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Physiological and Proteomic Studies of the Cyanobacterium Anabaena sp. Acclimated to Desiccation Stress

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Abstract

Agricultural productivity is threatened by increasing incidence of drought and the drought tolerant cyanobacteria offer a better solution in the restoration of soil fertility and productivity. The present study describes the comparative physiological response of the cyanobacterium Anabaena sp. acclimated and un-acclimated to desiccation stress induced by polyethylene glycol (10% PEG). While, the acclimated cyanobacterial cells grew luxuriantly with optimal chlorophyll content, photosynthetic activities and nitrogen fixation, the un-acclimated cells exhibited reduced growth rate, chlorophyll content, photosynthetic activities and nitrogen fixation. Distinct differences in the accumulation of lipid peroxidation products, proline and activity of superoxide dismutase were observed under identical growth conditions in the acclimated and un-acclimated cells. Desiccation-acclimated and un-acclimated cyanobacteria showed significant alterations in the abundance of important proteins in the proteome. Two-dimensional gel electrophoresis followed by MALDI-TOF–MS/MS analysis identified twelve proteins. The acclimated cells showed the up regulation of proteins such as Rubisco, fructose-bis-phosphate aldolase, fructose 1–6 bisphosphatase, phosphoglycerate dehydrogenase and elongation factors Tu and Ts as compared to un-acclimated cells. Therefore, the ability to maintain photosynthesis, antioxidants and increased accumulation of proteins related to energy metabolism helped the acclimated cyanobacterium Anabaena sp. to grow optimally under desiccation stress conditions.

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References

  1. Lan SB, Wu L, Zhang DL (2010) Effects of drought and salt stresses on man-made cyanobacterial crusts. Eur J Soil Biol 46:381–386

    Google Scholar 

  2. Makhalanyane TP, Valverde A, Gunnigle E, Frossard A, Ramond JB, Cowan DA (2015) Microbial ecology of hot desert edaphic systems. FEMS Microbiol Rev 39(2):203–221. https://doi.org/10.1093/femsre/fuu011

    Article  CAS  PubMed  Google Scholar 

  3. Ullah A, Sun H, Yang X, Zhang X (2017) Drought coping strategies in cotton: increased crop per drop. Plant Biotechnol J 15(3):271–284

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Pennisi E (2008) The blue revolution, drop by drop, gene by gene. Science 320(5873):171–173

    CAS  PubMed  Google Scholar 

  5. Stanier RY, Cohen-Bazire G (1977) Phototrophic prokaryotes: the cyanobacteria. Annu Rev Microbiol 31(1):225–274

    CAS  PubMed  Google Scholar 

  6. Hegde DM, Dwivedi BS, Sudhakara SN (1999) Biofertilizers for cereal production in India: a review. Ind J Agri Sci 69(2):73–83

    Google Scholar 

  7. Venkataraman GS (1972) Algal Biofertilizers and Rice Cultivation. Today and tomorrow Printers and Publishers, New Delhi

    Google Scholar 

  8. Dubey AK, Rai AK (1995) Application of algal biofertilizers (Aulosira fertilissima var tenius and Anabaena doliolum Bhardwaja) for sustained paddy cultivation in Northern India. Isr J Plant Sci 43(1):41–51

    Google Scholar 

  9. Cameron HJ, Julian GR (1988) Utilization of hydroxyapatite by cyanobacteria as their sole source of phosphate and calcium. Plant Soil 109(1):123–124

    CAS  Google Scholar 

  10. Sen S, Rai S, Yadav S et al (2017) Dehydration and rehydration-induced temporal changes in cytosolic and membrane proteome of the nitrogen fixing cyanobacterium Anabaena sp. PCC 7120. Algal Res 27:244–258

    Google Scholar 

  11. Park CH, Li XR, Zhao Y, Jia RL, Hur JS (2017) Rapid development of cyanobacterial crust in the field for combating desertification. PLoS ONE 12(6):e0179903. https://doi.org/10.1371/journal.pone.0179903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Cattivelli L, Rizza F, Badeck FW et al (2008) Drought tolerance improvement in crop plants: an integrative view from breeding to genomics. Field Crop Res 105(1–2):1–14

    Google Scholar 

  13. Potts M (2000) Nostoc. In: Whitton BA, Potts M (eds) The Ecology of Cyanobacteria. Springer, Dordrecht, pp 465–504

    Google Scholar 

  14. Olie JJ, Potts M (1986) Purification and biochemical analysis of the cytoplasmic membrane from the desiccation-tolerant cyanobacterium Nostoc commune UTEX 584. Appl Environ Microbiol 52(4):706–710

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Liang W, Zhou Y, Wang L et al (2012) Ultrastructural physiological and proteomic analysis of Nostoc flagelliforme in response to dehydration and rehydration. J Proteomics 75(18):5604–5627

    CAS  PubMed  Google Scholar 

  16. Rippka R, Deruelles J, Waterbury JB, Herdman M, Stanier RY (1979) Genetic assignments, strain histories and properties of pure culture of cyanobacteria. Microbiology 111(1):1–61

    Google Scholar 

  17. Codd GA, Cook CM, Stewart WDP (1979) Purification and subunit structure of D-ribulose 1, 5-bisphosphate carboxylase from the cyanobacterium Aphanothece halophytica. FEMS Lett 6(2):81–86

    CAS  Google Scholar 

  18. Kaushik BD (1987) Laboratory methods for blue green algae. Associated Publishing Company, New Delhi

    Google Scholar 

  19. Desikachary TV (1959) Cyanophyta, vol 2. Indian Council of Agricultural Research, New Delhi

    Google Scholar 

  20. Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoxidase in Beta vulgaris Plant Physiol 24:1–15

    CAS  PubMed  Google Scholar 

  21. Mackinney G (1941) Absorption of light by chlorophyll solutions. J Biol Chem 140(2):315–322

    CAS  Google Scholar 

  22. Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiol Plant 83(3):463–468

    CAS  Google Scholar 

  23. Giannopolitis CN, Ries SK (1977) Superoxide dismutase I. Occurr High Plants Plant Physiol 59(2):309–314

    CAS  Google Scholar 

  24. Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39(1):205–207

    CAS  Google Scholar 

  25. Swapnil P, Singh M, Singh S, Sharma NK, Rai AK (2015) Recombinant glycinebetaine improves metabolic activities, ionic balance and salt tolerance in diazotrophic fresh water cyanobacteria. Algal Res 11:194–203

    Google Scholar 

  26. Stewart WDP, Fitzgerald GP, Burris RH (1968) Acetylene reduction by nitrogen-fixing blue- green algae. Arch Microbiol 62(4):336–348

    CAS  Google Scholar 

  27. Isaacson T, Damasceno CMB, Saravanan RS et al (2006) Sample extraction techniques for enhanced proteomic analysis of plant tissues. Nat Protoc 1(2):769–774

    CAS  PubMed  Google Scholar 

  28. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72(12):248–254

    CAS  Google Scholar 

  29. Shevchenko A, Tomas H, Havli J, Olsen JV, Mann M (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protocols 1(6):2856–2860

    CAS  PubMed  Google Scholar 

  30. Khandelwal A, Narayanan N, Varghese E, Gupta S (2020) Linear and nonlinear isotherm models and error analysis for the sorption of kresoxim-methyl in agricultural soils of India. Bull Environ Contam Toxicol 104:503–510

    CAS  PubMed  Google Scholar 

  31. Walters C, Farrant JM, Pammenter NW, Berjak P (2002) Drying without dying. In: Pritchard HW, Black M (eds) Desiccation stress and damage in Desiccation and survival in plants. CABI Publishing, New York, pp 263–291

    Google Scholar 

  32. Lan S, Zhang Q, Wu L, Liu Y, Zhang D, Hu C (2014) Artificially accelerating the reversal of desertification: cyanobacterial inoculation facilitates the succession of vegetation communities. Environ Sci Technol 48(1):307–315

    CAS  PubMed  Google Scholar 

  33. Swapnil P, Rai AK (2018) Physiological responses to salt stress of salt-adapted and directly salt (NaCl and NaCl+Na2SO4 mixture)-stressed cyanobacterium Anabaena fertilissima. Protoplasma 255(3):963–976

    CAS  PubMed  Google Scholar 

  34. Hagemann M, Erdmann N, Schiewer U (1989) Salt adaptation of the cyanobacterium Microcystis firma and Synechocystis aquatilis in turbidostat cultures I Steady state values. Archiv für Hydrobiol Suppl Monogr Beitr 82(4):425–435

    Google Scholar 

  35. Gao K, Ye CP (2007) Photosynthetic insensitivity of the terrestrial cyanobacterium Nostoc flagelliforme to solar UV radiation while rehydrated or desiccated. J Phycol 43(4):628–635

    CAS  Google Scholar 

  36. Kirilovsky D, Kerfeld CA (2012) The orange carotenoid protein in photoprotection of photosystem II in cyanobacteria. Biochem Biophys Acta Bioenerg 1817(1):158–166

    CAS  Google Scholar 

  37. Lin CS, Wu JT (2014) Tolerance of soil algae and cyanobacteria to drought stress. J Phycology 50(1):131–139

    CAS  PubMed  Google Scholar 

  38. Tang D, Shi S, Li D, Hu C, Liu Y (2007) Physiological and biochemical responses of Scytonema javanicum (cyanobacterium) to salt stress. J Arid Environ 71(3):312–320

    Google Scholar 

  39. Abd El-Baky H, El Baz HFK, El-Baroty GS (2004) Production of antioxidant by the green alga Dunaliella salina. Int J Agric Biol 6:49–57

    CAS  Google Scholar 

  40. Bose J, Rodrigo-Moreno A, Shabala S (2014) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65(5):1241–1257

    CAS  PubMed  Google Scholar 

  41. Chaneva G, Pilarski P, Petrova DH (2011) Changes of proline content in a cyanobacterium under oxidative stress. Oxid Commun 34(2):439–445

    CAS  Google Scholar 

  42. Zhou C, Ma Z, Zhu L et al (2016) Rhizobacterial strain Bacillus megaterium BOFC15 induces cellular polyamine changes that improve plant growth and drought resistance. Int J Mol Sci 17(6):976

    PubMed Central  Google Scholar 

  43. van Rensburg L, Krüger GHJ (1993) Differential Inhibition of photosynthesis (in vivo and in vitro) and changes in chlorophyll a fluorescence induction kinetics of four tobacco cultivars under drought Stress. J Plant Physiol 141(3):357–365. https://doi.org/10.1016/S0176-1617(11)81748-7

    Article  Google Scholar 

  44. Pinheiro C, Chaves MM (2011) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62(3):869–882

    CAS  PubMed  Google Scholar 

  45. Flameling IA, Kromkamp J (1994) Responses of respiration and photosynthesis of Scenedesmus protuberans Fritsch to gradual and steep salinity increases. J Plankton Res 16(12):1781–1791

    Google Scholar 

  46. Lu C, Vonshak A (1999) Characterization of PS II photochemistry in salt-adapted cells of cyanobacterium Spirulina platensis. New Phytol 141(2):231–239

    CAS  PubMed  Google Scholar 

  47. Zeng MT, Vonshak A (1998) Adaptation of Spirulina platensis to salinity-stress. Comp Biochem Physiol Part A: Mol Integ Physiol 120(1):113–118

    Google Scholar 

  48. Alqueres SM, Oliveira JH, Nogueira EM et al (2010) Antioxidant pathways are up-regulated during biological nitrogen fixation to prevent ROS-induced nitrogenase inhibition in Gluconacetobacterdi azotrophicus. Arch Microbiol 192:835–841

    CAS  PubMed  PubMed Central  Google Scholar 

  49. Zhao W, Ye Z, Zhao JA (2007) A Membrane-associated Mn-superoxide dismutase protects the photosynthetic apparatus and nitrogenase from oxidative damage in the cyanobacterium Anabaena sp. PCC 7120. Plant Cell Physiol 48(4):563–572

    CAS  PubMed  Google Scholar 

  50. Pade N, Hagemann M (2015) Salt acclimation of cyanobacteria and their application in biotechnology. Life 5(1):25–49

    CAS  Google Scholar 

  51. Nakahara K, Yamamoto H, Miyake C, Yokota A (2003) Purification and characterization of class-I and class-II fructose-1,6-bisphosphate aldolases from the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 44(3):326–33

    CAS  PubMed  Google Scholar 

  52. Fridlyand LE, Scheibe R (1999) Regulation of the Calvin cycle for CO2 fixation as an example for general control mechanisms in metabolic cycles. Biosystems 51(2):79–93

    CAS  PubMed  Google Scholar 

  53. Ma W, Wei L, Wang Q, Shi D, Chen H (2008) Increased activity of the tandem fructose-1, 6-bisphosphate aldolase, triosephosphate isomerase and fructose-1, 6-bisphosphatase enzymes in Anabaena sp. strain PCC 7120 stimulates photosynthetic yield. J Appl Phycol 20(4):437–443

    CAS  Google Scholar 

  54. Murik O, Oren N, Shotland Y et al (2016) What distinguishes cyanobacteria able to revive after desiccation from those that cannot: the genome aspect. Environ Microbiol 19(2):535–550

    PubMed  Google Scholar 

  55. Srivastava AK, Bhargava P, Thapar R, Rai LC (2008) Salinity-induced physiological and proteomic changes in Anabaena doliolum. Environ Exp Bot 64(1):49–57

    CAS  Google Scholar 

  56. Cheng Z, Dong K, Ge P, Bian Y, Dong L, Deng X et al (2015) Identification of leaf proteins differentially accumulated between wheat cultivars distinct in their levels of drought tolerance. PLoS ONE 10(5):e0125302. https://doi.org/10.1371/journal.pone.0125302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Berg IA, Kockelkorn D, Ramos-Vera WH et al (2010) Autotrophic carbon fixation in archaea. Nat Rev Microbiol 8(6):447–460

    CAS  PubMed  Google Scholar 

  58. Zaffagnini M, Fermani S, Costa A, Lemaire SD, Trost P (2013) Plant cytoplasmic GAPDH: redox post-translational modifications and moonlighting properties. Front Plant Sci 4:450

    PubMed  PubMed Central  Google Scholar 

  59. Gao Y, Xiong W, Li XB et al (2009) Identification of the proteomic changes in Synechocystis sp. PCC 6803 following prolonged UV-B irradiation. J Exp Bot 60(4):1141–1154

    CAS  PubMed  Google Scholar 

  60. Babele PK, Kumar J, Chaturvedi V (2019) Proteomic de-regulation in cyanobacteria in response to abiotic stresses. Front Microbiol 10:1315

    PubMed  PubMed Central  Google Scholar 

  61. Wang B, Yang L, Zhang Y, Chen S, Gao X, Wan C (2019) Investigation of the dynamical expression of Nostoc flagelliforme proteome in response to rehydration. J Proteomics 192:160–168

    CAS  PubMed  Google Scholar 

  62. Pandey S, Rai R, Rai LC (2012) Proteomics combines morphological, physiological and biochemical attributes to unravel the survival strategy of Anabaena sp. PCC7120 under arsenic stress. J Proteomics 75(3):921–937

    CAS  PubMed  Google Scholar 

  63. Singh PK, Shrivastava AK, Chatterjee A, Pandey S, Rai S, Singh S, Rai LC (2015) Cadmium toxicity in diazotrophic Anabaena sp. adjudged by hasty up-accumulation of transporter and signaling and severe down-accumulation of nitrogen metabolism proteins. J proteomics 127:134–146

    CAS  PubMed  Google Scholar 

  64. Rajaram H, Apte SK (2010) Differential regulation of groESL operon expression in response to heat and light in Anabaena. Arch Microbiology 192(19):729–738

    CAS  Google Scholar 

  65. Rajaram H, Chaurasia AK, Apte SK (2014) Cyanobacterial heat-shock response: role and regulation of molecular chaperones. Microbiology 160(4):647–658

    CAS  PubMed  Google Scholar 

  66. Watanabe S, Sato M, Nimura-Matsune K, Chibazakura T, Yoshikawa H (2007) Protection of psbAII transcript from ribonuclease degradation in vitro by DnaK2 and DnaJ2 chaperones of the cyanobacterium Synechococcus elongatus PCC 7942. Biosci Biotechnol Biochem 71(1):279–282

    CAS  PubMed  Google Scholar 

  67. Kowata H, Tochigi S, Takahashi H, Kojima S (2017) Outer membrane permeability of cyanobacterium Synechocystis sp. strain PCC 6803: studies of passive diffusion of small organic nutrients reveal the absence of classical porins and intrinsically low permeability. J Bacteriol 199:e00371-17. https://doi.org/10.1128/JB.00371-17

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Chatterjee A, Rajarshi K, Ghosh H, Singh MK, Roy OP, Ray S (2020) Molecular chaperones in protein folding and stress management in cyanobacteria. In: Advances in Cyanobacterial Biology pp 119–128 Academic Press.

  69. Qiao J, Huang S, Te R, Wang J, Chen L, Zhang W (2013) Integrated proteomic and transcriptomic analysis reveals novel genes and regulatory mechanisms involved in salt stress responses in Synechocystis sp. PCC 6803. Appl Microbiol Biotechnol 97(18):8253–8264

    CAS  PubMed  Google Scholar 

  70. Pandhal J, Biggs C, Wright P (2008) Proteomics with a pinch of salt: A cyanobacterial perspective. Saline Syst 4(1):1–18

    PubMed  PubMed Central  Google Scholar 

  71. Martinez-Medina A, Flors V, Heil M et al (2016) Recognizing plant defense priming. Trends Plant Sci 21(10):818–822

    CAS  PubMed  Google Scholar 

  72. Mauch-Mani B, Baccelli I, Luna E, Flors V (2017) Defense priming: an adaptive part of induced resistance. Annu Rev Plant Biol 68:485–512

    CAS  PubMed  Google Scholar 

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Acknowledgements

The work was conducted as part of the in house project at ICAR-Indian Agricultural Research Institute, New Delhi. We gratefully acknowledge the authorities of ICAR-Indian Agricultural Research Institute, New Delhi. We gratefully acknowledge Director, ICAR-NIPB, New Delhi for helping in MALDI-TOF MS/MS analysis.

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GA conceived the idea, planned the experiments and interpreted the results. RKY and KNT helped in conducting the experiments and recording the observations and EV helped in the statistical analysis.

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Correspondence to Gerard Abraham.

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Yadav, R.K., Tripathi, K., Varghese, E. et al. Physiological and Proteomic Studies of the Cyanobacterium Anabaena sp. Acclimated to Desiccation Stress. Curr Microbiol 78, 2429–2439 (2021). https://doi.org/10.1007/s00284-021-02504-x

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