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Review Article

Ammonium photo-production by heterocytous cyanobacteria: potentials and constraints

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Pages 607-618 | Received 18 Sep 2013, Accepted 04 Dec 2014, Published online: 23 Jan 2015

References

  • Abdel Hameed SM, Hammouda EO. (2007). Biotechnological potential uses of immobilized algae. Int J Agri Biol, 9, 183–92
  • Atkinson B, Mavituna F. (1983). Biochemical engineering and biotechnology handbook. New York: Stockton Press
  • Badger MR, Price GD. (2003). CO2 concentrating mechanisms in cyanobacteria: molecular components, their diversity and evolution. J Exp Bot, 54, 609–22
  • Baker JA, Entsch B, McKay D. (2003). The cyanobiont in an Azolla fern is neither Anabaena nor Nostoc. FEMS Microbiol Lett, 229, 143–7
  • Bauersachs T, Compaore J, Hopmans EC, et al. (2009). Distribution of heterocyst glycolipids in cyanobacteria. Phytochem, 70, 2034–9
  • Bauersachs T, Stal LJ, Grego M, Schwark L. (2014). Temperature induced changes in the heterocyst glycolipid composition of N2 fixing heterocystous cyanobacteria. Organ Geochem, 69, 98–105
  • Berberoglu H, Pilon L. (2007). Experimental measurements of the radiation characteristics of Anabaena variabilis ATCC 29413-U and Rhodobacter sphaeroides ATCC 49419. Intern J Hydrogen Energy, 32, 4772–85
  • Berman-Frank I, Chen Y-B, Gao Y, et al. (2008). Feedbacks between the nitrogen, carbon and oxygen cycles. In: Capone DG, Bronk DA, Mulholland MR, et al. eds. Nitrogen in the marine environment. New York: Academic Press, 1512–37
  • Berman-Frank I, Lundgren P, Falkowski P. (2003). Nitrogen fixation and photosynthetic oxygen evolution in cyanobacteria. Res Microbiol, 154, 157–64
  • Bezdicek DF, Kennedy AC. (1988). Symbiotic nitrogen fixation and nitrogen cycling in terrestrial environments. In: Lynch JM, Hubbie JE, eds., Micro-organisms in action: concepts and applications in microbial ecology. Oxford: Blackwell, 241–60
  • Bothe H, Schmitz O, Yates MG, Newton WE. (2010). Nitrogen fixation and hydrogen metabolism in cyanobacteria. Microbiol Mol Biol Rev, 74, 529–51
  • Boussiba S. (1988). N2-fixing cyanobacteria as nitrogen biofertilizer – a study with the isolate Anabaena azollae. Symbiosis, 6, 129–38
  • Boussiba S. (1991). Nitrogen fixing cyanobacteria potential uses. Plant Soil, 137, 177–80
  • Brouers M, Hall D. (1986). Ammonia and hydrogen production by immobilized cyanobacteria. J Biotechnol, 3, 307–21
  • Bui LA, Dupré C, Legrand J, Grizeau D. (2014). Isolation, improvement and characterization of an ammonium excreting mutant strain of the heterocytous cyanobacterium, Anabaena variabilis PCC 7937. Biochem Eng J, 90, 279–85
  • Charyulu PBBN, Ramakrishna C, Rao VR. (1980). Effect of 2-amino-benzimidazole on nitrogen fixers in flooded soil and their nitrogenase. Bull Environ Contam Toxicol, 25, 482–7
  • Chauhan VS, Singh B, Singh S, et al. (2000). Isolation and characterization of the thylakoid membranes from the NaCl-resistant (NaClr) mutant strain of the cyanobacterium Anabaena variabilis. Curr Microbiol, 41, 321–7
  • Chaurasia AK, Apte SK. (2011). Improved eco-friendly recombinant Anabaena sp. strain PCC7120 with enhanced nitrogen biofertilizer potential. Appl Environ Microbiol, 77, 395–9
  • Chen YB, Zehr JP, Mellon M. (1996). Growth and nitrogen fixation of the diazotrophic filamentous non-heterocytous cyanobacterium Trichodesmium sp. IMS 101 in defined media: evidence for a circadian rhythm. J Phycol, 32, 916–23
  • Chisti Y. (2008). Biodiesel from microalgae beats bioethanol. Trends Biotechnol, 26, 126–31
  • Compaore J, Stal LJ. (2010). Effect of temperature on the sensitivity of nitrogenase to oxygen in two heterocystous cyanobacteria. J Phycol, 46, 1172–9
  • Danso SKA. (1995). Assessment of biological nitrogen fixation. Fertil Res, 42, 33–41
  • Dasgupta CN, Jose Gilbert J, Lindblad P, et al. (2010). Recent trends on the development of photobiological processes and photobioreactors for the improvement of hydrogen production. Int J Hydrogen Energy, 35, 10218–38
  • Davis R, Aden A, Pienkos PT. (2011). Techno-economic analysis of autotrophic microalgae for fuel production. Appl Energy, 88, 3524–31
  • Dwivedi M, Rai LC. (1990). Factor influencing photoproduction of ammonia from dinitrogen by Nostoc muscorum. Folia Microbiol, 35, 227–35
  • Elmerich C. (2007). Historical perspective: from bacterization to endophytes. In: Elmerich C, Newton WE, eds. Associative and endophytic nitrogen-fixing bacteria and cyanobacterial associations. Berlin; Springer, 1–20
  • Espinosa J, Forchhammer K, Burillo S, Contreras A. (2006). Interaction network in cyanobacterial nitrogen regulation: PipX, a protein that interacts in a 2-oxoglutarate dependent manner with PII and NtcA. Mol Microbiol, 61, 457–69
  • Fay P. (1992). Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol Rev, 56, 340–73
  • Fontes AG, Vargas MA, Moreno J, et al. (1987). Factors affecting the production of biomass by a nitrogen-fixing blue-green alga in outdoor culture. Biomass, 13, 33–43
  • Franche C, Lindström K, Elmerich C. (2009). Nitrogen-fixing bacteria associated with leguminous and non-leguminous plants. Plant Soil, 321, 35–59
  • Gallon JR. (1992). Tansley review no. 44. Reconciling the incompatible: N2 fixation and O2. New Phytol, 122, 571–609
  • Goebel NL, Turk KA, Achilles KM, et al. (2010). Abundance and distribution of major groups of diazotrophic cyanobacteria and their potential contribution to N2 fixation in the tropical Atlantic Ocean. Environ Microbiol, 12, 3272–89
  • González López CV, Acién Fernández FG, Fernández Sevilla JM, et al. (2009). Utilization of the cyanobacteria Anabaena sp. ATCC 33047 in CO2 removal processes. Bioresour Technol, 100, 5904–10
  • Hadj-Romdhane P, Zheng X, Jaouen P, et al. (2013). The culture of Chlorella vulgaris in a recycled supernatant: effects on biomass production and medium quality. Bioresour Technol, 132, 285–92
  • Haselkorn R. (2007). Heterocyst differentiation and nitrogen fixation in cyanobacteria. In: Elmerich C, Newton WE, eds. Associative and endophytic nitrogen-fixing bacteria and cyanobacteria associations. Springer, Dordrecht: the Netherlands, 233–55
  • Herrero A, Muro-Pastor AM, Flores E. (2001). Nitrogen control in cyanobacteria. J Bacteriol, 183, 411–25
  • Ivanova V, Petrova1 P, Hristov J. (2011). Application in the ethanol fermentation of immobilized yeast cells in matrix of alginate/magnetic nanoparticles, on chitosan-magnetite microparticles and cellulose-coated magnetic nanoparticles. Int Rev Chem Eng, 3, 289–99
  • Jaiswal P, Kashyap AK. (2002). Isolation and characterization of mutants of two diazotrophic cyanobacteria tolerant to high concentration of inorganic carbon. Microbiol Res, 157, 83–91
  • Jaiswal P, Prasanna R, Kashyap AK. (2005). Modulation of carbonic anhydrase activity in two nitrogen fixing cyanobacteria, Nostoc calcicola and Anabaena sp. J Plant Physiol, 162, 1087–94
  • Jeanfils J, Loudeche R. (1986). Photoproduction of ammonia by immobilized heterocystic cyanobacteria effect of nitrite and anaerobiosis. Biotech Lett, 8, 265–70
  • Kang RJ, Shi DJ, Cong W, et al. (2005). Regulation of CO2 on heterocyst differentiation and nitrate uptake in the cyanobacterium Anabaena sp. PCC 7120. J Appl Microbiol, 98, 693–8
  • Kangatharalingam N, Priscu JC, Paerl HW. (1992). Heterocyst envelope thickness, heterocyst frequency and nitrogenase activity in Anabaena flos-aqua: influence of exogenous oxygen tension. J Gen Microb, 138, 2673–8
  • Kannaiyan S, Rag KK, Hall DO. (1994). Immobilization of Anabaena azollae from Azolla filiculoides in polyvinyl foam for ammonia production in a photobioreactor system. WJ Microbiol Biotechnol, 10, 55–8
  • Kerby NW, Musgrave SC, Rowell P, et al. (1986). Photoproduction of ammonium by immobilized mutant strains of Anabaena variabilis. Appl Microbiol Biotechnol, 24, 42–6
  • Kistenmacher H, Maass HJ, Mostertz M, Forchhammer K. (2011). Method for biotechnological production of a hydrogen carrier. Patent application number: 20110256602
  • Komárek J, Mares J. (2012). An update to modern taxonomy (2011) of freshwater planktic heterocytous cyanobacteria. Hydrobiologia, 698, 327–51
  • Kumar K, Mella-Herrera RA, Golden JW. (2010). Cyanobacterial heterocysts. Cold Spring Harbor Perspect Biol, 2, 1–19
  • Kumar SS, Saramma AV. (2012). Nitrate and phosphate uptake by immobilized cells of Gloeocapsa gelatinosa. J Mar Biol Ass India, 54, 119–22
  • Kustka AB, Sanudo-Wilhelmy SA, Carpenter EJ, et al. (2003). Iron requirements for dinitrogen and ammonium-supported growth in cultures of Trichodesmium (IMS 101): comparison with nitrogen fixation rates and iron: carbon ratios of field populations. Limnol Oceanogr, 48, 1869–84
  • Ladha JK, Rowell P, Stewart WD. (1978). Effects of 5-hydroxylysine on acetylene reduction and - assimilation in the cyanobacterium Anabaena cylindrica. Biochem Biophys Res Commun, 83, 688–96
  • Laurent S, Chen H, Bedu S, et al. (2005). Non-metabolizable analogue of 2-oxoglutarate elicits heterocyst differentiation under repressive conditions in Anabaena sp. PCC 7120. Proc Natl Acad Sci, 102, 9907–12
  • Luque I, Forchhammer K. (2008). Nitrogen assimilation and C/N balance sensing. In: Flores E, Herrero A, eds. The cyanobacteria: molecular biology, genomics and evolution. Norwich, UK: Horizon Scientific Press, 335–82
  • Mackey EJ, Smith GD. (1983). Adaptation of the cyanobacterium Anabaena cylindrica to high oxygen tensions. FEBS Lett, 156, 108–12
  • Mahesh G, Kannaiyan S. (1993). Effect of immobilization of cyanobacteria in solid matrix on ammonia excretion and nitrogen fixing activity. Biotech Lett, 15, 975–8
  • Melnicki MR, Pinchuk GE, Hill EA, et al. (2013). Feedback-controlled LED photobioreactor for photophysiological studies of cyanobacteria. Bioresour Technol, 134, 127–33
  • Milligan AJ, Berman-Frank I, Gerchman Y, et al. (2007). Light-dependent oxygen consumption in nitrogen-fixing cyanobacteria plays a key role in nitrogenase protection. J Phycol, 43, 845–52
  • Misra HS, Tuli R. (2000). Differential expression of photosynthesis and nitrogen fixation genes in the cyanobacterium Plectonema boryanum. Plant Physiol, 122, 731–76
  • Mohr W, Großkopf T, Wallace DWR, LaRoche J. (2010). Methodological underestimation of oceanic nitrogen fixation rates. PLoS ONE, 5, e12583
  • Moisander PH, Hench JL, Kononen K, Paerl HW. (2002). Small-scale shear effects on heterocystous cyanobacteria. Limnol Oceanogr, 47, 108–19
  • Montaya JP, Voss M, Kahler P, Capone DG. (1996). A simple, high precision, high-sensitivity tracer assay for N2 fixation. Appl Environ Microbiol, 62, 986–93
  • Moreno J, Rodríguez H, Vargas MA, et al. (1995). Nitrogen-fixing cyanobacteria as source of phycobiliprotein pigments. Composition and growth performance of ten filamentous heterocytous strains. J Appl Phycol, 7, 17–23
  • Moreno J, Vargas MA, Olivares H, et al. (1998). Exopolysaccharide production by the cyanobacterium Anabaena sp. ATCC 33047 in batch and continuous culture. J Biotech, 60, 175–82
  • Moreno J, Vargas MA, Rodrıguez H, et al. (2003). Outdoor cultivation of a nitrogen-fixing marine cyanobacterium, Anabaena sp. ATCC 33047. Biomol Eng, 20, 191–7
  • Moreno-Garrido I. (2008). Microalgae immobilization: current techniques and uses. Bioresour Technol, 99, 3949–64
  • Mulholland MR, Bronk DA, Capone DG. (2004). Dinitrogen fixation and release of ammonium and dissolved organic nitrogen by Trichodesmium IMS101. Aquat Microb Ecol, 37, 85–94
  • Musgrave SC, Kerby NW, Codd GA, Stewart WDP. (1982). Sustained ammonia production by immobilized filaments of the nitrogen-fixing cyanobacterium Anabaena 27893. Biotech Lett, 4, 647–52
  • Nayak BK, Das D. (2013). Improvement of carbon dioxide biofixation in a photobioreactor using Anabaena sp. PCC 7120. Process Biochem, 48, 1126–32
  • Newton JW, Tyler DD. (1987). Involvement of photosystem II in the ammonia metabolism of a heterotrophic cyanobacterium. BBA-Bioenerget, 891, 49–55
  • Olmedo-Verd E, Muro-Pastor AM, Flores E, Herrero A. (2006). Localized induction of the ntcA regulatory gene in developing heterocysts of Anabaena sp. strain PCC 7120. J Bacteriol, 188, 6694–9
  • Park H, Rho KK, Hall DO. (1991). Photoproduction of hydrogen, hydrogen peroxide and ammonia using immobilized cyanobacteria. Int J Hydrogen Energy, 16, 313–8
  • Patzek TW. (2004). Thermodynamics of the corn-ethanol biofuel cycle. Crit Rev Plant Sci, 23, 519–67
  • Pratte BS, Thiel T. (2006). High-affinity vanadate transport system in the cyanobacterium Anabaena variabilis ATCC 29413. J Bacteriol, 188, 464–8
  • Prosperi, CH. (1994). A cyanophyte capable of fixing nitrogen under high levels of oxygen? J Phycol, 30, 222–4
  • Pulz O, Scheibenbogen K. (1998). Photobioreactors: design and performance with respect to light energy input. In: Scheper T, ed. Bioprocess and algae reactor technology, apoptosis. Berlin, Heidelberg: Springer, 123–52
  • Pushparaj B, Pelosi E, Torzillo G, et al. (1994). Growth physiology of a marine nitrogen-fixing cyanobacterium (Nodularia harveyana) in outdoor culture. J Appl Phycol, 6, 533–7
  • Querijero-Palacpac NM, Martinez MR, Boussiba S. (1990). Mass cultivation of the nitrogen-fixing cyanobacterium Gloeotrichia natans, indigenous to rice-fields. J Appl Phycol, 2, 319–25
  • Raghuvanshi R, Singh S, Bisens PS. (2007). Iron mediated regulation of growth and siderophore production in a diazotrophic cyanobacterium Anabaena cylindrica. Indian J Exp Biol, 45, 563–7
  • Rai AK, Abraham G. (1993). Salinity tolerance and growth analysis of the cyanobacterium Anabaena doliolum. B Environ Contam Tox, 51, 724–31
  • Rai AK, Sharma NK. (2006). Phosphate metabolism in the cyanobacterium Anabaena doliolum under salt stress. Curr Microbiol, 52, 6–12
  • Ramos JL, Guerrero MG, Losada M. (1984). Sustained photoproduction of ammonia from dinitrogen and water by the nitrogen-fixing cyanobacterium Anabaena sp. strain ATCC 33047. Appl Environ Microbiol, 48, 114–8
  • Ramos JL, Guerrero MG, Losada M. (1987). Factors affecting the photoproduction of ammonia from dinitrogen and water by the Cyanobacterium Anabaena sp. strain ATCC 33047. Biotechnol Bioeng, 21, 566–71
  • Rao KK, Cammack R. (2001). Chap 10 producing hydrogen as a fuel 201-230. In: Cammack R, Frey M, Robson R, eds. Hydrogen as a duel: learning from nature. London, New York: Taylor and Francis Publisher, 262
  • Reglinski A, Rowell P, Kerby NW, Stewart WDP. (1989). Characterization of methylammonium/ammonium transport in mutant strains of Anabaena variabilis resistant to ammonium analogues. J Gen Microbiol, 135, 1441–51
  • Rossignol N, Lebeau T, Jaouen P, Robert JM. (2000). Comparison of two membrane-photobioreactors, with free or immobilized cells, for the production of pigments by a marine diatom. Bioproc Eng, 23, 495–501
  • Sanchez OJ, Cardona CA. (2008). Trends in biotechnological production of fuel ethanol from different feedstocks. Bioresour Technol, 99, 5270–95
  • Sandh G, Xu L, Bergman B. (2012). Diazocyte development in the marine diazotrophic cyanobacterium Trichodesmium. Microbiol, 158, 345–52
  • Saxena RK, Raghuvanshi R, Singh S, Bisen PS. (2006). Iron induced metabolic changes in the diazotrophic cyanobacterium Anabaena PCC 7120. Indian J Exp Biol, 44, 849–51
  • Shi DJ, Brouers M, Hall DO, Robins RJ. (1987). The effects of immobilization on the biochemical, physiological and morphological features of Anabaena azollae. Planta, 172, 298–308
  • Singh AP, Tiwari DN. (1998). Phenotypic expression of ammonia-excreting mutants of Anabaena 7120 under nitrogen limitation. W J Microbiol Biotechnol, 14, 591–3
  • Singh HN, Singh RK, Sharma R. (1983). A l-methionine-d,l-sulfoximine-resistant mutant of the cyanobacterium Nostoc muscorum showing inhibitor-resistant γ−glutamyl-transferase, defective glutamine synthetase and producing extracellular ammonia during N2 fixation. FEBS Lett, 154, 10–14
  • Singh M, Pandey JP, 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. J Algal Biomass Utln, 2, 17–23
  • Spiller H, Latorre C, Hassan ME, Shanmugam KT. (1986). Isolation and characterization of nitrogenase-derepressed mutant strains of cyanobacterium Anabaena variabilis. J Bacteriol, 165, 412–9
  • Srivastava R, Amla DV. (2002). Molecular characteristics of glnA linked mutations in the nitrogen-fixing cyanobacterium Nostoc muscorum. Curr Microbiol, 44, 94–101
  • Staal M, Hekkert STL, Harren FJM, Stal LJ. (2001). Nitrogenase activity in cyanobacteria measured by the acetylene reduction assay: a comparison between batch incubation and on-line monitoring. Environ Microbiol, 3, 343–51
  • Stal LJ, Krumbein WE. (1985). Nitrogenase activity in the non-heterocytous cyanobacterium Oscillatoria sp. Grown under alternating light-dark cycles. Arch Microbiol, 143, 67–71
  • Stal LJ, Zehr JP. (2008). Cyanobacterial nitrogen fixation in the ocean: diversity, regulation, and ecology. In: Flores FG, ed. The cyanobacteria: molecular biology, genomics and evolution. Norwich, UK: Horizon Scientific Press, 423–46
  • Stewart WD, Fitzgerald GP, Burris RH. (1968). Acetylene reduction by nitrogen-fixing blue-green algae. Arch Mikrobiol, 62, 336–48
  • Subramanian G, Shanmugasundaram S. (1986). Uninduced ammonia release by the nitrogen-fixing cyanobacterium Anabaena. FEMS Microbiol Lett, 37, 151–4
  • Taniuchi Y, Yoshikawa S, Maeda SI, et al. (2008). Diazotrophy under continuous light in a marine unicellular diazotrophic cyanobacterium, Gloeothece sp. 68DGA. Microbiol, 15, 1859–65
  • Thomas J, Apte SK. (1984). Sodium requirement and metabolism in nitrogen-fixing cyanobacteria. J Biosci, 6, 771–94
  • Thomas SP, Zaritsky A, Boussiba S. (1990). Ammonium excretion by an l-methionine-d,l-sulfoximine-resistant mutant of the rice-field cyanobacterium Anabaena siamensis. Appl Environ Microbiol, 56, 3499–504
  • Thompson AW, Foster RA, Krupke A, et al. (2012). Unicellular cyanobacterium symbiotic with a single-celled eukaryotic alga. Science, 337, 1546–50
  • Thompson AW, Carter BJ, Turk-Kubo K, et al. (2014). Genetic diversity of the unicellular nitrogen-fixing cyanobacteria UCYN-A and its prymnesiophyte host. Environ Microbiol, 16, 3238–49
  • Vincenzini M, Philippis RD, Ena A, Florenzano G. (1986). Ammonia photoproduction by Cyanospira rippkae cells ‘entrapped' in dialysis tube. Experientia, 42, 1040–3
  • Walsby AE. (1968). Mucilage secretion and the movements of blue–green algae. Protoplasma, 65, 223–38
  • Walsby AE. (1985). The permeability of heterocysts to the gases nitrogen and oxygen. Proc R Soc Lond B, 226, 345–66
  • Walsby AE. (2007). Cyanobacterial heterocysts: terminal pores proposed as sites of gas exchange. Trends Microbiol, 15, 340–49
  • Wilson ST, Bottjer D, Church MJ, Karl DM. (2012). Comparative assessment of nitrogen fixation methodologies, conducted in the oligotrophic North Pacific. Ocean Appl Environ Microbiol, 78, 6516–23
  • Yang J, Xu M, Zhang XZ, et al. (2011). Life-cycle analysis on biodiesel production from microalgae: Water footprint and nutrients balance. Bioresour Technol, 102, 159–65
  • Yoon JH, Choi SS, Park TH. (2012). The cultivation of Anabaena variabilis in a bubble column operating under bubbly and slug flows. Bioresour Technol, 110, 430–6
  • Yu G, Shi D, Cai Z, Cong W, Ouyang F. (2011). Growth and physiological features of cyanobacterium Anabaena sp. strain PCC 7120 in a glucose-mixotrophic culture. Chin J Chem Eng, 19, 108–15
  • Yu H, Jia S, Dai Y. (2010). Accumulation of exopolysaccharides in liquid suspension culture of Nostoc flagelliforme cells. Appl Biochem Biotechnol, 160, 552–60
  • Zhang K, Kurano N, Miyachi S. (1999). Outdoor culture of a cyanobacterium with a vertical flat-plate photobioreactor: effects on productivity of the reactor orientation, distance setting between the plates and culture temperature. Appl Microbiol Biotechnol, 52, 781–6
  • Zhang W, Furusaki S. (2001). On the evaluation of diffusivities in gels using the diffusion cell technique. Biochem Eng J, 9, 73–82
  • Zhang Y, Pu H, Wang Q, et al. (2007). PII is important in regulation of nitrogen metabolism but not required for heterocyst formation in the cyanobacterium Anabaena sp. PCC 7120. J Biol Chem, 282, 33641–8
  • Zimmerman WJ. (1987). Growth, nitrogen fixation, and mass culture of isolated Anabaena azollae. Biotechnol Lett, 9, 31–6

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