diaz de Leon, 2002. Conventional and aliengenetic diversity for salt tolerance wheats: focus on current status and new germplasm development. Prospec. Saline Agric. 37: 69-82. https://doi.org/10.1007/978-94-017-0067-2_8

Nelson, D.W. and L.E. Sommers. 1996. Total carbon, organic carbon and matter. In: A.L. Page,R.H. Miller and D.R. Keeny ed. Methods of Soil Analysis Part II, 2nd edition. American Society of Agronomy. 9: 539-577.

Pandey, P.K., B.B. Singh, R. Mishra and P.S. Bisen. 1996. Calcium uptake and its regulation in the cyanobacterium Nostoc MAC. Curr. Microbial 32: 332-335.

Pendleton, R.L and S.D. Warren. 1995. Effects of cryptobiotic soil crusts and VA mycorrhizal inoculation on growth of five rangeland plant species. In: West, N.E. (ed), Proceedings of the fifth international rangeland congress. Society for Range Management, Salt Lake City, UT. pp. 436–437.

Prabu, P.C. and C. Udayasoorian. 2007. Native cyanobacteria Westiellopsis (TL-2) sp. For reclaiming paper mill effluent polluted saline sodic soil habitat of India. EJEAFChe. 6(2) 1775-1786.

Qadir, M., E. Quillerou, V. Nangia, G. Murtaza, M. Singh, R.J. Thomeas, P. Drechsel and A.D. Noble. 2014. Economics of salts-induced land degradation and restoration. Nat. Res. Forum. 4: 282-295.

Qayyum, B., M. Shahbaz and N.A. Akram. 2007. Interactive effect of foliar application of 24- Epibrassinolide and root zone salinity on morpho- physiological attributes of wheat (Triticum aestivum L.). Int. J. Agric. Biol. 9(4):584-589.

Qu, C., C. Lin, X. Gong, C. Li, M. Hong, L. Wang and F. Hong. 2012. Impairment of maize seedling photosynthesis caused by a combination of potassium deficiency and salt stress. Environ. Exp. Bot. 75:134-141. https://doi.org/10.1016/j.envexpbot.2011.08.019

Rai. V., N.K. Sharma and A.K. Rai. 2006. Growth and cellular ion content of a salt-sensitive symbiotic system Azolla pinnata- Anabaena azollae under NaCl stress. J. Plant Physiol. 937-944.12.

Reed, R.H and W.D.P. Stewart. 1985. Evidence for turgor sensitive K+ influx in cyanobacteria Anabaena variabilis ATCC 29413 and Synechocystis PCC 6714. Biochim. Biophys. Acta. 81(2):155–162. https://doi.org/10.1016/0005-2736(85)90533-4

Richard, L.A. 1954. Diagnosis and Improvement of Saline and Alkali Soil. USDA Agric. US Hand Book 60, Washington.

Rogers, S.L. and R.G. Burns. 1994. Changes in aggregate stability nutrient status, indigenous microbial populations, and seedling emergence following inoculation of soil with Nostoc muscorum. Biol. Fert. Soils. 18:209–215.

Rogers, S.L. and R.G. Burns. 1994. Changes in aggregate stability nutrient status, indigenous microbial populations, and seedling emergence following inoculation of soil with Nostoc muscorum. Biol.Fertile Soils. 18: 209-215. https://doi.org/10.1007/BF00647668

Roychoudhury, P. and B.D. Kaushik. 1989. Solubilization of mussorie rock phosphate by cyanobacteria. Curr. Sci. 58:569–570.

Roychoudhury, P., B.D. Kaushik and G.S. Venkataraman. 1985. Response of Tolypothrix ceylonica to sodium stress. Curr. Sci. 54:1181–1183.

Ryan, J., G. Estefan and R. Sommer. 2013.Soil and Laboratory Manual. 2nd Edition. Jointly published by the Internatinal Center for Agricultural Research in the Dry Areas (ICARDA) and the National Agricultural Research Center (NARC). Pp. 27-75.

Shahzad, M., K. Witzel, C. Zorb, and K.H. Muhling. 2012. Growth related in subcellular ion patterns in maize leaves (Zea mays L.) under salt stress. J. Agron. Crop Sci. 198: 46-56.

Shehata, F.H.A. and B.A. Whitton. 1982. Zinc tolerance in strains of blue-green alga Anacystis nidulans. Br. Phycol. 17: 5–12. https://doi.org/10.1080/00071618200650021

Singh, D.P. 1985. Cu+2 transport in the unicellular cyanobacterium Anacystis nidulans. J. Gen. Appl. Microbiol. 31:277–284. https://doi.org/10.2323/jgam.31.277

Singh, R.N. 1961. Reclamation of USAR lands. Role of Blue Green Algae in nitrogen Economy of Indian Agriculture New Delhi, Indian Council of Agricultural Research. Pp. 83-98.

Smith, R.J. and S. Hobson and I. Ellis. 1987. Evidence for calcium mediated regulation of heterocyst frequency and nitrogenase activity in Nostoc 6720. New Phytol. 105:531–541. https://doi.org/10.1111/j.1469-8137.1987.tb00891.x

Soltanpour, P.N. and A.P. Schawab. (ed). 1977. A new soil test for simultaneous extraction of macro and micronutrients in alkaline soils. Commun. Soil Sci. Plant Anal. 8: 195-207. https://doi.org/10.1080/00103627709366714

Steel, R.G.D. and J.H. Torrie. 1980. Principles and Procedures of Statistics: A biometrical approach. McGraw-Hill,New York, N. Y. 2nd edition. Pp.633.

Verma, K.S and I.P. Abrol. 1980. Effect of gypsum and pyrite on soil properties in a highly sodic soil. Indian J. Agric. Sci. 50:844–851.

Villa-Astoria, M., A.P. Ellery, E.A. Catalan-Valencia and M.D. Ramming. 2003. Salinity and nitrogen rates effects on the growth and yield of Chile pepper plant. Soil Sci. Soc. Am. J. 67:1781-90. https://doi.org/10.2136/sssaj2003.1781

Wafaa, M.T. Eletr, F.M. Ghazal, A.A. Mahmoud and G.H. Yossef. 2013. Responses of wheat–rice cropping system to cyanobacteria inoculation and different soil conditioners sources under saline soil. Nat. Sci. 11(10): 118-129.