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RESEARCH PAPER
Effect of encapsulated and free-living cells of Chlorella vulgaris L. on nitrogen retention in soils
Wojciech Kozieł 1
,
 
Katarzyna Jaromin-Gleń 1
,
 
Cezary Polakowski 1
,
 
Anna Walkiewicz 1
,
 
Piotr Bulak 1
 
 
 
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1
Institute of Agrophysics, Polish Academy of Sciences, Doświadczalna 4, 20-290 Lublin, Poland
 
 
Acceptance date: 2018-10-16
 
 
Publication date: 2019-02-14
 
 
Int. Agrophys. 2019, 33(1): 127-136
DOI: https://doi.org/10.31545/intagr/104415
 
 
Article (PDF)
References (64)
 
KEYWORDS
Alginate
sodium alginate
encapsulation
Chlorella vulgaris
nitrogen fertiliser application
soil
 
TOPICS
Soil Physicochemistry
 
ABSTRACT
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.
 
REFERENCES (64)
1.
Angelova N. and Hunkeler D., 1999. Rationalizing the design of polymeric biomaterials. Trends Biotechnol., 17(10), 409-421.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
5.
Becker E.W., 2008. Microalgae: biotechnology and microbiology. Cambridge University Press, https://trove.nla.gov.au/versi....
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
12.
Chisti Y., 2007. Biodiesel from microalgae. Biotechnol. Adv., 25(3), 294-306.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
17.
Draget K.I., Smidsrød O. and Skjåk-Bræk G., 2005. Alginates from algae. In: Biopolymers Online Biopolymers (Ed. A. Steinbüchel), https://onlinelibrary.wiley.co....
Google Scholar
 
 
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.
Google Scholar
 
 
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., https://www.ncbi.nlm.nih.gov/p....
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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., https://www.researchgate.net/p....
Google Scholar
 
 
24.
ENCAPSULATION_OF_PROBIOTIC_Lactobacillus_curvatus_G7_FROM_CHICKEN_CROP.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
27.
Jen A.C., Wake M.C., and Mikos A.G., 1996. Review: Hydrogels for cell immobilization. Biotechnol. Bioeng., 50(4), 357-364.
Google Scholar
 
 
28.
Jensen P.E. and Leister D., 2014. Chloroplast evolution, structure and functions. F1000prime Rep., 6, 40.
Google Scholar
 
 
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., https://www.frontiersin.org/ar....
Google Scholar
 
 
30.
Kizilel S., Garfinkel M., and Opara E., 2005. The bioartificial pancreas: progress and challenges. Diabetes Technol. Ther., 7(6), 968-985.
Google Scholar
 
 
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....
Google Scholar
 
 
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.
Google Scholar
 
 
33.
Lee C.S. and Chu I.M., 1997. Characterization of modified alginate-poly-L-lysine microcapsules. Artif. Organs, 21(9), 1002-1006.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
45.
Richmond A. (Ed.), 2007. Handbook of Microalgal Culture: Biotechnology and Applied Phycology. Blackwell Publishing Ltd., Carlton, Victora 3053, Australia.
Google Scholar
 
 
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.
Google Scholar
 
 
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., https://www.ncbi.nlm.nih.gov/p....
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
51.
Stępniewski W. and Stępniewska Z., 2009. Selected oxygen-dependent process. Response to soil management and tillage. Soil Till. Res., 102(2), 193-200.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
54.
Vemmer M. and Patel A.V., 2013. Review of encapsulation methods suitable for microbial biological control agents. Biol. Control, 67(3), 380-389.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
58.
WFT, 2015. World Fertilizer Trends and Outlook to 2018. Food and agriculture organization of the united nations (FAO) - Rome, 2015, https://agrilinks.org/library/....
Google Scholar
 
 
59.
Wheeler P. and Kokkinakis S.A., 1990. Ammonium recycling limits nitrate use in the oceanic subarctic Pacific. Limnol. Oceanogr., 35(6), 1267-1278.
Google Scholar
 
 
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), https://medcraveonline.com/JAM..., DOI: 10.15406/jamb.2017.06.00143.
CrossRef
 
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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.
Google Scholar
 
 
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