Stress response in cyanobacteria

Subject Areas : Stress Physiology

Maryam  Rezayian ¹ (Department of Plant Biology and Center of Excellence in Phylogeny of Living Organisms in Iran, School of Biology, College of Science, University of Tehran, Tehran 14155, Iran)
Vahid  Niknam ² (Department of Plant Biology and Center of Excellence in Phylogeny of Living Organisms in Iran, School of Biology, College of Science, University of Tehran, Tehran 14155, Iran)
Hassan  Ebrahimzadeh ³ (Department of Plant Biology and Center of Excellence in Phylogeny of Living Organisms in Iran, School of Biology, College of Science, University of Tehran, Tehran 14155, Iran)

Received: 2019-08-05 Accepted : 2019-08-05 Published : 2019-05-01

Keywords: Stress, reactive oxygen species, Tolerance, Cyanobacteria, antioxidants, mitigation strategies,

Abstract :

Cyanobacteria are an important source of natural products. In this article, we briefly review the responses of cyanobacteria to different stresses. Abiotic stresses (temperature, salt, heavy metals, metalloid and ultraviolet (UV) influence cell growth and metabolism in cyanobacteria. Salt stress is a major abiotic factor that decreases the growth of cyanobacteria and affects the different processes including photosynthesis, respiration, and metabolism. The basic mechanisms for salinity adaptation include the active extrusion of inorganic ions and the accumulation of compatible solutes such as sucrose, trehalose, glucosyl glycerol, and glycine betaine. Cyanobacteria have a complex antioxidative system including enzymatic and nonenzymatic antioxidants for mitigation of oxidative damage under salt stress. Cyanobacteria have some defense mechanisms for the decline of the direct and indirect destructive effects of UV. These mechanisms include avoidance, scavenging of reactive oxygen species (ROS), synthesis of UV-absorbing/screening compounds such as mycosporine-like amino acids and scytonemin, repair of UV-induced damage in DNA, and resynthesis of proteins. Metals are involved in key metabolic pathways as redox cofactors in proteins. High concentration of metals causes the generation of ROS and oxidative damage. Thus, the major role of metal homeostasis in maintaining the intracellular concentration of metal within a range compatible with cell viability becomes evident. The biosynthesis of metabolites can be triggered by a number of abiotic stresses because they affect metabolic pathways.

References:

Allen, M.B. and D.I. Arnon. 1955. ˈStudies on nitrogen-fixing blue-green algae. I. Growth and nitrogen fixation by Anabaena cylindricaLemmˈ. Plant Physiology, 30:366-372.

Apte, S.K. and A.A. Bhagwat. 1989. ˈSalinity stress-induced proteins in two nitrogen-fixing Anabaena strains differentially tolerant to saltˈ. Journal of Bacteriology, 171:909-915.

Asish, K.P. and B.D. Anath. 2005. ˈSalt tolerance and salinity effects on plants: a reviewˈ. Ecotoxicology Environmental Safety, 60:324-349.

Avonce, N., A. Mendoza-Vargas, E. Morett, and G Iturriaga. 2006. ˈInsights on the evolution of trehalose biosynthesisˈ. BMC Evolutionary Biology, 6:109.

Begum, H., F.M. Yusoff, S. Banerjee, H. Khatoon and M. Shariff. 2016. ˈAvailability and utilization of pigments from microalgaeˈ. Critical Review in Food Science and Nutrition, 5:2209-2222.

Battchikova, N., J.P. Vainonen, N. Vorontsova, M. Keranen, D. Carmel, and E.M. Aro. 2010. ˈDynamic changes in the proteome of Synechocystis 6803 in response to CO₂ limitation revealed by quantitative proteomicsˈ. Journal of Proteome Research, 9:5896-5912.

Bhandari, R. and P.K. Sharma. 2006. ˈHigh-light-induced changes on photosynthesis, pigments, sugars, lipids, and antioxidant enzymes in freshwater (Nostoc spongiaeforme) and marine (Phormidium corium) cyanobacteriaˈ. Photochemistry and Photobiology, 82:702-710.

Bhargava, S. and K. Singh. 2006. The ˈDifferential response of NaCl resistant mutants of the cyanobacterium Nostoc muscorum to salinity and osmotic stressˈ. World Journal of Microbiology and Biotechnology, 22:783-789.

Bhaya, D., R. Schwarz, and A.R. Grossman. 2000. ˈMolecular responses to environmental stress. In The ecology of Cyanobacteria: their diversity in time and space (Whitton, B.A. & Potts, M., editors), 397-442. Kluwer, Dordrechtˈ.

Blakefield, M.K., and D.O. Harris. 1994. ˈDelay of cell differentiation in Anabaena aequalis caused by UV-B radiation and the role of photoreactivation and excision repairˈ. Photochemistry and Photobiology, 59:204-208.

Blindauer, C.A. 2008. ˈZinc-handling in cyanobacteria: An updateˈ. Chemistry and Biodiversity, 5:1990-2013.

Blindauer, C.A. 2011. ˈBacterial metallothioneins: Past, present, and questions for the futureˈ. Journal of Biology Inorganic Chemistry, 16:1011-1024.

Borges, N., A. Ramos, N.D.H. Raven, R.J. Sharp, and H. Santos. 2002. ˈComparative study of the thermostabilizing properties of mannosylglycerate and other compatible solutes on model enzymesˈ. Extremophiles, 6:209-216.

Borowitzka, M.A. 2018. ˈThe ‘stress concept in microalgal biology-homeostasis, acclimation, and adaptationˈ. Journal of Applied Phycology, https://doi.org/10.1007/s10811-018-1399-0.

Bremer, E. and R. Kramer. 2000. ˈCoping with osmotic challenges: osmoregulation through accumulation and release of compatible solute in bacteriaˈ. In Bacterial Stress Responses; Hengge-Aronis, R., Ed.; ASM Press: Washington, DC, USA, pp. 79-96.

Bruins, M.R., S. Kapil, and F.W. Oehme. 2000. ˈMicrobial resistance to metals in the environmentˈ. Ecotoxicology Environmental Safety, 45:198-207.

Bultel-Poncé, V., F. Felix-Theodore, C. Sarthon, J.F. Ponge and B. Bodo. 2004. ˈNew pigments from the terrestrial cyanobacterium Scytonema sp. collected on the Mitaka Inselberg, French Guyanaˈ. Journal of Natural Product, 67:678-681.

Cardozo, K.H.M., T. Guaratini, M.P. Barros, V.R. Falcao, A.P. Tonon, N.P. Lopes, S. Campos, M.A. Torres, A.O. Souza, P. Colepicolo and E. Pinto. 2007. ˈMetabolites from algae with economic impactˈ. Comparative Biochemistry and Physiology C Toxicology Pharmacology, 146:60-78.

Cheng, D., and Q. He. 2014. ˈAssessment of environmental stresses for enhanced microalgal biofuel production–an overviewˈ. Frontiers in energy research,2:26-34.

Chintalapati, S., J.S.S. Prakash, P. Gupta, S. Ohtani, I. Suzuki, T. Sakamoto, and S. Shivaji. 2006. ˈA novel Δ9 acyl-lipid desaturase, DesC2, from cyanobacteria acts on fatty acids esterified to the sn− 2 positions of glycerolipidsˈ. Biochemical Journal, 398:207-214.

Chisti, Y. 2007. ˈBiodiesel from microalgaeˈ. Biotechnology Advance, 25:294-306.

Chris, A., Zeeshan, M., Abraham, G. and Prasad, S.M. 2006. ˈProline accumulation in Cylindrospermum sp.ˈ Environmental and Experimental and Botany, 57:154-159.

Dadheech, N. 2010. ˈDesiccation tolerance in cyanobacteriaˈ. African Journal of Microbiology Research, 4:1584-1593.

Duché, O., F. Trémoulet, P. Glaser and J. Labadie. 2002. ˈSalt stress proteins induced in Listeria monocytogenesˈ. Applied environmental microbiology, 68:1491-1498.

E. Beck, A., H. C. Bernstein and P. P. Carlson. 2017. ˈStoichiometric Network Analysis of Cyanobacterial Acclimation to Photosynthesis-Associated Stresses Identifies Heterotrophic Nichesˈ. Processes, 5:32; doi:10.3390/pr5020032.

Feierabend, J. and S. Engel. 1986. ˈPhotoinactivation of catalase in vitro and in leavesˈ. Archive Biochemistry Biophysics, 251:567.

Ferjani, A., L. Mustardy, R. Sulpice, K. Marin, I. Suzuki, M. Hagemann, and N. Murata. 2003. ˈGlucosylglycerol, a compatible solute, sustains cell division under salt stressˈ. Plant Physiology, 131:1628-1637.

Fischer, W.F. 2008. ˈLife before the rise of oxygenˈ. Nature, 455:1051-1052.

Fulda, S., S. Mikkat, F. Huang, J. Huckauf, K. Marin, B. Norling, and M. Hagemann. 2006. ˈProteome analysis of salt stress response in the cyanobacterium Synechocystis sp. strain PCC 6803ˈ. Proteomics, 6:2733-2745.

Gao, K., H. Yu, and M.T. Brown. 2007. ˈSolar PAR and UV radiation affect the physiology and morphology of the cyanobacterium Anabaena sp. PCC 7120ˈ. Journal of Photochemistry Photobiology B Biology, 89:117-124.

Giraldez-Ruiz, N., P. Mateo, I Bonilla and F. Fernandez-Pinas. 1997. ˈThe relationship between intracellular pH, growth characteristics and calcium in the cyanobacterium Anabaena sp. strain PCC7120 exposed to low pHˈ. New Phytologist, 137:599-605.

George, B., I. Pancha, C. Desai, K. Chokshi, C. Paliwal, T Ghosh, and S. Mishra. 2014. ˈEffects of different media composition, light intensity and photoperiod on morphology and physiology of freshwater microalgae Ankistrodesmusfalcatus – a potential strain for bio-fuel productionˈ. Bioresource Technology, 171:367-374.

Hagemann, M., R. Jeanjean, S. Fulda, M. Havaux, F. Joset, and N. Erdmann. 1999. ˈFlavodoxin accumulation contributes to enhanced cyclic electron flow around photosystem I in salt‐stressed cells of Synechocystis sp. strain PCC 6803ˈ. Physiologia Plantarum, 105:670-678.

Hagemann, M. 2011. ˈMolecular biology of cyanobacterial salt acclimationˈ. FEMS Microbiology Review, 35:87-123.

Halliwell, B., and J.M.C. Gutteridge. 1999. In: Halliwell, B., Gutteridge, J.M.C. (Eds.), Free Radicals in Biology and Medicine, third ed. Oxford, New York.

He, Y.Y. and D.P. Hader. 2002. ˈUV-B-induced formation of reactive oxygen species and oxidative damage of the cyanobacterium Anabaena sp.: protective effects of ascorbic acid and N-acetyl-L-cysteineˈ. Journal of Photochemistry and Photobiology B: Biology, 66:115-124.

He, Y.Y. and D.P. Hader. 2002. ˈReactive oxygen species and UV-B: effect on cyanobacteriaˈ. Photochemistry Photobiology Science, 1:729-736.

Horie, T., I. Karahara, and M. Katsuhara. 2012. ˈSalinity tolerance mechanisms in glycophytes: An overview with the central focus on rice plantsˈ. Rice, 5:11-29.

Illman, A.M., A.H. Scragg and S.W. Shales. 2000. ˈIncrease in Chlorella strains calorific values when grown in low nitrogen mediumˈ. Enzyme Microbiology Technology, 27:631-635.

Imlay, J.A. 2003. ˈPathways of oxidative damageˈ. Annual Review Microbiology, 57:395-418.

Inoue, N., Y. Taira, T. Emi, Y. Yamane, Y. Kashino, H. Koike and K. Satoh. 2001. ˈAcclimation to the growth temperature and the high-temperature effects on photosystem II and plasma membranes in a mesophilic cyanobacterium, Synechocystis sp. PCC6803ˈ. Plant and Cell Physiology, 42:1140-1148.

Jeanjean, R., H.C. Matthijs, B. Onana, M. Havaux, and F. Joset. 1993. ˈExposure of the cyanobacterium Synechocystis PCC6803 to salt stress induces concerted changes in respiration and photosynthesisˈ. Plant and cell physiology, 34:1073-1079.

Kallas, T. and R.W. Castenholz. 1982. ˈInternal pH and ATP-ADP pools in the cyanobacterium Synechococcus sp. during exposure to growth inhibiting low pHˈ. Journal of Bacteriology, 149:229-236.

Katoh, H., N. Hagino, A.R. Grossman and T. Ogawa. 2001. ˈGenes essential to iron transport in the cyanobacterium Synechocystis sp. strain PCC 6803ˈ. Journal of bacteriology, 183:2779-2784.

Kim, S.Y., Y. He, Y. Jacob, Y.S. Noh, S. Michaels, and R. Amasino. 2005. ˈEstablishment of the vernalization-responsive, winter-annual habit in Arabidopsis requires a putative histone H3 methyl transferaseˈ. The Plant Cell, 17:3301-3310.

Klähn, S., C. Steglich, W.R. Hess and M. Hagemann. 2010. ˈGlucosylglycerate: a secondary compatible solute common to marine cyanobacteria from nitrogen‐poor environmentsˈ. Environmental Microbiology, 12:83-94.

Kranzler, C., M. Rudolf, N. Keren, and E. Schleiff. 2013. ˈIron in cyanobacteriaˈ. Advance Botany Research, 65:57-105.

Ladas, N.P. and G.C. Papageorgiou. 2000. ˈCell turgor: A critical factor for the proliferation of cyanobacteria at unfavorable salinityˈ. Photosynthetic Research, 65:155-164.

Lesser, M.P. 2008. ˈEffects of ultraviolet radiation on productivity and nitrogen fixation in the cyanobacterium, Anabaena sp. (Newton’s strain) ˈ. Hydrobiology, 598:1-9.

Los, D.A., A. Zorina, M. Sinetova, S. Kryazhov, K. Mironov and V.V. Zinchenko. 2010. ˈStress sensors and signal transducers in cyanobacteriaˈ. Sensors, 10:2386-2415.

Lu, C. and A. Vonshak. 2002. ˈEffects of salinity on photosystem II function in cyanobacterial Spirulina platensis cellsˈ. Physiologia Plantarum, 114:405-413.

Lynn, S.G., S.S. Kilham, D.A. Kreeger, and S.J. Interlandi. 2000. ˈEffect of nutrient availability on the biochemical and elemental stoichiometry in freshwater diatom Stephanodiscusminutulus bacillariophyceaeˈ. Journal of Phycology, 36:510-522.

Mansilla, M.C., L.E. Cybulski, D. Albanesi and D. de Mendoza. 2004. ˈControl of membrane lipid fluidity by molecular thermosensorsˈ. Journal of bacteriology, 186:6681-6688.

Marin, K., I. Suzuki, K. Yamaguchi, K. Ribbeck, H. Yamamoto, Y. Kanesaki, M. Hagemann and N. Murata. 2003. ˈIdentification of histidine kinases that act as sensors in the perception of salt stress in Synechocystis sp. PCC 6803ˈ. Proceedings of the National Academy of Sciences, 100:9061-9066.

Marin, K., M. Stirnberg, M. Eisenhut, R. Krämer, and M. Hagemann. 2006. ˈOsmotic stress in Synechocystis sp. PCC 6803: low tolerance towards nonionic osmotic stress results from lacking activation of glucosylglycerol accumulationˈ. Microbiology, 152:2023-2030.

McKersie, B.D., and Y.Y. Leshem. 1994. ˈStress and Stress Coping in Cultivated Plantsˈ. Kluwer Academic Publishers, Dordrecht.

Meeks, J.C. and R.W. Castenholz. 1971. ˈGrowth and photosynthesis in an extreme thermophile, Synechococcus lividus (Cyanophyta)ˈ. Archive of Microbiology, 78:25-41.

Meloni, D.A., M.A. Oliva, C.A. Martinez, and J. Cambraia. 2003. ˈPhotosynthesis and activity of superoxide dismutase, peroxidase, and glutathione reductase in cotton under salt stressˈ. Environmental Experimental Botany, 49:69-76.

Mire, C.E., J.A. Tourjee, W.F. O’Brien, K.V. Ramanujachary and G.B. Hecht. 2004. ˈLead precipitation by Vibrio harveyi: evidence for novel quorum-sensing interactionsˈ. Applied Environmental Microbiology, 70:855-864.

Morgan-Kiss, R.M., J.C. Priscu, T. Pocock, L. Gudynaite-Savitch and N.P. Hunter. 2006. ˈAdaptation and acclimation of photosynthetic microorganisms to permanently cold environmentsˈ. Microbiology Molecular Biology Review, 70:222-252.

Murata, N. and D.A. Los. 1997. ˈMembrane fluidity and temperature perceptionˈ. Plant Physiology, 115:875-879.

Murata, N., H. Wada, and Z. Gombos. 1992. ˈModes of fatty-acid desaturation in cyanobacteriaˈ. Plant Cell Physiology, 33:933-941.

Murata, N. and H. Wada. 1995. ˈAcyl-lipid desaturases and their importance in the tolerance and acclimatization too cold of cyanobacteriaˈ. Biochemistry Journal, 308:1-8.

Nagalakshmi, N. and M.N.V. Prasad. 2001. ˈResponses of glutathione cycle enzymes and glutathione metabolism to copper stress in Scenedesmusbijugatusˈ. Plant Science, 160:291-299.

Neill, S., R. Desikan and J. Hancock. 2002. ˈHydrogen peroxide signalingˈ. Current Opinion Plant Biology, 5:388-395.

Ning, S.B., H.L. Guo, L. Wang, and Y.C. Song. 2002. ˈSalt stress induces programmed cell death in prokaryotic organism Anabaenaˈ. Journal of Applied Microbiology, 93:15-28.

Nishida, I. and N. Murata. 1996. ˈChilling sensitivity in plants and cyanobacteria: The crucial contribution of membrane lipidsˈ. Annual Review Plant Physiology Plant Molecular Biology, 47:541.

Nissen, P., J. Hansen, N. Ban, P.B. Moore, and T.A. Steitz. 2000. ˈThe structural basis of ribosome activity in peptide bond synthesisˈ. Science, 289:920-930.

Niyogi, K.K. 1999. ˈPhotoprotection revisited: genetics and molecular approachesˈ. Annual Review Plant Physiology, 50:333-359.

Noctor, G. and C.H. Foyer. 1998. ˈAscorbate and glutathione: keeping active oxygen under controlˈ. Annual Review Plant Physiology Plant Molecular Biology, 49:249-279.

Paliwal, C., M. Mitra, K. Bhayani, S.V.V. Bharadwaj, T. Ghosh, S. Dubey, and S. Mishra. 2017. ˈAbiotic stresses as tools for metabolites in microalgaeˈ. Bioresource Technology, 244:1216-1226.

Psenner, R. and B. Sattler. 1998. ˈLife at the freezing pointˈ. Science, 280:2073-2074.

Pulz, O. and W. Gross. 2004. ˈValuable products from biotechnology of microalgaeˈ. Applied Microbiology Biotechnology, 65:635-648.

Priya, B., J. Premanandh, R.T. Dhanalakshmi, T. Seethalakshmi, L. Uma, D. Prabaharan and G. Subramanian. 2007. ˈComparative analysis of cyanobacterial superoxide dismutases to discriminate canonical formsˈ. BMC Genomics, 8:435.

Priya, B., R.K. Sivaprasanth, V.D. Jensi, L. Uma, G. Subramanian and D. Prabaharan. 2010. ˈCharacterization of manganese superoxide dismutase from a marine cyanobacterium Leptolyngbya valderiana BDU20041ˈ. Saline System, 6, http://dx.doi.org/10.1186/1746-1448-6-6.

Quesada, A. and W.F. Vincent. 1997. ˈStrategies of adaptation by Antarctic cyanobacteria to ultraviolet radiationˈ. European Journal of Phycology, 32:335-342.

Rastogi, R.P. and R.P. Sinha. 2009. The ˈBiotechnological and industrial significance of cyanobacterial secondary metabolitesˈ. Biotechnology Advance, 27:521-539.

Rastogi, R.P. and R.P. Sinha. 2011. ˈSolar ultraviolet radiation-induced DNA damage and protection/repair strategies in cyanobacteriaˈ. International Journal Pharma and Bio Science, 2:271-288.

Reed, R.H., L.J. Borowitzka, M.A. Mackay, J.A. Chudek, R. Foster, S.R.C. Warr, D.J. Moore, and W.D.P. Stewart. 1986. ˈOrganic solute accumulation in osmotically stressed cyanobacteriaˈ. FEMS Microbiology Letter, 39:51-56.

Reed, R.H. and W.D.P. Stewart. 1988. ˈThe response of cyanobacteria to salt stressˈ. In Biochemistry of the Algae and Cyanobacteria, Roger, L. J., and Gallon, J. R. (Eds.). Oxford University Press, Oxford, U.K., pp. 217–231.

Reynolds, C.S., R.L. Oliver and A.E. Walsby. 1987. ˈCyanobacterial dominance: the role of buoyancy regulation in dynamic lake environmentsˈ. N Z Journal Marin Freshwater Research, 21:379-390.

Roberts, M.F. 2005. ˈOrganic compatible solutes of halotolerant and halophilic microorganismsˈ. Saline System, 1:5.

Sato, N. 1995. ˈA family of cold-regulated RNA-binding protein genes in the cyanobacterium Anabaena variabilis M3ˈ. Nucleic Acids Research, 23:2161-2167.

Schuliger, J.W., S.H. Brown, J.A. Baross and R.M. Kelly. 1993. ˈPurification and characterization of a novel amylolytic enzyme from ES 4, a marine Hyperthermophilic archaeumˈ. Molecular Marin Biology Biotechnology, 2:76-87.

Saha, J., E.K. Brauer, A. Sengupta, S.C. Popescu, K. Gupta and B. Gupta. 2015. ˈPolyamines as redox homeostasis regulators during salt stress in plantsˈ. Frontiers in Environmental Science, 3:21-34.

Singh, S.C., R.P. Sinha, and D.P. Hader. 2002. ˈRole of lipid and fatty acids in stress tolerance in cyanobacteriaˈ. Acta Protozoology, 41:297-308.

 Singh, S.V.P., P.K. Srivastava and S.M. Prasad. 2011. ˈDifferential physiological and biochemical responses of two cyanobacteria Nostoc muscorum and Phormidium foveolarum against oxyfluorfen and UV-B radiationˈ. Ecotoxicology Environmental Safety, 74:1981-1993.

Sinha, R.P. and D.P. Hader. 2008. ˈUV-protectants in cyanobacteriaˈ. Plant Science, 174:278-289.

Sinha, R.P., M. Lebert, A. Kumar, H.D. Kumar, and D.P. Hader. 1995. ˈDisintegration of phycobilisomes in a rice field cyanobacterium Nostoc sp. following UV irradiationˈ. Biochemistry Molecular Biology International, 37:697-706.

Sinha, R.P., R.P. Rastogi, N.K. Ambasht and D.P. Hader. 2008. ˈLife of wetland cyanobacteria under enhancing solar UV-B radiationˈ. Proceeding Natation Academy Science India, 78:53-65.

Sinetova, M.A. and D.A. Los. 2016. ˈNewinsights in cyanobacterial cold stress responses: Genes, sensors, and molecular triggersˈ. Biochemistry Biophysics Acta, 1860:2391-2403.

Singh, S.P., D.P. Häder, and R.P. Sinha. 2010. ˈCyanobacteria and ultraviolet radiation (UVR) stress: mitigation strategiesˈ. Age Research Review, 9:79-90.

Slabas, A.R., I. Suzuki, N. Murata, W.J. Simon, and J.J. Hall. 2006. ˈProteomic analysis of the heat shock response in Synechocystis PCC6803 and a thermally tolerant knockout strain lacking the histidine kinase 34 geneˈ. Proteomics, 6:845-864.

Sørensen, L., A. Hantke and N.T. Eriksen. 2013. ˈPurification of the photosynthetic pigment C-Phycocyanin from heterotrophic Galdieria sulphurariaˈ. Journal of Science Food Agriculture, 93:2933-2938.

Srivastava, A.K., P. Bhargava and L.C. Rai. 2005. ˈSalinity and copper-induced oxidative damage and changes in antioxidative defense system of Anabaena doliolumˈ. World Journal Microbiology Biotechnology, 22:1291.

Srivastava, A.K., P. Bhargava and L.C. Rai. 2008. ˈA physiological and proteomic analysis of salinity-induced changes in Anabaena doliolumˈ. Environmental and Experimental Botany, 64: 49-57.

Stanier, R.Y. and G. Cohen-Bazire. 1977. ˈPhototrophic prokaryotes: the cyanobacteriaˈ. Annual Review Microbiology, 31:225-274.

Stumn, W. and J.J. Morgan. 1981. ˈAquatic chemistryˈ. 2nd ed. New York: Wiley.

Tasaka, Y., Z. Gombos, Y. Nishiyama, P. Mohanty, T. Ohba, K. Ohki, and N. Murata. 1996. ˈTargeted mutagenesis of acyl-lipid desaturases in Synechocystis: evidence for the important roles of polyunsaturated membrane lipids in growth, respiration, and photosynthesisˈ. The EMBO Journal, 15:6416-6425.

Tchounwou, P.B., C.G. Yedjou, A.K. Patlolla, and D.J. Sutton. 2012. ˈHeavy metal toxicity and the environmentˈ. Molecular Clinical Environmental Toxicology, 101:133-164.

Tijen, D. and T. Ismail. 2006. ˈExogenous glycinebetaine affects growth and proline accumulation and retards senescence in two rice cultivars under NaCl stressˈ. Environmental Experimental Botany, 56:72-79.

Torok, Z., P. Goloubinoff, I. Horvath, N.M. Tsvetkova, A. Glatz, G. Balogh, V. Varvasovszki, D.A. Los, E. Vierling, J.H. Crowe  and L. Vigh. 2001. ˈSynechocystis HSP17 is an amphitropic protein that stabilizes heat-stressed membranes and binds denatured proteins for subsequent chaperone-mediated refoldingˈ. Proceeding Natation Academy Science, 98:3098-3103.

Vaishampayan, A., R.P. Sinha, D.P. Hader, T. Dey, A.K. Gupta, U. Bhan, and A.L. Rao. 2001. ˈCyanobacterial biofertilizers in rice agricultureˈ. The Botany Review, 67:453-516.

Van Thor, J.J., R. Jeanjean, M. Havaux, K.A. Sjollema, F. Joset, K.J. Hellingwerf, and H.C. Matthijs. 2000. ˈSalt shock-inducible photosystem I cyclic electron transfer in Synechocystis PCC6803 relies on binding of ferredoxin: NADP⁺ reductase to the thylakoid membranes via its CpcD phycobilisome-linker homologous N-terminal domainˈ. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1457:129-144.

Verschooten, L., S. Claerhout, A.V. Laethemii, P. Agostinis, and M. Garmyn. 2006. ˈNew strategies of photoprotectionˈ. Photochemistry Photobiology, 82:1016-1023.

Wada, H., Z. Gombos and N. Murata. 1990. ˈEnhancement of chilling tolerance of a cyanobacterium by genetic manipulation of fatty acid desaturationˈ. Nature, 347:200-203.

Ward, D.M., M.J. Ferris, S.C. Nold and M.M. Bateson. 1998. ˈA natural view of microbial biodiversity within hot spring cyanobacterial mat communitiesˈ. Microbiology Molecular Biology Review, 62:1353-1370.

Walsby, A.E. 1982. ˈCell-water and cell-solute relationsˈ. In: Carr NG, Whitton BA, editors. The biology of cyanobacteria, Oxford: Blackwell Science Publications; p. 237-262.

Wang, Z., D. Li, G. Li, and Y. Liu. 2010. ˈMechanism of photosynthetic response in Microcystis aeruginosa PCC 7806 to low inorganic phosphorusˈ. Harmful Algae, 9:613-619.

Wang, B., J. Wang, W. Zhang, and D.R. Meldrum. 2012. ˈApplication of synthetic biology in cyanobacteria and algaeˈ. Front Microbiology,3:344.doi:10.3389/fmicb.2012.00344

Weisburd, S. 1988. ˈDeath-defying dehydrationˈ. Science News, 13:107-110.

Whitton, B.A. and M. Potts. 2000. ˈThe Ecology of Cyanobacteria: Their Diversity in Time and Spaceˈ, Kluwer Academic Publishers, Dordrecht, the Netherlands, pp. 669.

Xie, Z., Y. Wang, Y. Liu, and Y. Liu. 2009. ˈUltraviolet-B exposure induces photooxidative damage and subsequent repair strategies in a desert cyanobacterium Microcoleus vaginatusˈ. European Journal of Soil Biology, 45:377-382.

Xu, J., Y.S. Tian, R.H. Peng, A.S. Xiong, B. Zhu, X.L. Hou, and Q.H. Yao. 2010. ˈCyanobacteria MT gene SmtA enhance zinc tolerance in Arabidopsisˈ. Molecular biology report, 37:1105.

Ybarra, G. and R. Webb. 1999. ˈEffects of divalent metal cations and resistance mechanisms of the Cyanobacterium Synechococcus sp. strain PCC 7942ˈ. Journal of Hazard Substance Research, 2:1-9.

Zamocky, M., P.G. Furtmüller and C. Obinger. 2008. ˈEvolution of catalases from bacteria to humansˈ. Antioxidant Redox Signal, 10:1527-1548.

Zhu, J.K. 2001. ˈPlant salt toleranceˈ. Trends Plant Science, 6:66-71.