In cyanobacteria both photosynthesis and nitrogen fixation can be affected by UV radiation. Two of the most abundant heterocystous cyanobacteria isolates from a temperate ricefield in Uruguay belonging to Anabaena and Calothrix genus were exposed for 1 or 3 hours to UV-B dosis similar to those to which they are exposed in summer. Anabaena survival after 1 h of UV-B exposure was 10% whereas in Calothrix’s was 30%. Both the quantum yields of photosybtem II fluorescence and O 2 photoevolution decreased with time of UV-B exposure for Calothrix and only till 1 h for Anabaena . Only the Calothrix strain presented phycoerithryn as antenna pigment and constitutive UV-B screening mycosporine like aminoacids. In the Anabaena strain, nitrogenase activity was drastically reduced with UV-B irradiation but in Calothrix was not affected. Proline content and lipid peroxidation increased after 3 hours of UV-B exposure only in Anabaena sp. The antioxidant enzyme activities evaluated followed different trends for both isolates, with an increase in superoxide dismutase activity in the Calothrix isolate. These results show that the two nitrogen-fixing cyanobacteria studied have different responses to UV-B radiation and that cyanobacteria diversity may be considered when selecting strains to be used as biofertilizers.
KeywordsCyanobacteriaAntioxidant Responses to UV-BMycosporineNitrogenase Activity
V. L. Orce, A. Paladini and E. W. Helbling, “Radiación Ultravioleta y Ozono Atmosférico: Influencia del Agujero de Ozono en Argentina,” In: G. R. Forno and F. M. Andrade, Eds., Naturaleza y Efectos de la Radiación Ultravioleta y la Capa de Ozono, Instituto de Investigaciones Físicas-UMSA, La Paz, 1997, pp. 31-41.
Y.-Y. He, M. Klisch and D.-P. Hader, “Adaptation of Cyanobacteria to UV-B Stress Correlated with Oxidative Stress and Oxidative Damage,” Photochemistry and Photobiology, Vol. 76, No. 2, 2002, pp. 188-196.
D.-P. Hader, H. D. Kumar, R. C. Smith and R. C. Worrest, “Effects of Solar UV Radiation on Aquatic Ecosystems and Interactions with Climate Change,” Photochemical & Photobiological Sciences, Vol. 10, No. 3, 2007, pp. 267- 285.
R. P. Sinha and D.-P. Hader, “UV-Protectants in Cyanobacteria,” Plant Science, Vol. 174, No. 3, 2008, pp. 278- 289. doi:10.1016/j.plantsci.2007.12.004
A.Vaishampayan, R. P. Sinha, D.-P. Hader, T. Dey, A. K. Gupta, U. Bhan and A. L. Rao, “Cyanobacterial Biofertilizers in Rice Agriculture,” Botanical Review, Vol. 67, No. 4, 2001, pp. 453-516. doi:10.1007/BF02857893
P. Irisarri, “Role of Cyanobacteria as Biofertilizers: Potentials and Limitations,” In: M. K. Rai, Ed., Handbook of Microbial Fertilizers, The Haworth Press Inc., Binghamton, 2006. pp. 417-430.
P. Irisarri, S. Gonnet, E. Deambrosi and J. Monza, “Cyanobacterial Inoculation and Nitrogen Fertilization in Rice,” World Journal of Microbiology and Biotechnolology, Vol. 23, No. 2, 2007, pp. 237-242. doi:10.1007/s11274-006-9219-0
L. Aubriot, D. Conde, S. Bonilla and R. Sommaruga, “Phosphate Uptake Behavior of Natural Phytoplankton during Exposure to Solar Ultraviolet Radiation in a Shallow Coastal Lagoon,” Marine Biology, Vol. 144, No. 4, 2004, pp. 623-631. doi:10.1007/s00227-003-1229-y
T. D. B. MacKenzie, R. A. Burns and D. Campbell, “Carbon Status Constrains Light Acclimation in the Cyanobacterium Synechococcus elongatus,” Plant Physiology, Vol. 136, No. 2, 2004, pp. 3301-3312. doi:10.1104/pp.104.047936
P. Irisarri, S. Gonnet, E. Deambrosi and J. Monza, “Diversidad de Cyanobacterias con Heterocisto en Suelos Cultivados con Arroz,” Agrociencia, Vol. 1, No. 3, 1999, pp. 44-49.
R. Rippka, J. Deruelles, J. B. Watterbury, M. Herdman and R. Y. Stainer, “Generic Assignments, Strain Histories and Properties of Pure Cultures of Cyanobacteria,” Journal of General Microbiology, Vol. 111, No. 1, 1979, pp. 1-61.
V. A. Donkor and D.-P. Hader, “Effects of Ultraviolet Irradiation on Photosynthetic Pigments in Some Filamentous Cyanobacteria,” Aquatic Microbial Ecology, Vol. 11, No. 2, 1996, pp. 143-149. doi:10.3354/ame011143
A. Benett and L. Bogorad, “Complementary Chromatic Adaptation in a Filamentous Blue-Green Alga,” Journal of Cell Biology, Vol. 58, No. 2, 1973, pp. 419-435. doi:10.1083/jcb.58.2.419
D.-P. Hader, M. Lebert, R. Marangoni and G. Colombetti, “ELDONET-European Light Dosimeter Network Hardware and Software,” Journal of Photochemistry and Photobiology B: Biology, Vol. 52, No. 1-3, 1999, pp. 51-58. doi:10.1016/S1011-1344(99)00102-5
K. Rohácek and M. Barták, “Technique of the Modulated Chlorophyll Fluorescence: Basic Concepts, Useful Parameters, and Some Applications,” Photosynthetica, Vol. 37, No. 3, 1999, pp. 339-363. doi:10.1023/A:1007172424619
R. P. Sinha, M. Klisch, A. Vaishampayan and D.-P. Hader, “Biochemical and Spectroscopic Characterization of the Cyanobacterium Lyngbya sp. Inhabiting Mango (Mangifera indica) Trees: Presence of an Ultraviolet-Absorbing Pigment, Scytonemin,” Acta Protozoologica, Vol. 38, No. 4, 1999, pp. 291-298.
G. Minotti and S. Aust, “The Requirement for Iron (III) in the Initiation of Lipid Peroxidation by Iron (II) and Hydrogen Peroxide,” Journal of Biological Chemistry, Vol. 262, No. 3, 1987, pp. 1098-1104.
C. Rusterucci, V. Stallaert, M. Milat, A. Pugin, P. Ricci and J. Blein, “Relationship between Active Oxygen Species, Lipid Peroxidation, Necrosis, and Phytoalexin Production Induced by Elicitins in Nicotiana,” Plant Physiology, Vol. 111, No. 3, 1996, pp. 885-891.
O. Borsani, P. Díaz and J. Monza, “Proline is Involved in Water Stress Responses of Lotus corniculatus Nitrogen Fixing and Nitrate Fed Plants,” Journal of Plant Physiology, Vol. 155, No. 2, 1999, pp. 269-273. doi:10.1016/S0176-1617(99)80018-2
J. G. Foster and J. L. Hess, “Responses of Superoxide Dismutase and Glutathione Reductase Activities in Cotton Leaf Tissue Exposed to an Atmosphere Enriched in Oxygen1,” Plant Physiology, Vol. 66, No. 3, 1980, pp. 482- 487. doi:10.1104/pp.66.3.482
R. F. Beer and I. W. Sizer, “A Spectrophotometric Method for Measuring the Breakdown of Hydrogen Peroxide by Catalase,” Journal of Biological Chemistry, Vol. 195, 1952, pp. 133-140.
G.-X. Chen and K. Asada, “Ascorbate Peroxidase in Tea Leaves: Occurrence of Two Isozymes and the Differences in Their Enzymatic and Molecular Properties,” Plant Cell Physiology, Vol. 30, No. 7, 1989, pp. 987-998.
O. H. Lowry, N. J. Rosenbrough, A. L. Farr and R. J. Randall, “Protein Measurement with the Folin Phenol Reagent,” Journal of Biological Chemistry, Vol. 193, 1951, pp. 265-275.
J. L. Donahue, C. M. Okpodu, C. L. Cramer, E. A. Grabau and R. G. Alscher, “Responses of Antioxidants to Paraquat in Pea Leaves (Relationships to Resistance),” Plant Physiology, Vol. 113, No. 1, 1997, pp. 249-257.
M. Sainz, P. Díaz, J. Monza and O. Borsani, “Heat Stress Results in Loss of Chloroplast Cu/Zn Superoxide Dismutase and Increased Damage to Photosystem II in Combined Drought-Heat Stressed Lotus japonicus,” Physiologia Plantarum, Vol. 140, No. 1, 2010, pp. 46-56. doi:10.1111/j.1399-3054.2010.01383.x
R. P. Sinha, M. Klisch, A. Groniger and D.-P. Hader, “Ultraviolet Absorbing/Screening Substances in Cyanobacteria, Phytoplankton and Macroalgae,” Journal of Photochemistry & Photobiology. B: Biology, Vol. 47, No. 2-3, 1998, pp. 83-94. doi:10.1016/S1011-1344(98)00198-5
Y. Y. He and D.-P. Hader, “UV-B Induced Formation of Reactive Oxygen Species and Oxidative Damage of the Ascorbic Acid and N-Acetyl.L-Cysteine,” Photochemical & Photobiological Sciences, Vol. 1, No. 10, 2002, pp. 729- 736. doi:10.1039/b110365m
P. S. Singh, R. P. Sinha, M. Klisch and D.-P. Hader, “Mycosporine-Like Amino Acids (MAAs) Profile of a Rice-Weld Cyanobacterium Anabaena doliolum as Influenced by PAR and UVR,” Planta, Vol. 229, No. 1, 2008, pp. 225-233. doi:10.1007/s00425-008-0822-1
M. P. Lesser, “Effects of Ultraviolet Radiation on Productivity and Nitrogen Fixation in the Cyanobacterium, Anabaena sp. (Newton’s Strain)”, Hydrobiologia, Vol. 598, No. 1, 2008, pp. 1-9. doi:10.1007/s10750-007-9126-x
D. Campbell, V. Hurry, A. K. Clarke, P. Gustaffson and G. Oquist, “Chlorophyll Fluorescence Analysis of Cyano-bacterial Photosynthesis and Acclimation,” Microbiology & Molecular Biology Review, Vol. 62, No. 3, 1998, pp. 667-683.
M. Lesser, “Oxidative Stress in Marine Environments: Biochemistry and Physiological Ecology,” Annual Review of Physiology, Vol. 68, 2006, pp. 253-278. doi:10.1146/annurev.physiol.68.040104.110001
M. Lesser, J. Neale and J. J. Cullen, “Acclimation of Antartic Phytoplankton to Ultraviolet Radiation: Ultraviolet-Absorbing Compounds and Carbon Fixation,” Molecular Marine Biology Technology, Vol. 5, No. 4, 1996, pp. 314-332.
C. Hazzard, M. P. Lesser and R. A. Kinzie III, “Effects of Ultraviolet Radiation on Photosynthesis in the Subtropical Marine Diatom, Chaetoceros gracilis (Baccilariophyceae),” Journal of Phycology, Vol. 33, No. 6, 1997, pp. 960-968. doi:10.1111/j.0022-3646.1997.00960.x
J. N. Bouchard, D. A. Roy and D. A. Campbell, “UVB Effects on the Photosystem II-D1 Protein of Phytoplankton and Natural Phytoplankton Communities,” Photochemistry & Photobiology, Vol. 82, No. 4, 2006, pp. 936- 951. doi:10.1562/2005-08-31-IR-666
J. W. Newton, D. D. Tyler and M. E. Slodki, “Effects of Ultraviolet-B (290-320 nm) Radiation on Blue-Green Algaea (cyanobacteria), Possible Biological Indicators of Straspheric Ozone Depletion,” Applied and Environmental Microbiology, Vol. 37, No. 6, 1979, pp. 1137-1141.
W. D. P. Stewart, “Some Aspects of Structure and Function in N Fixing Cyanobacteria,” Annual Review of Microbiology, Vol. 34, 1980, pp. 497-536. doi:10.1146/annurev.mi.34.100180.002433
A. Kumar, M. Tyagi, P. B. Jha, G. Srinivas and A. Singh, “Inactivation of Cyanobacterial Nitrogenase after Exposure to Ultraviolet-B Radiation,” Current Microbiology, Vol. 46, No. 5, 2003, pp. 380-384. doi:10.1007/s00284-001-3894-8
M. Ehling-Schulz and S. Scherer, “UV Protection in Cyanobacteria,” European Journal of Phycology, Vol. 34, No. 4, 1999, pp. 329-338. doi:10.1080/09670269910001736392
S. Scherer, H. Riege and P. Boger, “Light-Induced Proton Release by the Cyanobacterium Anabaena variabilis: Dependence on Carbon Dioxide and Sodium,” Plant Physiology, Vol. 86, No. 3, 1988, pp.769-772. doi:10.1104/pp.86.3.769
D. R. Hill, S. L. Hladun, S. Scherer and M. Potts, “Water Stress Proteins of Nostoc commune (Cyanobacteria) are Secreted with UV-A/B-absorbing Pigments and Associate with 1,4-b-D-Xylanxylanohydrolase Activity,” Journal of Biological Chemistry, Vol. 269, No. 10, 1994, pp. 7726- 7734.
G. A. Bohm, W. Pfleiderer, P. Boger and S. Scherer, “Structure of a Novel Oligosaccharide-Mycosporine-Amino Acid Ultraviolet A/B Sunscreen Pigment from the Terrestrial Cyanobacterium Nostoc commune,” Journal of Biological Chemistry, Vol. 270, 1995, pp. 8536-8539. doi:10.1074/jbc.270.15.8536
W. C. Dunlap and Y. Yamamoto, “Small-Molecule Antioxidants in Marine Organisms: Antioxidant Activity of Mycosporine-Glycine,” Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, Vol. 112, No. 1, 1995, pp.105-114. doi:10.1016/0305-0491(95)00086-N
R. W. Castenholz, “Multiple Strategies for UV Tolerance in Cyanobacteria,” Spectrum, Vol. 10, 1997, pp. 10-16.
F. Garcia-Pichel and R. W. Castenholz, “Occurrence of UV-Absorbing, Mycosporine-Like Compounds among Cyanobacterial Isolates and an Estimate of Their Screen- ing Capacity,” Applied and Environmental Microbiology, Vol. 59, No. 1, 1993, pp. 163-169.
J. G. Dillon, M. C. Tatsumi, P. G. Tandingan and R. W. Castenholz, “Effect of Environmental Factors on the Synthesis of Scytonemin, a UV Screening Pigment, in Cyanobacteria (Chroococcidiopsis sp.),” Archives of Microbiol- ogy, Vol. 177, No. 4, 2002, pp. 322-331. doi:10.1007/s00203-001-0395-x
M. Zeeshan and S. M. Prasad, “Differential Response of Growth, Photosynthesis, Antioxidant Enzymes and Lipid Peroxidation to UV-B Radiation in Three Cyanobacteria,” South African Journal of Botany, Vol. 75, No. 3, 2009, pp. 466-474. doi:10.1016/j.sajb.2009.03.003
L. Szabados and A. Savouré, “Proline: A Multifunctional Amino Acid,” Trends in Plant Science, Vol. 15, No. 2, 2009, pp. 89-97.
A. K. Singh, D. Chakravarty, T. P. K. Singh and H. N. Singh, “Evidence for a Role of L-Proline as a Salinity Protectant in the Cyanobacterium Nostoc muscorum,” Plant Cell Environment, Vol. 19, No. 4, 1996, pp. 490-494. doi:10.1111/j.1365-3040.1996.tb00342.x
A. Chris, M. Zeeshan, G. Abraham and S. M. Prasad, “Proline Accumulation in Cylindrospermum sp.,” Environmental & Experimental Botany, Vol. 57, No. 1-2, 2006, pp.154-159. doi:10.1016/j.envexpbot.2005.05.008
B. N. Tripathi and J. P. Gaur, “Relationship between Copperand Zinc-Induced Oxidative Stress and Proline Accumulation in Scenedesmus sp.,” Planta, Vol. 219, No. 3, 2004, pp. 397-404. doi:10.1007/s00425-004-1237-2
K. Asada, “Superoxide Dismutase,” In: S. Otsuka and T. Yamanaka, Eds., Metalloproteins, Elsevier, Amsterdam, 1988, pp 331-341.
C. Obinger, C. Günther, M. Regelsberger, A. Pircher, G. Strasser and G. Pescheck, “Scavenging of Superoxide and Hydrogen Peroxide in Blue-Green Algae (Cyanobacteria),” Physiologia. Plantarum, Vol. 104, No. 4, 1998, pp. 693-698. doi:10.1034/j.1399-3054.1998.1040425.x
S. Mackerness, C. F. John, B. R. Jordan and B. Thomas, “Early Signaling Components in Ultraviolet-B Responses: Distinct Roles for Different Reactive Oxygen Species and Nitric Oxide,” FEBS Letters, Vol. 489, No. 2, 2001, pp. 237-242. doi:10.1016/S0014-5793(01)02103-2
P. Bhargava, N. Atri, A. K. Srivastava and L. C. Rai, “Cadmium Mitigates Ultraviolet-B Stress in Anabaena doliolum: Enzymatic and Non-Enzymatic Antioxidants,” Biologia Plantarum, Vol. 51, No. 3, 2007, pp. 546-550. doi:10.1007/s10535-007-0118-5
B. Shirkey, D. P. Kovarcik, D. J. Wright, G. Wilmoth, T. F. Prickett, R. F. Helm, E. M. Gregory and M. Potts, “Active Fe-Containing Superoxide Dismutase and Abundant sodF mRNA in Nostoc commune (Cyanobacteria) after Years of Desiccation,” Journal of. Bacteriology, Vol. 182, No. 1, 2000, pp. 189-197. doi:10.1128/JB.182.1.189-197.2000
X. F. Zhang, F. X. Kong, H. S. Cao, J. K. Tan, Y. Tao and M. L Wang, “Research on Recruitment Dynamics of Bloom-Forming Cyanobacteria in Meiliang Bay, Taihu Lake”, Chinese Journal of Applied Ecology, Vol. 16, No. 7, 2005, 1346-1350.
J. Dat, S. Vandenabeele, E.Vranová, M. Van Montagu, D. Inzé and F. Van Breusegem, “Dual Action of the Active Oxygen Species during Plant Stress Responses,” Cellular Molecular Life Sciences, Vol. 57, No. 5, 2000, pp. 779- 795. doi:10.1007/s000180050041
R. Aráoz and D.-P. Hader, “Phycoerythrin Synthesis is Induced by Solar UV-B in the Cyanobacterium Nostoc,” Plant Physiology and Biochemistry, Vol. 37, No. 3, 1999, pp. 223-229. doi:10.1016/S0981-9428(99)80037-0
P. Streb, A. Michael-Knauf and J. Feierabend, “Preferential Photoinactivation of Catalase and Photoinhibition of Photosystem II Are Common Early Symptoms under Various Osmotic and Chemical Stress Conditions,” Physiologia Plantarum, Vol. 88, No. 4, 1993, pp. 590-598. doi:10.1111/j.1399-3054.1993.tb01376.x
M. Wirstam, M. R. A. Blomberg and P. E. M. Siegbahn, “Reaction Mechanism of Compound I Formation in Heme Peroxidases: A Density Functional Theory Study,” Journal of American Chemistry Society, Vol. 121, No. 43, 1999, pp. 10178-10185. doi:10.1021/ja991997c