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Volume 161, Issue 7

Deciphering the mechanisms against oxidative stress in developing and mature akinetes of the cyanobacterium Free

Abstract

Cells of filamentous cyanobacteria of the orders and can differentiate into dormant forms called akinetes. Akinetes play a key role in the survival, abundance and distribution of the species, contributing an inoculum for their perennial blooms. In the cyanobacterium potassium deficiency triggers the formation of akinetes. Here we present experimental evidence for the production of reactive oxygen species (ROS) during akinete development in response to potassium deficiency. The function of ROS as a primer signal for akinete differentiation was negated. Nevertheless, akinetes acquired protective mechanisms against oxidative damage during their differentiation and maintained them as they matured, giving akinetes advantages enabling survival in harsh conditions.

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© 2015 The Authors
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2015-07-01
2024-04-18
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References

  1. Adams D.G., Duggan P.S. (1999). Heterocyst and akinete differentiation in cyanobacteriaNew Phytol 1443–33 [View Article]. [Google Scholar]
  2. Aguirre J., Ríos-Momberg M., Hewitt D., Hansberg W. (2005). Reactive oxygen species and development in microbial eukaryotesTrends Microbiol 13111–118 [View Article][PubMed]. [Google Scholar]
  3. Alahari A., Apte S.K. (1998). Pleiotropic effects of potassium deficiency in a heterocystous, nitrogen-fixing cyanobacterium, Anabaena torulosa Microbiology 1441557–1563 [View Article][PubMed]. [Google Scholar]
  4. Bailly C. (2004). Active oxygen species and antioxidants in seed biologySeed Sci Res 1493–107 [View Article]. [Google Scholar]
  5. Bailly C., Audigier C., Ladonne F., Wagner M.H., Coste F., Corbineau F., Côme D. (2001). Changes in oligosaccharide content and antioxidant enzyme activities in developing bean seeds as related to acquisition of drying tolerance and seed qualityJ Exp Bot 52701–708[PubMed]. [Google Scholar]
  6. Bailly C., El-Maarouf-Bouteau H., Corbineau F. (2008). From intracellular signaling networks to cell death: the dual role of reactive oxygen species in seed physiologyC R Biol 331806–814 [View Article][PubMed]. [Google Scholar]
  7. Banker R., Carmeli S., Hadas O., Teltsch B., Porat R., Sukenik A. (1997). Identification of cylindrospermopsin in Aphanizomenon ovalisporum (Cyanophyceae) isolated from Lake KinneretIsrael. J Phycol 33613–616 [View Article]. [Google Scholar]
  8. Baxter A., Mittler R., Suzuki N. (2014). ROS as key players in plant stress signallingJ Exp Bot 651229–1240 [View Article][PubMed]. [Google Scholar]
  9. Beauchamp C., Fridovich I. (1971). Superoxide dismutase: improved assays and an assay applicable to acrylamide gelsAnal Biochem 44276–287 [View Article][PubMed]. [Google Scholar]
  10. Bernroitner M., Zamocky M., Furtmüller P.G., Peschek G.A., Obinger C. (2009). Occurrence, phylogeny, structure, and function of catalases and peroxidases in cyanobacteriaJ Exp Bot 60423–440 [View Article][PubMed]. [Google Scholar]
  11. Buettner G.R., Jurkiewicz B.A. (1996). Catalytic metals, ascorbate and free radicals: combinations to avoidRadiat Res 145532–541 [View Article][PubMed]. [Google Scholar]
  12. Cabiscol E., Tamarit J., Ros J. (2000). Oxidative stress in bacteria and protein damage by reactive oxygen speciesInt Microbiol 33–8[PubMed]. [Google Scholar]
  13. Checchetto V., Segalla A., Allorent G., La Rocca N., Leanza L., Giacometti G.M., Uozumi N., Finazzi G., Bergantino E., Szabò I. (2012). Thylakoid potassium channel is required for efficient photosynthesis in cyanobacteriaProc Natl Acad Sci U S A 10911043–11048 [View Article][PubMed]. [Google Scholar]
  14. Checchetto V., Teardo E., Carraretto L., Formentin E., Bergantino E., Giacometti G.M., Szabo I. (2013). Regulation of photosynthesis by ion channels in cyanobacteria and higher plantsBiophys Chem 18251–57 [View Article][PubMed]. [Google Scholar]
  15. Chow W.S., Wagner G., Hope A.B. (1976). Light-dependent redistribution of ions in isolated spinach chloroplastsAustral J Plant Physiol 3853–861.[CrossRef] [Google Scholar]
  16. Claessen D., Rozen D.E., Kuipers O.P., Søgaard-Andersen L., van Wezel G.P. (2014). Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodiesNat Rev Microbiol 12115–124 [View Article][PubMed]. [Google Scholar]
  17. D'Autréaux B., Toledano M.B. (2007). ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasisNat Rev Mol Cell Biol 8813–824 [View Article][PubMed]. [Google Scholar]
  18. Dietz K.J. (2011). Peroxiredoxins in plants and cyanobacteriaAntioxid Redox Signal 151129–1159 [View Article][PubMed]. [Google Scholar]
  19. Dilley R.A., Vernon L.P. (1965). Ion and water transport processes related to the light-dependent shrinkage of spinach chloroplastsArch Biochem Biophys 111365–375 [View Article][PubMed]. [Google Scholar]
  20. Fang G.-C., Hanau R.M., Vaillancourt L.J. (2002). The SOD2 gene, encoding a manganese-type superoxide dismutase, is up-regulated during conidiogenesis in the plant-pathogenic fungus Colletotrichum graminicola Fungal Genet Biol 36155–165 [View Article][PubMed]. [Google Scholar]
  21. Fay P. (1969). Metabolic activities of isolated spores of Anabaena cylindrica J Exp Bot 20100–109 [View Article]. [Google Scholar]
  22. Gapper C., Dolan L. (2006). Control of plant development by reactive oxygen speciesPlant Physiol 141341–345 [View Article][PubMed]. [Google Scholar]
  23. Goldberg I., Hochman A. (1989). Purification and characterization of a novel type of catalase from the bacteriumKlebsiella pneumoniae. Biochim Biophys Acta 991330–336.[CrossRef] [Google Scholar]
  24. Halliwell B. (1996). Vitamin C: antioxidant or pro-oxidant in vivo?Free Radic Res 25439–454 [View Article][PubMed]. [Google Scholar]
  25. Hansberg W., Aguirre J., Rís-Momberg M., Rangel P., de Peraza L. (2008). Cell differentiation as a response to oxidative stress., ch. 15. In Stress in Yeast and Filamentous Fungi, pp. 235–257. Edited by Avery S. V., Stratford M., Van West P. Br Mycol Soc Symp Ser vol. 27LondonElsevier [View Article]. [Google Scholar]
  26. Hense I., Beckmann A. (2006). Towards a model of cyanobacteria life cycle—effects of growing and resting stages on bloom formation of N2-fixing speciesEcol Modell 195205–218 [View Article]. [Google Scholar]
  27. Joliot P., Johnson G.N. (2011). Regulation of cyclic and linear electron flow in higher plantsProc Natl Acad Sci U S A 10813317–13322 [View Article][PubMed]. [Google Scholar]
  28. Kaplan-Levy R., Hadas O., Summers M., Rücker J., Sukenik A. (2010). Akinetes: dormant cells of cyanobacteria. In Dormancy and Resistance in Harsh Environments, pp. 5–27. Edited by Lubzens E., Cerda J., Clark M. Topics Curr Genet vol. 21BerlinSpringer [View Article]. [Google Scholar]
  29. Kesheri M., Richa, Sinha R.P. (2011). Antioxidants as natural arsenal against multiple stresses in cyanobacteriaInt J Pharm Bio Sci 2168–187. [Google Scholar]
  30. Kramer D.M., Cruz J.A., Kanazawa A. (2003). Balancing the central roles of the thylakoid proton gradientTrends Plant Sci 827–32 [View Article][PubMed]. [Google Scholar]
  31. Latifi A., Ruiz M., Zhang C.C. (2009). Oxidative stress in cyanobacteriaFEMS Microbiol Rev 33258–278 [View Article][PubMed]. [Google Scholar]
  32. Leymarie J., Vitkauskaité G., Hoang H.H., Gendreau E., Chazoule V., Meimoun P., Corbineau F., El-Maarouf-Bouteau H., Bailly C. (2012). Role of reactive oxygen species in the regulation of Arabidopsis seed dormancyPlant Cell Physiol 5396–106 [View Article][PubMed]. [Google Scholar]
  33. Maldener I., Summers M.L., Sukenik A. (2014). Cellular differentiation in filamentous cyanobacteria. In The Cell Biology of Cyanobacteria, pp. 263–292. Edited by Flores E., Herrero A. WymondhamCaister Academic Press. [Google Scholar]
  34. Malinska D., Mirandola S.R., Kunz W.S. (2010). Mitochondrial potassium channels and reactive oxygen speciesFEBS Lett 5842043–2048 [View Article][PubMed]. [Google Scholar]
  35. Mittler R., Vanderauwera S., Suzuki N., Miller G., Tognetti V.B., Vandepoele K., Gollery M., Shulaev V., Van Breusegem F. (2011). ROS signaling: the new wave?Trends Plant Sci 16300–309 [View Article][PubMed]. [Google Scholar]
  36. Navarro R.E., Stringer M.A., Hansberg W., Timberlake W.E., Aguirre J. (1996). catA, A new Aspergillus nidulans gene encoding a developmentally regulated catalaseCurr Genet 29352–359[PubMed]. [Google Scholar]
  37. Perelman A., Uzan A., Hacohen D., Schwarz R. (2003). Oxidative stress in Synechococcus sp. strain PCC 7942: various mechanisms for H2O2 detoxification with different physiological rolesJ Bacteriol 1853654–3660 [View Article][PubMed]. [Google Scholar]
  38. Pfeil B.E., Schoefs B., Spetea C. (2014). Function and evolution of channels and transporters in photosynthetic membranesCell Mol Life Sci 71979–998[PubMed].[CrossRef] [Google Scholar]
  39. Pluthero F.G. (1993). Rapid purification of high-activity Taq DNA polymeraseNucleic Acids Res 214850–4851 [View Article][PubMed]. [Google Scholar]
  40. Rastogi R.P., Singh S.P., Häder D.P., Sinha R.P. (2010). Detection of reactive oxygen species (ROS) by the oxidant-sensing probe 2′,7′-dichlorodihydrofluorescein diacetate in the cyanobacterium Anabaena variabilis PCC 7937Biochem Biophys Res Commun 397603–607 [View Article][PubMed]. [Google Scholar]
  41. Rippka R., Deruelles J., Waterbury J.B., Herdman M., Stanier R.Y. (1979). Generic assignments, strain histories and properties of pure cultures of cyanobacteriaJ Gen Microbiol 1111–61 [View Article]. [Google Scholar]
  42. Sambrook J., Russell D.W. (2001). Molecular Cloning: a Laboratory Manual3rd ednCold Spring Harbor, NY: Cold Spring Harbor Laboratory Press. [Google Scholar]
  43. Samuilov V.D., Timofeev K.N., Sinitsyn S.V., Bezryadnov D.V. (2004). H2O2-induced inhibition of photosynthetic O2 evolution by Anabaena variabilis cellsBiochemistry (Mosc) 69926–933 [View Article][PubMed]. [Google Scholar]
  44. Schwarz R., Forchhammer K. (2005). Acclimation of unicellular cyanobacteria to macronutrient deficiency: emergence of a complex network of cellular responsesMicrobiology 1512503–2514 [View Article][PubMed]. [Google Scholar]
  45. Seaver L.C., Imlay J.A. (2001). Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli J Bacteriol 1837173–7181 [View Article][PubMed]. [Google Scholar]
  46. Simon R. (1987). Inclusion bodies in the cyanobacteria: cyanophycin, polyphosphate, polyhedral bodies. In The Cyanobacteria, pp. 199–225. Edited by Fay P., van Baalen C. AmsterdamElsevier. [Google Scholar]
  47. Stanier R.Y., Kunisawa R., Mandel M., Cohen-Bazire G. (1971). Purification and properties of unicellular blue-green algae (order Chroococcales)Bacteriol Rev 35171–205[PubMed]. [Google Scholar]
  48. Sukenik A., Beardall J., Hadas O. (2007). Photosynthetic characterization of developing and mature akinetes of Aphanizomenon ovalisporum (Cyanoprokaryota)J Phycol 43780–788 [View Article]. [Google Scholar]
  49. Sukenik A., Kaplan-Levy R.N., Welch J.M., Post A.F. (2012). Massive multiplication of genome and ribosomes in dormant cells (akinetes) of Aphanizomenon ovalisporum (Cyanobacteria)ISME J 6670–679 [View Article][PubMed]. [Google Scholar]
  50. Sukenik A., Kaplan-Levy R.N., Viner-Mozzini Y., Quesada A., Hadas O. (2013). Potassium deficiency triggers the development of dormant cells (akinetes) in Aphanizomenon ovalisporum (Nostocales, Cyanoprokaryota)J Phycol 49580–587 [View Article]. [Google Scholar]
  51. Utermöhl H. (1958). Perfecting quantitative phytoplankton methodologies.Mitt int Ver theor angew Limnol 91–38. [Google Scholar]
  52. Weissman L., Garty J., Hochman A. (2005). Characterization of enzymatic antioxidants in the lichen Ramalina lacera and their response to rehydrationAppl Environ Microbiol 716508–6514 [View Article][PubMed]. [Google Scholar]
  53. Zhao W., Ye Z., Zhao J. (2007). RbrA, a cyanobacterial rubrerythrin, functions as a FNR-dependent peroxidase in heterocysts in protection of nitrogenase from damage by hydrogen peroxide in Anabaena sp. PCC 7120Mol Microbiol 661219–1230 [View Article][PubMed]. [Google Scholar]
  54. Zhou R., Wolk C.P. (2002). Identification of an akinete marker gene in Anabaena variabilis J Bacteriol 1842529–2532 [View Article][PubMed]. [Google Scholar]
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Deciphering the mechanisms against oxidative stress in developing and mature akinetes of the cyanobacterium Aphanizomenon ovalisporum
Microbiology 161, 1485 (2015); https://doi.org/10.1099/mic.0.000101
/content/journal/micro/10.1099/mic.0.000101
/content/journal/micro/10.1099/mic.0.000101
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