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Optimizing a cyanobacterial biofertilizer manufacturing system for village-level production in Ethiopia

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Abstract

A series of experiments in laboratory and hoop house environments was conducted to develop a cyanobacteria-based biological N fertilizer source that can be produced in Ethiopian villages, thus providing an alternative to expensive, imported urea. In the laboratory, factorial combinations of four Anabaena species strains (E-2, E-3, E-5, and E-9) isolated from Ethiopian soils and three water sources (river, lake, and ground water) were laid out in a complete randomized design in a light box constructed for this purpose with three replications. Factorial combinations of two pond-lining materials (transparent and black plastic sheets) and two aeration intervals (1-hour and 30-min intervals) were laid out in a complete randomized design with three replications in a hoop house using small ponds (1 m × 2 m × 0.25 m). Cyanobacteria strain E-3 performed best in the river water and was selected based on significantly higher values of optical density, growth rate, heterocyst frequency, and total Kjeldahl nitrogen than the other strains. DNA sequencing showed that clones of E-3 shared 99% similarity with Anabaena oscillariodes. Moreover, transparent plastic–lined ponds with a 1-hour aeration interval provided the best growing conditions for the E-3 strain based on its significantly higher dry biomass, optical density, and growth rate under these conditions as compared with ponds lined with black plastic or aerated in 30-min intervals. Therefore, transparent plastic–lined ponds with 1-hour aeration intervals are recommended for the mass production of A. osciolloides strain E-3 for use as a biofertilizer.

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References

  • Abuye F, Achamo B (2016) Potential use of cyanobacterial bio-fertilizer on growth of tomato yield components and nutritional quality on grown soils contrasting pH. J Biol Ag Healthcare 6:54–62

    Google Scholar 

  • Allakhverdiev S, Sakamoto A, Nishiyama Y, Inaba M, Murata N (2000) Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp. Plant Physiol 123:1047–1056

    CAS  PubMed  PubMed Central  Google Scholar 

  • Allen MB, Arnon DI (1955) Studies on nitrogen-fixing blue-green algae. I. Growth and nitrogen fixation by Anabaena cylindrica Lemm. Plant Physiol 30:366–372

    CAS  PubMed  PubMed Central  Google Scholar 

  • APHA (American Public Health Association) (2005). Standard methods for examination of water and wastewater. 21st Ed. Washington DC, USA

  • Asmamaw M, Wolde G, Yohannes M, Yigrem S, Woldemeskel E, Chala A, Davis JG (2019) Comparison of cyanobacterial bio-fertilizer with urea on three crops and two soils of Ethiopia. Afr J Ag Res 14:588–596

    CAS  Google Scholar 

  • Ben-Amatoz A, Avron M (1989) The biotechnology of mass culturing Dunaliella for products of commercial interest. In: Cresswell RC, Rees TAV, Shah N (eds) Algal and cyanobacterial biotechnology. Longman Scientific and Technical, Harlow, pp 90–114

    Google Scholar 

  • Bernhard M, Zattera A, Filesi P (1966) Suitability of various substances for use in the culture of marine organisms. J Mar Ecol 35:89–104

    Google Scholar 

  • Blankey WF (1973) Toxic and inhibitory materials associated with culturing. In: Stein J (ed) Handbook of phycological methods: culture methods and growth measurements. Cambridge University Press, Cambridge, pp 207–299

    Google Scholar 

  • Borowitzka AM (2005) Culturing microalgae in outdoor ponds. In: Andersen AR (ed) Algal culturing techniques. Elsevier, London, pp 205–218

    Google Scholar 

  • Briand JF, Leboulanger C, Humbert FJ (2004) Cylindrospermopsis raciborskii (cyanobacteria) invasion at mid-latitudes: selection, wide physiological tolerance, or global warming. J Phycol 40:231–238

    Google Scholar 

  • Chisti Y (2007) Biodiesel from microalgae. Adv Biotechnol 25:294–306

    CAS  Google Scholar 

  • Chittapun S, Limbipichai S, Amnuaysin N, Boonkerd R, Charoensook M (2018) Effects of using cyanobacteria and fertilizer on growth and yield of rice, Pathum Thani I: a pot experiment. J Appl Phycol 30:79–85

    Google Scholar 

  • Christopher P, Shantha PR, Nandagopal S (2009) Influence of coir pith based cyanobacterial basal and foliar biofertilizer on Hibiscus esculentus. Int J Appl Bioeng 4:132–167

    Google Scholar 

  • Czerny J, Ramos BE, Riebesell U (2009) Influence of elevated CO2 concentrations on cell division and nitrogen fixation rates in the bloom-forming cyanobacterium Nodularia spumigena. Biogeosci Discuss 6:4279–4304

    Google Scholar 

  • De Philippis R, Faraloni C, Margheri CM, Sili C, Herdman M, Vincenzini M (2000) Morphological and biochemical characterization of the exocellular investments of polysaccharide-producing Nostoc strains from the Pasteur Culture Collection. World J Microbiol 16:655–661

    Google Scholar 

  • Erwiha GM, Ham J, Sukor A, Wickham A, Davis JG (2020) Organic fertilizer source and application method impact ammonia volatilization. Commun Soil Sci Plant Anal 51:1469–1482

    CAS  Google Scholar 

  • Ethiopian Agricultural Transformation Agency (ATA) (2016) Soil fertility status and fertilizer recommendation atlas of the Southern, Nations, Nationalities and Peoples’ Regional State, Ethiopia. Addis Ababa, Ethiopia p76

  • Faheed FA, Abdel FZ (2008) Effect of Chlorella vulgaris as bio-fertilizer on growth parameters and metabolic aspects of lettuce plant. J Ag Social Sci 4:165–169

    Google Scholar 

  • Fassil K, Yamoah C (2009) Soil fertility status and numass fertilizer recommendation of typic hapluusterts in the northern highlands of Ethiopia. World Appl Sci J 6:1473–1480

    Google Scholar 

  • Fernandez A, Camacho FG, Perez AJ, Sevilla MG, Grima ME (1998) Modeling of biomass productivity in tubular photobioreactors for microalgal cultures: effects of dilution rate, tube diameter, and solar irradiance. Aust J Biotechnol 58:605–616

    CAS  Google Scholar 

  • Garcia J, Mujeriego R, Marine HM (2000) High rate algal pond operating strategies for urban wastewater nitrogen removal. J Appl Phycol 12:331–339

    CAS  Google Scholar 

  • Gokason T, Zekeriyaoglu Z, Ilknur KA (2007) The growth of Spirulina platensis in different culture systems under greenhouse condition. Turk J Biol 31:47–52

    Google Scholar 

  • Grant WD, Mwatha WE, Jones BE (1990) Alkaliphiles: ecology, diversity and applications. FEMS Microbiol Rev 6:255–269

    Google Scholar 

  • Grobbelaar JU (2009) From laboratory to commercial production: a case study of a Spirulina (Arthrospira) facility in Musina, South Africa. J Appl Phycol 21:523–527

    CAS  Google Scholar 

  • Havlin JL, Beaton JD, Tisdale SL, Nelson WL (2014) Soil fertility and fertilizers. Prentice Hall. Inc, New Jersely

    Google Scholar 

  • Hegazi AZ, Mostafa SS, Ahmed HM (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

    Google Scholar 

  • Hu Q, Richmond A (1996) Productivity and photosynthetic efficiency of Spirulina platensis affected by light intensity, cell density and rate of mixing in a flat plate photo-bioreactor. J Appl Phycol 8:139–145

    Google Scholar 

  • Huisman J, Sharples J, Stroom J, Visser MP, Kardinaal AEW, Verspagen HM (2004) Changes in turbulent mixing shift competition for light between phytoplankton species. Ecology 85:2960–2970

    Google Scholar 

  • Jagannath SB, Dengi U, Sedamakar E (2002) Algalization studies on chickpea (Cicer arietinum L). In: Rakak RC (ed) Biotechnology of microbes and sustainable utilization. Scientific Publishers, Jodhpur, India, pp 145–150

    Google Scholar 

  • Katsutoshi H, Shun’ichi I, Gakuro I (2002) Behavior of filamentous cyanobacterium Anabaena in water column and its cellular characteristics. J Biochem Eng Inst Technol 34:217–225

    Google Scholar 

  • Khosravi M, Ganji MT, Rakhshaee R (2005) Toxic effect of Pb, Cd, Ni and Zn on Azolla filiculoides in the international Anzali wetland. Int J Environ Sci Technol 2:35–40

    CAS  Google Scholar 

  • Kranz SA, Levitan O, Richter KU, Prášil O, Berman-Frank I, Rost B (2010) Combined effects of CO2 and light on the N2-fixing cyanobacterium Trichodesmium IMS101: physiological responses. Plant Physiol 154:334–345

    CAS  PubMed  PubMed Central  Google Scholar 

  • Krishna MS, Subramaniyan V, Malliga P (2012) Effect of coir pith cyanobacterial biofertilizer on morphological and yield characters of Aloe barbadensis in pot experiment. J Algal Biomass Utiliz 3:33–41

    Google Scholar 

  • Lehtimaki J, Moisander P, Sivonen K, Kononen K (1997) Growth, nitrogen fixation, and nodularin production by two Baltic Sea cyanobacteria. Appl Environ Microbiol 63:1647–1656

    CAS  PubMed  PubMed Central  Google Scholar 

  • Levitan O, Kranz SA, Spungin D, Prášil O, Rost B, Berman-Frank I (2010) Combined effects of CO2 and light on the N2-fixing cyanobacterium Trichodesmium IMS101: a mechanistic view. Plant Physiol 154:346–356

    CAS  PubMed  PubMed Central  Google Scholar 

  • Maberly SC (1996) Daily episodic and seasonal changes in pH and concentrations of inorganic carbon in a productive lake. Freshw Biol 35:579–598

    CAS  Google Scholar 

  • Mahmoud A, Mostafa S, Abd El-Al M, Azza MA, Hegazi ZA (2007) Effect of cyanobacterial inoculation in presence of organic and inorganic amendments on carrot yield and sandy soil properties under drip irrigation regime. Egypt Sci Appl Sci 22:716–733

    Google Scholar 

  • Mahmoud HAF, Amara MAT (2000) Response of tomato to biological and mineral fertilizers under calcareous soil conditions. Bulletin Faculty of Agriculture, University of Cairo 51:151–174

  • Malik KA, Mirza SM, Hassan U, Mehnaz S, Rasul G, Haurat J, Bally R, Normand P (2002) The role of plant-associated beneficial bacteria in rice-wheat cropping system. In: Kennedy IR, Choudhury ATMA (eds) Biofertilisers in action. RIRDC, Canberra, pp 73–83

    Google Scholar 

  • Marino R, Chan F, Howarth RW, Pace M, Likens GE (2002) Ecological and biogeochemical interactions constrain planktonic nitrogen fixation in estuaries. Ecosystems 5:719–725

    CAS  Google Scholar 

  • McGinn PJ, Price GD, Maleszka R, Badger MR (2003) Inorganic carbon limitation and light control the expression of transcripts related to the CO2-concentrating mechanism in the cyanobacterium Synechocystis sp. strain PCC6803. Plant Physiol 132:218–229

    CAS  PubMed  PubMed Central  Google Scholar 

  • Menamo M, Wolde Z (2013) Effect of cyanobacteria application as biofertilizer on growth, yield and yield components of Romaine lettuce (Lactuca sativa L.) on soils of Ethiopia. Am Sci Res J Eng Technol Sci 4:50–58

    Google Scholar 

  • Morin N, Vallaeys T, Hendrickx L, Natalie L, Wilmotte A (2010) An efficient DNA isolation protocol for filamentous cyanobacteria of the genus Arthrospira. J Microbiol Methods 80:148–154

    CAS  PubMed  Google Scholar 

  • NMA (National Meteorological Agency) (2012) National meteorological agency. Hawassa Branch Directorate, Southern Nations, Nationalities and Peoples Region, Ethiopia

    Google Scholar 

  • Nubel U, Garcia-Pichel F, Muyzer G (1997) PCR primers to amplify 16S rRNA genes from cyanobacteria. Appl Environ Microbiol 63:3327–3332

    CAS  PubMed  PubMed Central  Google Scholar 

  • Park JBK, Craggs JR (2010) Wastewater treatment and algal production in high rate algal ponds with CO2 addition. Water Sci Technol 61:633–639

    CAS  PubMed  Google Scholar 

  • Park BK, Craggs JR, Shilton NA (2011) Wastewater treatment high rate algal ponds for biofuel production. Bioresour Technol 102:35–42

    CAS  PubMed  Google Scholar 

  • Pisciotta JM, Zou Y, Baskakov IV (2010) Light-dependent electrogenic activity of cyanobacteria. J Plant Soil Sci 5:10–21

    Google Scholar 

  • Price GD, Sültemeyer BK, Ludwig M, Badger RM (1998) The functioning of the CO2 concentrating mechanism in several cyanobacterial strains: a review of general physiological characteristics, genes, proteins, and recent advances. Can J Bot 76:973–1002

  • Qiu B, Gao K (2002) Effects of CO2 enrichment on the bloom forming cyanobacterium Microcystis aeruginosa: physiological responses and relationships with the availability of dissolved inorganic carbon. J Phycol 38:721–729

    CAS  Google Scholar 

  • Richmond A (ed) (1987) Handbook of algal mass culture. CRC Press, Boca Raton

    Google Scholar 

  • Rippka R, Deruelles J, Waterbury BJ, Herdman M, Stainer YR (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61

    Google Scholar 

  • Ronda SR, Bokka SC, Ketineni C, Rijal B, Allu RP (2012) Aeration effect on Spirulina platensis growth and gamma-linolenic acid production. Braz J Microbiol 15:12–20

    Google Scholar 

  • Sahu JK (2000) Growth and nitrogen fixation of cyanobacteria from rice fields of Puri district Orissa. Adv Plant Sci 13:47–50

    Google Scholar 

  • Shapiro J (1990) Current beliefs regarding dominance by blue-greens: the case for the importance of CO2 and pH. Int Verein Theor Angew Limnol Verhandl 24:38–54

    Google Scholar 

  • Singh M, Pandey PJ, Tiwari A, Chauhan UK (2011) Impact of graded concentration of NaCl on the growth and heterocyst frequency of parent and mutant strain of Anabaena variabilis RDU-1. utilization. Algal Biomass Utiliz 2:17–23

    CAS  Google Scholar 

  • Smaling EMA, Nandwa MS, Janssen HB (1997) Soil fertility in Africa is at stake. In: Buresh RJ, Sanchez PA, Calhoun F (eds) Replenishing soil fertility in Africa. SSSA Spec. Publ 51. Soil Science Society of America, Madison, pp 47–61

    Google Scholar 

  • Tang EP, Tremblay R, Vincent FW (1997) Cyanobacterial dominance of polar freshwater ecosystems: is high-latitude mat-formers adapted to low temperature. J Phycol 33:171–181

    Google Scholar 

  • Teresa M, Mata AA, Martins AA, Caetano SN (2010) Microalgae for biodiesel production and other applications. Renew Sust Energy Rev J 14:217–232

    Google Scholar 

  • Terry KL, Raymond LP (1985) System design for the autotrophic production of microalgae. Enzym Microb Technol 7:474–487

    Google Scholar 

  • Thamizh SK, Sivakumar K (2012) Effect of cyanobacteria on growth and yield parameters in Oryza sativa, variety (ADT 38). Int J Dev Res 2:1008–1011

    Google Scholar 

  • Toonsiri P, Del Grosso SJ, Sukor A, Davis JG (2016) Greenhouse gas emissions from solid and liquid organic fertilizers applied to lettuce. J Environ Qual 45:1812–1821

    CAS  PubMed  Google Scholar 

  • Tripathi U, Sarada R, Ravishankar AG (2001) A culture method for microalgal forms using two-tier vessel providing carbon-dioxide environment: studies on growth and carotenoids production. J Microbiol Biotechnol 17:325–329

    CAS  Google Scholar 

  • Tsedeke A, Degefu T, Wolde-meskel E, Davis J (2016) The effect of pond depth and lining plastic color on nitrogen fixing capacity of the cyanobacteria, Anabaena sp. E3. Afr J Biotechnol 15:1442–1451

    CAS  Google Scholar 

  • Van Dok W, Hart TB (1996) Akinete differentiation in Anabaena circinalis. J Phycol 32:557–565

    Google Scholar 

  • Wang Q, Ding Y, Shen Y, Jin C, Lu J, Zhu J, Li S (1991) Studies on mixed mass cultivation of Anabaena spp. (nitrogen-fixing blue-green algae, cyanobacteria) on a large scale. Bioresour Technol 38:221–228

    CAS  Google Scholar 

  • Wen X, Gong H, Lu C (2005) Heat stress induces an inhibition of excitation energy transfer from phycobilisomes to photosystem II but not to photosystem I in a cyanobacterium Spirulina platensis. Plant Physiol Biochem 43:389–395

    CAS  PubMed  Google Scholar 

  • Wenz J, Davis JG, Storteboom H (2019) Influence of light on endogenous phytohormone concentrations of a nitrogen-fixing Anabaena sp. cyanobacterium culture in open raceways for use as fertilizer for horticultural crops. J Appl Phycol 31:3371–3384

    CAS  Google Scholar 

  • West JA (2005) Long term macroalgal culture maintenance. In: Andersen AR (ed) Algal culturing techniques, Academic Press, New York, pp 157–163

    Google Scholar 

  • Wood AM, Everroad RC, Wingard LM (2005) Measuring growth rates in microalgal cultures. In Andersen AR (ed) Algal Culturing Techniques,1st ed. Academic Press, New York, USA, 269-288.

  • Yamamoto Y, Nakahara H (2005) Competitive dominance of the cyanobacterium Microcystis aeruginosa in nutrient-rich culture conditions with special reference to dissolved inorganic carbon uptake. Phycol Res 53:201–208

    Google Scholar 

  • Yoder N, Davis JG (2020) Organic fertilizer comparison on growth and nutrient content of three kale cultivars. HortTechnol 30:176–184

    CAS  Google Scholar 

  • Young EB, Tucker CR, Pansch AL (2010) Alkaline phosphatase in freshwater Cladophora-epiphyte assemblages: regulation in response to phosphorus supply and localization. J Phycol 46:93–101

    CAS  Google Scholar 

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Funding

This study was funded by the National Collegiate Inventors and Innovators Alliance.

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Authors and Affiliations

  1. Department of Plant Science, College of Agriculture and Natural Resource, Wolkite University, Wolkite, Ethiopia

    G. Wolde

  2. Department of Horticulture, Samara University, Samara, Ethiopia

    M. Asmamaw

  3. School of Plant and Horticultural Science, College of Agriculture, Hawassa University, Hawassa, Ethiopia

    M. Y. Sido & A. Chala

  4. College of Agricultural Sciences, Arba Minch University, Arba Minch, Ethiopia

    S. Yigrem

  5. World Agroforestry (ICRAF), Addis Ababa, Ethiopia

    E. Wolde-meskel

  6. Department of Soil and Crop Sciences, Colorado State University, Fort Collins, CO, 80523-1170, USA

    H. Storteboom

  7. Department of Horticulture and Landscape Architecture, Colorado State University, Fort Collins, CO, 80523-1173, USA

    J. G. Davis

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  1. G. Wolde
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  3. M. Y. Sido
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  8. J. G. Davis
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Wolde, G., Asmamaw, M., Sido, M.Y. et al. Optimizing a cyanobacterial biofertilizer manufacturing system for village-level production in Ethiopia. J Appl Phycol 32, 3983–3994 (2020). https://doi.org/10.1007/s10811-020-02221-1

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