Algologia 2019, 29(1): 40–58 https://doi.org/10.15407/alg29.01.040Physiology, Biochemistry, Biophysics
Effects of alkalinity, extremely low carbon dioxide concentration and irradiance on spectral properties, phycobilisome, photosynthesis, photosystems and functional groups of the native cyanobacterium Calothrix sp. ISC 65
Abbasi B.1, Shokravi Sh.1, Golsefidi M.Ah.2, Sateiee A.1, Kiaei E.1- 1Department of Biology, Gorgan Branch, Islamic Azad University, Gorgan, Iran
- 2Department of Chimistry, Gorgan Branch, Islamic Azad University, Gorgan, Iran
Abstract
In this research, Calothrix sp. ISC 65 was characterized physiologically by the combination of extremely low irradiance (2 μE·m-2·s-1), different alkalinity (pH 7, 9, 11), and extremely limited carbon dioxide concentration (no aeration, no carbon dioxide enrichment). Spectroscopical analysis showed that pH 9, after 96 hours, caused a significant increase in growth rate, chlorophyll, and phycocyanin production. A lower (pH of 7) caused a decrease of phycobilisome production even after 24 hours. Excitation of the light harvesting complex and the reaction center of photosystems resulted from a pH of 9. Phycocyanin seems to be the main part of phycobilisome but pH 9 caused phycoerythrin and allophycocyanin production excitation in the outer part of the photosynthetic antenna as well. A fluorimetric and photosynthesis-irradiance curve analysis showed that increasing alkalinity (up to pH 9) caused an increase in photosynthesis efficiency and a decrease of non-photochemical fluorescence especially after 96 hours. PSII : PSI ratio increased by increasing alkalinity from pH 7 to 9 and reached the highest level after 96 hours. Surface response plot analysis showed that there is a narrow border line around pH 9 and 96 hours which caused the highest PSII : PSI ratio. FTIR analysis showed that alkalinity caused configuration changes of the functional groups. The difference of the functional group patterns between pH 7 and 11 was significant especially after 24 hours. Differences in asymmetric carbon vibration, lipid stretching and OH bending of the polysaccharides occurred with both pH 9 and 11 treatments. pH 9 caused the most physiological activities in Calothrix sp. ISC 65 at extremely limited irradiance and carbon dioxide concentration.
Keywords: alkalinity, Calothrix, cyanobacteria, dissolved inorganic carbon, limited irradiance
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References
- Amirlatifi F., Soltani N., Saadatmand S., Shokravi S., Dezfulian M. 2013. Crude oil-induced morphological and physiological responses in cyanobacterium Microchaete tenera ISC13. Int. J. Environ. Res. 7(4): 1007-1014.
- Amirlatifi H.S., Shokravi S., Sateei A., Golsefidi M.A., Mahmoudjanlo M. 2018. Samples of cyanobacterium Calothrix sp. ISC 65 collected from oil polluted regions respond to combined effects of salinity, extremely low-carbon dioxide concentration and irradiance. Algologia. 28(2): 182-201. https://doi.org/10.15407/alg28.02.182
- Bajwa K., Bishnoi N.R. 2015. Osmotic stress induced by salinity for lipid overproduction in batch culture of Chlorella pyrenoidosa and effect on others physiological as well as physicochemical attributes. J. Algal Biomass Utln. 6: 26-34.
- Bañares-España E., Kromkamp J.C., López-Rodas V., Costas E., Flores-Moya A. 2013. Photoacclimation of cultured strains of the cyanobacterium Microcystis aeruginosa to high-light and low-light conditions. FEMS Microbiol. Ecol. 83(3): 700-710. https://doi.org/10.1111/1574-6941.12025 https://www.ncbi.nlm.nih.gov/pubmed/23057858
- Borah D., Vimala N., Thajuddin N. 2016. Biochemical composition and chemotaxonomy of cyanobacteria isolated from Assam, North-East India. Phykos. 46(2): 33-34.
- Brutemark A., Engström-Öst J., Vehmaa A., Gorokhova E. 2015. Growth, toxicity and oxidative stress of a cultured cyanobacterium (Dolichospermum sp.) under different CO2/pH and temperature conditions. Phycol. Res. 63: 56–63. https://doi.org/10.1111/pre.12075
- Cohen Z., Margheri M.C., Tomaselli L. 1995. Chemotaxonomy of cyanobacteria. Phytochemistry. 40(4): 1155-1158. https://doi.org/10.1016/0031-9422(95)00335-5
- Cole J.J., Caraco N.F., Kling G.W., Kratz T.K. 1994. Carbon dioxide supersaturation in the surface waters of lakes. Science. 265: 1568–1570. https://doi.org/10.1126/science.265.5178.1568 https://www.ncbi.nlm.nih.gov/pubmed/17801536
- Deblois C.P., Marchand A., Juneau P. 2013. Comparison of photoacclimation in twelve freshwater photoautotrophs (Chlorophyte, Bacillaryophyte, Cryptophyte and Cyanophyte) isolated from a natural community. PLOS ONE. 8(3): e57139. https://doi.org/10.1371/journal.pone.0057139 https://www.ncbi.nlm.nih.gov/pubmed/23526934 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3602455
- Dezfulian M., Soltani N., Shokravi S., Baftehchi L., Alnajar N., Ehsan S., Abolhasani Soorki A. 2010. Ecophysiological charecteres PCR - identification on Calothrix sp. ISC 65 isolated from south of Iran. NCBI : GU591756.
- Dhiab R.B., Quada H.B., Boussseta H., Franck F., Elabed A., Brouuers M. 2007. Growth, fluorescence, photosynthesis O2 production and pigment content of salt adapted cultures of Arthrospira (Spirulina) platensis. J. Appl. Phycol. 19: 293-301. https://doi.org/10.1007/s10811-006-9113-z
- Desikachary T.V. 1959. Cyanophyta. New Delhi: ICAR Monograph Algae. 686 p.
- Fernández-Valiente E., Leganés F. 1989. Regulatory effect of pH and incident irradiance on the levels of nitrogenase activity in the cyanobacterium Nostoc UAM 205. J. Plant Physiol. 135: 623–627. https://doi.org/10.1016/S0176-1617(11)80647-4
- Fraser J.M., Tulk S.E., Jeans J.A., Campbell D.A., Bibby T.S., Cockshutt A.M. 2013. Photophysiological and photosynthetic complex changes during iron starvation in Synechocystis sp. PCC 6803 and Synechococcus elongatus PCC 7942. PLoS One. 8(3): e59861. https://doi.org/10.1371/journal.pone.0059861 https://www.ncbi.nlm.nih.gov/pubmed/23527279 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3602374
- Gan F., Shen G., Bryant D.A. 2014. Occurrence of far-red light photoacclimation (FaRLiP) in diverse cyanobacteria. Life. 5(1): 4–24. https://doi.org/10.3390/life5010004 https://www.ncbi.nlm.nih.gov/pubmed/25551681 https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4390838
- Ghobadian S., Ganjidoost H., Ayati B., Soltani N. 2015. Evaluation of the effects of aeration cycle and culture medium concentration on biomass qualitative and quantitative indices in microalga Spirulina as candidate for wastewater treatment. J. Aquat. Ecol. 5(2): 87–99.
- Inoue-Kashino N., Kashino Y., Satoh K., Terashima I., Pakrasi H.B. 2005. PsbU provides a stable architecture for the oxygen-evolving system in cyanobacterial photosystem II. Biochemistry. 44(36): 12214–12228. https://doi.org/10.1021/bi047539k https://www.ncbi.nlm.nih.gov/pubmed/16142920
- Iranshahi S., Nejadsattari T., Soltani N., Shokravi S., Dezfulian M. 2014. The effect of salinity on morphological and molecular characters and physiological responses of Nostoc sp. ISC 101. Iranian J. Fisher. Sci. 13(4): 907–917.
- John D.M., Whitton B.W., Brook A.J. 2003. The Freshwater Algal Flora of the British Isles. Cambridg: Cambridge Univ. Press. 702 p.
- Kaushik B.D. 1987. Laboratory methods for blue-green algae. New Delhi: Assoc. Publ. Comp. 171 p. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC1454123
- Kenne G. van der Merwe D. 2013. Classification of toxic cyanobacterial blooms by Fourier-transform infrared technology (FTIR). Advan. in Microbiol. 3(6A): 1–8. https://doi.org/10.4236/aim.2013.36A001
- Kiaei E., Soltani N., Mazaheri Assadi M., Khavarinegad R., Dezfulian M. 2013. Study of optimal conditions in order to the use of the cyanobacteria Synechococcus sp. ISC106 as a candidate for biodiesel production. J. Aquat. Ecol. 2(4): 40–51.
- Komárek J., Anagnostidis K. 1989. Modern approach to the classification system of cyano-phytes. 4. Nostocales. Arch. Hydrobiol. Suppl. Monograph. Beiträge. 82(3): 247–345.
- Lu C., Vonshak A. 1999. Photoinhibition in outdoor Spirulina platensis cultures assessed by polyphasic chlorophyll fluorescence transients. J. Appl. Phycol. 11(4): 355–359. https://doi.org/10.1023/A:1008195927725
- Lu C., Vonshak A. 2002. Effects of salinity stress on photosystem II function in cyanobacterial Spirulina platensis cells. Physiol. Plant. 114(3): 405–413. https://doi.org/10.1034/j.1399-3054.2002.1140310.x https://www.ncbi.nlm.nih.gov/pubmed/12060263
- Marvizadeh S., Shokravi Sh., Sateii A. 2013. Ecophysiological characterization of two soil cyanobacteria Nostoc sp. FS 101 and Microcheate sp. FS 13 at the combination of salinity, extremely low irradiance and monochromatic conditions. Cell. and Mol. Plant Biol. J. 7(4): 63–67.
- Moser M., Callieri C., Weisse Th. 2009. Photosynthetic and growth response of freshwater picocyanobacteria are strain-specific and sensitive to photoacclimation. J. Plan. Res. 31(4): 349-357.
- Ogawa T., Sonoike K. 2016. Effects of bleaching by nitrogen deficiency on the quantum yield of photosystem II in Synechocystis sp. PCC 6803 revealed by Chl. fluorescence measurements. Plant and Cell Physiol. 57(3): 558-567. https://doi.org/10.1093/pcp/pcw010 https://www.ncbi.nlm.nih.gov/pubmed/26858287
- Padhi S.B., Behura S., Behera G., Behera S., Swain P., Panigrahi M., Panigrahi H., Mishra A., Beja S., Baidya S., Pradhan S. 2011. Effect of cultural conditions on biomass and nitrate reductase activity in six strains of Anabaena isolated from paddy field soils of Ganjam (Orissa). Int. J. Microbiol. Res. 2(2): 17-29.
- Poza-Carrión C., Fernández-Valiente E., Pi-as F.F., Leganés F. 2001. Acclimation to photosynthetic pigments and photosynthesis of the cyanobacterium Nostoc sp. strain UAM 206 to combined fluctuations of irradiance, pH, and inorganic carbon availability. J. Plant Physiol. 158: 1455-1461. https://doi.org/10.1078/0176-1617-00555
- Prescott G.W. 1962. Algae of the western great lake area. Dubuque, Iowa: W.M.C. Brown Comp. 977 p.
- Ratledge C., Wilkinson S.G. 1988. An overview of microbial lipids. In: Microbial lipids. Vol 1. London: Acad. Press. Pp. 3–22.
- Safaie Katoli M., Nejad Sattari T., Majd A., Shokravi Sh. 2015. Physiological, morpho-logical and ultrastructural responses of cyanobacterium Calothrix sp. ISC 65 to combination effects of extreme conditions. J. Appl. Environ. Biol. Sci. 5(1): 135–149.
- Shokravi Sh., Safaei M., Jorjani S. 2010. Studying of acclimation of the cyanobacterium Haplosiphon sp. FS 44 to the combination effects of pH and carbon dioxide concentration. Quart. J. Plant Sci. Res. 5(3): 31–42.
- Shokravi Sh., Soltani N. 2011. Acclimation of the Hapalosiphon sp. FS 56 (cyanobacteria) to combination effects of dissolved inorganic carbon and pH at extremely limited irradiance. Int. J. Algae. 13(4): 379–391. https://doi.org/10.1615/InterJAlgae.v13.i4.60
- Shokravi Sh., Amirlatifi F., Safaie M., Ghasemi Y., Soltani N. 2012. Some physiological responses of Nostoc sp. JAH 109 to the combination effects of limited irradiance, pH and DIC availability. Quart. J. Plant Sci. Res. 1(3): 55–63.
- Shokravi Sh., Amirlatifi H.S., Pakzad A., Abbasi B., Soltani N. 2014. Physiological and morphological responses of unexplored cyanobacteria Anabaena sp. FS 77 collected from oil polluted soils under a combination of extreme conditions. Int. J. Algae. 16(2): 164–180. https://doi.org/10.1615/InterJAlgae.v16.i2.70
- Soltani N., Khavarinejad R.A., Tabatabaei Yazdi M., Shokravi Sh. Fernández-Valiente E., 2005. Physiological and antimicrobial characterizations of some cyanobacteria in Extreme environments. Сand. Sci. Diss. Abstract.
- Soltani N., Khavarinejad R.A., Shokravi Sh. 2006. The effect of ammonium on growth and metabolism of soil cyanobacteria Fischerella sp. FS18. Quart. J. Plant Sci. Res. 1(1): 48–53.
- Soltani N., Khavarinejad R.A., Tabatabaie M., Shokravi Sh., Fernandez Valiente E.F., 2007. Variation of nitrogenase activity, photosynthesis and pigmentation of cyanobacteria Fischerella ambigua strain FS18 under different irradiance and pH. World J. Microbiol. Biotechnol. 22(6): 571–577. https://doi.org/10.1007/s11274-005-9073-5
- Soltani N., Zarrini G., Ghasemi Y., Shokravi Sh., Baftechi L. 2009. Characterization of soil cyanobacterium Fischerella sp. FS18 under NaCl stress. J. Biol. Sci. 7(6): 931–936.
- Soltani N., Baftechi L., Dezfulian M., Shokravi Sh., Alnajar N. 2012. Molecular and morphological characterization of oil polluted microalgae. Int. J. Environ. Res. 6(2): 481–492.
- Summerfield T.C., Crowford T.S., Young R.D., Chau J.P.S., Macdonald R.L., Sherman L.A., Eaton-Ray J.J. 2013. Environmental pH affects photoautotrophic growth of Synechocystis sp. PCC 6803 strains carrying mutations in the lumenal proteins of PSII. Plant Cell Phisiol. 54(6): 859–874. https://doi.org/10.1093/pcp/pct036 https://www.ncbi.nlm.nih.gov/pubmed/23444302
- Tiffany L., Britton M. 1971. The Algae of Illinois. New York: Hafner Publ. Co. 407 p.
- Tiwari S., Mohanty P. 1996. Cobalt induced changes in photosystem activity in Synechocystis PCC 6803: Alterations in energy distribution and stoichiometry. Photosynth. Res. 50(3): 243–256. https://doi.org/10.1007/BF00033123 https://www.ncbi.nlm.nih.gov/pubmed/24271963
- Tyler D.B., MacKenzie R., Burns A., Campbell D.A. 2004. Carbon status constrains light acclimation in the cyanobacterium Synechococcus elongates. Plant Physiol. 136: 3301–3312. https://doi.org/10.1104/pp.104.047936
- Wang Qiang, Saowarath Jantaro, Bingshe Lu, Waqar Majeed, Marian Bailey, Qingfang He. 2008. The high light-inducible polypeptides stabilize trimeric photosystem I complex under high light conditions in Synechocystis PCC 6803. Plant Physiol. 147: 1239–1259.
- Yamanaka G., Glazer A.N. 1981. Dynamic aspects of phycobilisome structure: modulation of phycocyanin content of Synechococcus phycobilisomes. Arch. Microbiol. 130: 23–30. https://doi.org/10.1007/BF00527067
- Zeng M.T., Vonshak A. 1998. Adaptation of Spirulina platensis to salinity-stress. Comparative biochemistry and physiology. Pt A. Mol. and Integr. Physiol. 120(1): 113–118. https://doi.org/10.1016/S1095-6433(98)10018-1
- Zorz J.K., Allanach J.R., Murphy C.D., Roodvoets M.S., Campbell D.A., Cockshutt A.M. 2015. The RUBISCO to photosystem II ratio limits the maximum photosynthetic rate in picocyanobacteria. Life. 5(1): 403–417. https://doi.org/10.3390/life5010403 https://www.ncbi.nlm.nih.gov/pubmed/25658887PMCid:PMC4390859