Effect of encapsulated and free-living cells of Chlorella vulgaris L. on nitrogen retention in soils
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Institute of Agrophysics, Polish Academy of Sciences, Doświadczalna 4, 20-290 Lublin, Poland
Publish date: 2019-02-14
Acceptance date: 2018-10-16
Int. Agrophys. 2019, 33(1): 127–136
We hypothesised that the addition of free-living and alginate-encapsulated algae Chlorella vulgaris to the soil would change the availability of soluble forms of nitrogen, increasing the retention of nitrates, which is especially important due to fertilisers misuse and nitrogen leaching. C. vulgaris were grown on Knop and Baslerowa-Dvorakova media. The best growth was observed on Knop medium in 25ºC. Three different soils (Brunic Arenosol, Haplic Umbrisol, Mollic Umbrisol) were tested in both flooded conditions and conditions corresponding to field water capacity. Capsules prepared with 1.0-2.5% sodium alginate and 0.5-5% CaCl2 kept shape and consistency, but at a different level of durability. From nine different concentrations of alginate used to form the capsules, 1% proved to be the most suitable. In contrast to encapsulated C. vulgaris, the addition of free-living algae had a positive effect on the reduction of NO3- in non-flooded soils, which can be beneficial in terms of reducing N leaching. Encapsulated microalgae seemed to have assimilated NH4+ under flooded conditions, but this effect was generally blurred by alginate capsule sorption/ adsorption. In two sandy and one silty soil, encapsulated algae were rather ineffective, and their impact was limited to a minor reduction of NO3- and NH4+ content under flooded conditions.
1. Angelova N. and Hunkeler D., 1999. Rationalizing the design of polymeric biomaterials. Trends Biotechnol., 17(10), 409-421.
2. Bai J., Wang X., Jia J., Zhang G., Wang Y., and Zhang S., 2017. Denitrification of soil nitrogen in coastal and inland salt marshes with different flooding frequencies. Phys. Chem. Earth Parts, ABC, 97, 31-36.
3. Balk M., Laverman A.M., Keuskamp J.A., and Laanbroek H.J., 2015. Nitrate ammonification in mangrove soils: a hidden source of nitrite? Front. Microbiol., 6, 166.
4. Banerjee A., Nayak D., and Lahiri S., 2007. A new method of synthesis of iron doped calcium alginate beads and determination of iron content by radiometric method. Biochem. Eng. J., 33(3), 260-262.
5. Becker E.W., 2008. Microalgae: biotechnology and microbiology. Cambridge University Press,
6. Bieganowski A., Witkowska-Walczak B., Gliński J., Sokołowska Z., Sławiński C., Brzezińska M., and Włodarczyk T., 2013. Database of Polish arable mineral soils: a review. Int. Agrophysics, 27(3), 335-350.
7. Blandino A., Macías M., and Cantero D., 1999. Formation of calcium alginate gel capsules: influence of sodium alginate and CaCl2 concentration on gelation kinetics. J. Biosci. Bioeng., 88(6), 686-689.
8. Brodie J., Chan C.X., De Clerck O., Cock J.M., Coelho S.M., Gachon C., Grossman A.R., Mock T., Raven J.A., Smith A.G., Yoon H.S., and Bhattacharya D., 2017. The Algal Revolution. Trends Plant Sci., 22(8), 726-738.
9. Chandy T., Mooradian D.L., and Rao G.H., 1999. Evaluation of modified alginate-chitosan-polyethylene glycol microcapsules for cell encapsulation. Artif. Organs, 23(10), 894-903.
10. Chia M.A., Lombardi A.T., da Graça Gama Melão M., and Parrish C.C., 2015. Combined nitrogen limitation and cadmium stress stimulate total carbohydrates, lipids, protein and amino acid accumulation in Chlorella vulgaris (Trebouxiophyceae). Aquat. Toxicol. Amst. Neth., 160, 87-95.
11. Chia M.A., Lombardi A.T., and Melão M. da G.G., 2013. Growth and biochemical composition of Chlorella vulgaris in different growth media. An. Acad. Bras. Cienc., 85(4), 1427-1438.
12. Chisti Y., 2007. Biodiesel from microalgae. Biotechnol. Adv., 25(3), 294-306.
13. Covarrubias S.A., de-Bashan L.E., Moreno M., and Bashan Y., 2012. Alginate beads provide a beneficial physical barrier against native microorganisms in wastewater treated with immobilized bacteria and microalgae. Appl. Microbiol. Biotechnol., 93(6), 2669-2680.
14. Daemi H. and Barikani M., 2012. Synthesis and characterization of calcium alginate nanoparticles, sodium homopolymannuronate salt and its calcium nanoparticles. Sci. Iran., 19(6), 2023-2028.
15. Davarcı F., Turan D., Ozcelik B., and Poncelet D., 2017. The influence of solution viscosities and surface tension on calcium-alginate microbead formation using dripping technique. Food Hydrocoll., 62, 119-127.
16. Di H.J. and Cameron K.C., 2002. Nitrate leaching in temperate agroecosystems: sources, factors and mitigating strategies. Nutr. Cycl. Agroecosystems, 64(3), 237-256.
17. Draget K.I., Smidsrød O. and Skjåk-Bræk G., 2005. Alginates from algae. In: Biopolymers Online Biopolymers (Ed. A. Steinbüchel),
18. Dusseault J., Leblond F.A., Robitaille R., Jourdan G., Tessier J., Ménard M., Henley N., and Hallé J.-P., 2005. Microencapsulation of living cells in semi-permeable membranes with covalently cross-linked layers. Biomaterials, 26(13), 1515-1522.
19. Giles M., Morley N., Baggs E.M., and Daniell T.J., 2012. Soil nitrate reducing processes – drivers, mechanisms for spatial variation, and significance for nitrous oxide production. Front. Microbiol.,
20. Glibert P.M., Wilkerson F.P., Dugdale R.C., Raven J.A., Dupont, Leavitt P.R., Parker A.E., Burkholder J.M., and Kana T.M., 2015. Pluses and minuses of ammonium and nitrate uptake and assimilation by phytoplankton and implications for productivity and community composition, with emphasis on nitrogen-enriched conditions. Limnol. Oceanogr., 61(1), 165-197.
21. Goh C.H., Heng P.W.S., and Chan L.W., 2012. Alginates as a useful natural polymer for microencapsulation and therapeutic applications. Carbohydr. Polym., 88(1), 1-12.
22. Griffiths M.J., van Hille R.P., and Harrison S.T.L., 2014. The effect of nitrogen limitation on lipid productivity and cell composition in Chlorella vulgaris. Appl. Microbiol. Biotechnol., 98(5), 2345-2356.
23. Houria O., Tayeb I., Mohamed S., Messaouda G., and Messaouda B., 2012. Isolation, characterization and microencapsulation of probiotic Lactobacillus curvatus g7 from chicken crop. TOJSAT Online J. Sci. Technol.,
25. Hsieh C.-H. and Wu W.-T., 2009. Cultivation of microalgae for oil production with a cultivation strategy of urea limitation. Bioresour. Technol., 100(17), 3921-3926.
26. Ikaran Z., Suárez-Alvarez S., Urreta I., and Castañón S., 2015. The effect of nitrogen limitation on the physiology and metabolism of Chlorella vulgaris var L3. Algal Res., 10, 134-144.
27. Jen A.C., Wake M.C., and Mikos A.G., 1996. Review: Hydrogels for cell immobilization. Biotechnol. Bioeng., 50(4), 357-364.
28. Jensen P.E. and Leister D., 2014. Chloroplast evolution, structure and functions. F1000prime Rep., 6, 40.
29. Juárez P., Alberto G., Spasojevic M., Faas M.M., and de Vos P., 2014. Immunological and technical considerations in application of alginate-based microencapsulation systems. Front. Bioeng. Biotechnol.,
30. Kizilel S., Garfinkel M., and Opara E., 2005. The bioartificial pancreas: progress and challenges. Diabetes Technol. Ther., 7(6), 968-985.
31. Kwietniewska E., Tys J., Krzemińska I., and Kozieł W., 2012. Microalgae – cultivation and application of biomass as a source of energy: a review. Acta Agrophysica Monographiae, 124, 1-108, http://www.acta-agrophysica-mo....
32. Lamorski K., Bieganowski A., Ryżak M., Sochan A., Sławiński C., and Stelmach W., 2014. Assessment of the usefulness of particle size distribution measured by laser diffraction for soil water retention modelling. J. Plant Nutr. Soil Sci., 177(5), 803-813.
33. Lee C.S. and Chu I.M., 1997. Characterization of modified alginate-poly-L-lysine microcapsules. Artif. Organs, 21(9), 1002-1006.
34. Leick S., Henning S., Degen P., Suter D., and Rehage H., 2010. Deformation of liquid-filled calcium alginate capsules in a spinning drop apparatus. Phys. Chem. Chem. Phys. PCCP, 12(12), 2950-2958.
35. L’Helguen S., Maguer J.-F., and Caradec J., 2008. Inhibition kinetics of nitrate uptake by ammonium in size-fractionated oceanic phytoplankton communities: implications for new production and f-ratio estimates. J. Plankton Res., 30(10), 1179-1188.
36. Li T., Xu J., Gao B., Xiang W., Li A., and Zhang C., 2016. Morphology, growth, biochemical composition and photosynthetic performance of Chlorella vulgaris (Trebouxiophyceae) under low and high nitrogen supplies. Algal Res., 16, 481-491.
37. Liu N., Li F., Ge F., Tao N., Zhou Q., and Wong M., 2015. Mechanisms of ammonium assimilation by Chlorella vulgaris F1068: Isotope fractionation and proteomic approaches. Bioresour. Technol., 190, 307-314.
38. Machefert S.E., Dise N.B., Goulding K.W.T., and Whitehead P.G., 2002. Nitrous oxide emission from a range of land uses across Europe. Hydrol. Earth Syst. Sci. Discuss., 6(3), 325-338.
39. Mirón A.S., Garcı́a M.C.C., Gómez A.C., Camacho F.G., Grima E.M., and Chisti Y., 2003. Shear stress tolerance and biochemical characterization of Phaeodactylum tricornutum in quasi steady-state continuous culture in outdoor photobioreactors. Biochem. Eng. J., 16(3), 287-297.
40. Naga Pavan Kumar B., Kondal Reddy K., and Mallikarjuna P.V., 2012. Characterisation of blended sodium alginate microcapsules for controlled release of animal feed supplements in the GIT. Int. J. Food Agric. Vet. Sci., 2(2), 161-166.
41. Orive G., Hernández R.M., Rodríguez Gascón A., Calafiore R., Chang T.M.S., de Vos P., Hortelano G., Hunkeler D., Lacík I., and Pedraz J.L., 2004. History, challenges and perspectives of cell microencapsulation. Trends Biotechnol., 22(2), 87-92.
42. Perez-Garcia O., Escalante F.M.E., de-Bashan L.E., and Bashan Y., 2011. Heterotrophic cultures of microalgae: Metabolism and potential products. Water Res., 45(1), 11-36.
43. Rachlin J.W. and Grosso A., 1991. The effects of pH on the growth of Chlorella vulgaris and its interactions with cadmium toxicity. Arch. Environ. Contam. Toxicol., 20(4), 505-508.
44. Ribeiro H., de Sousa T., Santos J.P., Sousa A.G.G., Teixeira C., Monteiro M.R., Salgado P., Mucha A.P., Almeida C.M.R., Torgo L., and Magalhães C., 2018. Potential of dissimilatory nitrate reduction pathways in polycyclic aromatic hydrocarbon degradation. Chemosphere, 199, 54-67.
45. Richmond A. (Ed.), 2007. Handbook of Microalgal Culture: Biotechnology and Applied Phycology. Blackwell Publishing Ltd., Carlton, Victora 3053, Australia.
46. Ryan C., Green T.B., Hartley A., Green T.B., Browning B., Green T.B., Garvin C., and Green T.B., 2009. Cultivation Clean Energy: The Promise of Algae Biofuels.
47. Sanz-Luque E., Chamizo-Ampudia A., Llamas A., Galvan A., and Fernandez E., 2015. Understanding nitrate assimilation and its regulation in microalgae. Front. Plant Sci.,
48. Schoebitz M., López M.D., and Roldán A., 2013. Bioencapsulation of microbial inoculants for better soil-plant fertilization. A review. Agron. Sustain. Dev., 33(4), 751-765.
49. Scragg A.H., Illman A.M., Carden A., and Shales S.W., 2002. Growth of microalgae with increased calorific values in a tubular bioreactor. Biomass Bioenergy, 23(1), 67-73.
50. Soto M.J., Retamales J., Palza H., and Bastías R., 2018. Encapsulation of specific Salmonella enteritidis phage f3αSE on alginate-spheres as a method for protection and dosification. Electron. J. Biotechnol., 31, 57-60.
51. Stępniewski W. and Stępniewska Z., 2009. Selected oxygen-dependent process. Response to soil management and tillage. Soil Till. Res., 102(2), 193-200.
52. Temprano F.J., Albareda M., Camacho M., Daza A., Santamaría C., and Rodríguez-Navarro D.N., 2002. Survival of several Rhizobium/Bradyrhizobium strains on different inoculant formulations and inoculated seeds. Int. Microbiol. Off. J. Span. Soc. Microbiol., 5(2), 81-86.
53. Thu B., Bruheim P., Espevik T., Smidsrød O., Soon-Shiong P., and Skjåk-Braek G., 1996. Alginate polycation microcapsules. I. Interaction between alginate and polycation. Biomaterials, 17(10), 1031-1040.
54. Vemmer M. and Patel A.V., 2013. Review of encapsulation methods suitable for microbial biological control agents. Biol. Control, 67(3), 380-389.
55. Vernimmen R.R.E., Verhoef H.A., Verstraten J.M., Bruijnzeel L.A., Klomp N.S., Zoomer H.R., and Wartenbergh P.E., 2007. Nitrogen mineralization, nitrification and denitrification potential in contrasting lowland rain forest types in Central Kalimantan, Indonesia. Soil Biol. Biochem., 39(12), 2992-3003.
56. Wan J., Gordon J.B., Muirhead K., Hickey M.W., and Coventry M.J., 1997. Incorporation of nisin in micro-particles of calcium alginate. Lett. Appl. Microbiol., 24(3), 153-158.
57. Wang C., Li H., Wang Q., and Wei P., 2010. Effect of pH on growth and lipid content of Chlorella vulgaris cultured in biogas slurry. Sheng Wu Gong Cheng Xue Bao Chin. J. Biotechnol., 26(8), 1074-1079.
58. WFT, 2015. World Fertilizer Trends and Outlook to 2018. Food and agriculture organization of the united nations (FAO) - Rome, 2015,
59. Wheeler P. and Kokkinakis S.A., 1990. Ammonium recycling limits nitrate use in the oceanic subarctic Pacific. Limnol. Oceanogr., 35(6), 1267-1278.
60. Wong Y., Ho Y.H., Ho K., Leung H., and Yung K., 2017. Growth Medium Screening for Chlorella vulgaris Growth and Lipid Production. J. Aquac. Mar. Biol., 6(1),, DOI: 10.15406/jamb.2017.06.00143.
61. Yamagiwa K., Shimizu Y., Kozawa T., Onodera M., and Ohkawa A., 1992. Formation of Calcium-Alginate Gel Coating on Biocatalyst Immobilization Carrier. J. Chem. Eng. Jpn., 25(6), 723-728.
62. Yoo I.-K., Seong G.H., Chang H.N., and Park J.K., 1996. Encapsulation of Lactobacillus casei cells in liquid-core alginate capsules for lactic acid production. Enzyme Microb. Technol., 19(6), 428-433.
63. Young C.-C., Rekha P.D., Lai W.-A., and Arun A.B., 2006. Encapsulation of plant growth-promoting bacteria in alginate beads enriched with humic acid. Biotechnol. Bioeng., 95(1), 76-83.
64. Zhu S., Huang W., Xu J., Wang Z., Xu J., and Yuan Z., 2014. Metabolic changes of starch and lipid triggered by nitrogen starvation in the microalga Chlorella zofingiensis. Bioresour. Technol., 152, 292-298.