DOI QR코드

DOI QR Code

Iron Starvation-Induced Proteomic Changes in Anabaena (Nostoc) sp. PCC 7120: Exploring Survival Strategy

  • Narayan, Om Prakash (Molecular Biology Section, Centre of Advanced Study in Botany, Banaras Hindu University) ;
  • Kumari, Nidhi (Molecular Biology Section, Centre of Advanced Study in Botany, Banaras Hindu University) ;
  • Rai, Lal Chand (Molecular Biology Section, Centre of Advanced Study in Botany, Banaras Hindu University)
  • Received : 2010.09.13
  • Accepted : 2010.11.04
  • Published : 2011.02.28

Abstract

This study provides first-hand proteomic data on the survival strategy of Anabaena sp. PCC 7120 when subjected to long-term iron-starvation conditions. 2D-gel electrophoresis followed by MALDI-TOF/MS analysis of iron-deficient Anabaena revealed significant and reproducible alterations in ten proteins, of which six are associated with photosynthesis and respiration, three with the antioxidative defense system, and the last, hypothetical protein all1861, conceivably connected with iron homeostasis. Iron-starved Anabaena registered a reduction in growth, photosynthetic pigments, PSI, PSII, whole-chain electron transport, carbon and nitrogen fixation, and ATP and NADPH content. The kinetics of hypothetical protein all1861 expression, with no change in expression until day 3, maximum expression on the $7^{th}$ day, and a decline in expression from the $15^{th}$ day onward, coupled with in silico analysis, suggested its role in iron sequestration and homeostasis. Interestingly, the up-regulated FBP-aldolase, Mn/Fe-SOD, and all1861 all appear to assist the survival of Anabeana subjected to iron-starvation conditions. Furthermore, the $N_2$-fixation capabilities of the iron-starved Anabaena encourage us to recommend its application as a biofertilizer, particularly in iron-limited paddy soils.

Keywords

References

  1. Allen, A. E., J. LaRoche, U. Maheswari, M. Lommer, N. Schauer, P. J. Lopez, G. Finazzi, A. R. Fernie, and C. Bowler. 2008. Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation. Proc. Natl Acad. Sci. USA 105: 10438-10443. https://doi.org/10.1073/pnas.0711370105
  2. Apte, S. K. A. and A. Bhagwat. 1989. Salinity stress induced proteins in two nitrogen fixing Anabaena strains differentially tolerant to salt. J. Bacteriol. 171: 909-915. https://doi.org/10.1128/jb.171.2.909-915.1989
  3. Bauer, C. C., L. Scappino, and R. Robert Haselkorn. 1993. Growth of the cyanobacterium Anabaena on molecular nitrogen: Nifj is required when iron is limited. Proc. Natl. Acad. Sci. USA 90: 8812-8816. https://doi.org/10.1073/pnas.90.19.8812
  4. Bhargava, P., Y. Mishra, A. K. Srivastava, O. P. Narayan, and L. C. Rai. 2008. Excess copper induces anoxygenic photosynthesis in Anabaena doliolum: A homology based proteomic assessment of its survival strategy. Photosynth. Res. 96: 61-74. https://doi.org/10.1007/s11120-007-9285-7
  5. Brody, S. S. and M. A. Brody. 1961. Quantitative assay for the number of chromophores on a chromoprotein: Its application to phycoerythrin and phycocyanin. Biochim. Biophys. Acta 50: 348-352. https://doi.org/10.1016/0006-3002(61)90333-X
  6. Cheng, Y., J. H. Li, L. Shi, L. Wang, A. Latifi, and C. C. Zhang. 2006. A pair of iron responsive genes encoding protein kinases with a Ser/Thr kinase domain and His kinase domain are regulated by NtcA in the cyanobacterium Anabaena sp. strain PCC 7120. J. Bacteriol. 188: 4822-4829. https://doi.org/10.1128/JB.00258-06
  7. Fausto da Silva, J. J. R. and R. J. P. Williams. 1994. 2001. The biological chemistry of the elements. In: The Inorganic Chemistry of Life, 2nd Ed. Oxford University Press, Oxford, United Kingdom.
  8. Ferreira, F. and N. A. Straus. 2003. Iron deprivation in cyanobacteria. J. Appl. Phycol. 6: 199-210.
  9. Georgiou, G. and L. Masip. 2003. Biochemistry: An over oxidation journey with a return ticket. Science 300: 592-594. https://doi.org/10.1126/science.1084976
  10. Halliwell, B. and J. M. C. Gutteridge. 2006. Free Radicals in Biology and Medicine, 4th Ed. Clarendon Press, Oxford, United Kingdom.
  11. Herranen, M., N. Battchikova, P. Zhang, A. Graf, S. Sirpiö, V. Paakkarinen, and E. M. Aro. 2004. Towards functional proteomics of membrane protein complexes in Synechocystis sp. PCC 6803. Plant Physiol. 134: 470-481. https://doi.org/10.1104/pp.103.032326
  12. Ivanov, A. G., M. Krol, E. Selstam, P. V. Sane, D. Sveshnikov, N. P. A. Park, Y-II. Oquist, and G. Huner. 2007. The induction of CP43 by iron-stress in Synechococcus sp. PCC 7942 is associated with carotenoid accumulation and enhanced fatty acid unsaturation. Biochim. Biophys. Acta 1767: 807-813. https://doi.org/10.1016/j.bbabio.2007.02.006
  13. Kupper, H., I. Setlik, S. Seibert, O. Prasil, E. Setlikova, M. Strittmatter, O. Levitan, J. L. Iwona Adamska, and I. Berman- Frank. 2008. Iron limitation in the marine cyanobacterium Trichodesmium reveals new insights into regulation of photosynthesis and nitrogen fixation. New Phytol. 179: 784-798. https://doi.org/10.1111/j.1469-8137.2008.02497.x
  14. Larson, C. M. and T. Olsson. 1979. Firefly assay of adenine nucleotide from algae: Comparison of extraction methods. Plant Cell Physiol. 2: 145-155.
  15. Latifi, A., R. Jeanjean, S. Lemeille, M. Havaux, and C. C. Zhang. 2005. Iron starvation leads to oxidative stress in Anabaena sp. strain PCC 7120. J. Bacteriol. 187: 6596-6598. https://doi.org/10.1128/JB.187.18.6596-6598.2005
  16. Leonhardt, K. and N. A. Straus. 1994. Photosystem II genes isiA, psbDI and psbC, in Anabaena sp. PCC 7120: Cloning, sequencing and transcriptional regulation in iron stressed and iron repleted cells. Plant Mol. Biol. 24: 63-73. https://doi.org/10.1007/BF00040574
  17. Mackinney, G. 1941. Absorption of light by chlorophyll solutions. J. Biol. Chem. 140: 315-322.
  18. Meng, F., Y. Wei, and X. Yang. Iron content and bioavailability in rice. 2005. J. Trace Elem. Med. Biol. 18: 333-338. https://doi.org/10.1016/j.jtemb.2005.02.008
  19. Michel, K. P. and E. K. Pistorius. 2004. Adaptation of the photosynthetic electron transport chain in cyanobacteria to iron deficiency: The function of idiA and isiA. Physiol. Plant 120: 36-50. https://doi.org/10.1111/j.0031-9317.2004.0229.x
  20. Mishra, Y., N. Chaurasia, and L. C. Rai. 2009. Heat pretreatment alleviates UV-B toxicity in the cyanobacterium Anabaena doliolum: A proteomic analysis of cross tolerance. Photochem. Photobiol. 85: 824-833. https://doi.org/10.1111/j.1751-1097.2008.00469.x
  21. Myers, J. and W. A. Kratz. 1955. Relationship between pigment content and photosynthetic characteristics in a blue green alga. J. Gen. Physiol. 39: 11-21. https://doi.org/10.1085/jgp.39.1.11
  22. O'Farrell, P. H. 1975. High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250: 4007-4021.
  23. Rakkiyappan, P., S. Thangavelu, and R. Radhamani. 2002. Effect of ferrous sulphate on sugarcane varieties grown in iron deficient soil. Sugar Tech. 4: 33-37. https://doi.org/10.1007/BF02956877
  24. Regelsberger, G., U. Laaha, D. Dietmann, F. Rüker, A. Canini, M. Grilli-Caiola, et al. 2004. The iron superoxide dismutase from the filamentous cyanobacterium Nostoc PCC 7120: Localization, overexpression, and biochemical characterization. J. Biol. Chem. 279: 44384-44393. https://doi.org/10.1074/jbc.M406254200
  25. Rippka, R., J. Deruelles, J. B. Waterbury, M. Herdman, and R. Y. Stanier. 1979. Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J. Gen. Microbiol. 111: 1-6. https://doi.org/10.1099/00221287-111-1-1
  26. Sandmann, G. and R. Malkin. 1983. Iron-sulfur centers and activities of the photosynthetic electron transport chain in iron deficient cultures of the blue-green alga Aphanocapsa. Plant Physiol. 73: 724-728. https://doi.org/10.1104/pp.73.3.724
  27. Sandmann, G., M. L. Peleato, M. F. Fillat, M. C. Lfizaro, and C. Gumez-Moreno. 1990. Consequences of the iron-dependent formation of ferredoxin and flavodoxin on photosynthesis and nitrogen fixation on Anabaena strains. Photosynth. Res. 26: 119-125. https://doi.org/10.1007/BF00047083
  28. Sandstrom, S., A. G. Ivanovb, G. Parkc, Y-Il. Oquista, and P. Gustafssona. 2002. Iron stress responses in the cyanobacterium Synechococcus sp. PCC7942. Physiol. Plant 116: 255-263. https://doi.org/10.1034/j.1399-3054.2002.1160216.x
  29. Shcolnick, S., T. C. Summerfield, L. Reytman, L. A. Sherman, and N. Keren. 2009. The mechanism of iron homeostasis in the unicellular cyanobacterium Synechocystis sp. PCC 6803 and its relationship to oxidative stress. Plant Physiol. 150: 2045-2056. https://doi.org/10.1104/pp.109.141853
  30. Singh, A. K., L. M. McIntyre, and L. A. Sherman. 2003. Microarray analysis of the genome-wide response to iron deficiency and iron reconstitution in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol. 132: 1825-1839. https://doi.org/10.1104/pp.103.024018
  31. Singh, A. K. and L. A. Sherman. 2000. Identification of ironresponsive, differential gene expression in the cyanobacterium Synechocystis sp. strain PCC 6803 with a customized amplification library. J. Bacteriol. 182: 3536-3543. https://doi.org/10.1128/JB.182.12.3536-3543.2000
  32. Smyth, D. A. and W. M. Dugger. 1981. Cellular changes during iron deficient culture of the diatom Cylindrotheca fusiformis. Physiol. Plant 51: 111-117. https://doi.org/10.1111/j.1399-3054.1981.tb00887.x
  33. Srivastava, A. K., A. Ara, P. Bhargava. Y. Mishra, S. P. Rai, and L. C. Rai. 2007. A rapid and cost-effective method of genomic DNA isolation from cyanobacterial culture, mat and soil suitable for genomic fingerprinting and community analysis. J. Appl. Phycol. 19: 373-382. https://doi.org/10.1007/s10811-006-9144-5
  34. Stewart, W. D. P., G. P. Fitzgerald, and R. H. Burris. 1968. Acetylene reduction by nitrogen fixing blue-green algae. Arch. Microbiol. 62: 336-348.
  35. Straus, N. A. 1994. Iron deprivation: Physiology and gene regulation, pp. 731-750. In D. A. Bryant (ed.). The Molecular Biology of Cyanobacteria. Kluwer Academic Publishers, The Netherlands.
  36. Timperio, A. M., G. M. D'Amici, C. Barta, F. Loreto, and L. Zolla. 2007. Proteomics, pigment composition, and organization of thylakoid membranes in iron-deficient spinach leaves. J. Exp. Bot. 58: 3695-3710. https://doi.org/10.1093/jxb/erm219
  37. Tripathy, B. C. and P. Mohanty. 1980. Zinc-inhibited electron transport of photosynthesis in isolated barley chloroplasts. Plant Physiol. 66: 1174-1178. https://doi.org/10.1104/pp.66.6.1174
  38. Wagner, M. A., M. Eschenbrenner, T. A. Honrn, J. A. Kraycer, C. V. Mujer, S. Hagius, P. Elzer, and V. G. DelVecchio. 2002. Global analysis of the Brucella melitensis proteome: Identification of proteins expressed in laboratory grown culture. Proteomics 2: 1047-1060. https://doi.org/10.1002/1615-9861(200208)2:8<1047::AID-PROT1047>3.0.CO;2-8
  39. Xu, W. L., R. Jeanjean, Y. D. Liu, and C. C. Zhang. 2003. pkn22 (alr 2502) encoding a putative Ser/Thr kinase in the cyanobacterium Anabaena sp. PCC 7120 is induced by both iron starvation and oxidative stress and regulates the expression of isiA. FEBS Lett. 553: 179-182. https://doi.org/10.1016/S0014-5793(03)01019-6

Cited by

  1. DIFFERENTIAL RESPONSES OF ANABAENA SP. PCC 7120 (CYANOPHYCEAE) CULTURED IN NITROGEN‐DEFICIENT AND NITROGEN‐ENRICHED MEDIA TO ULTRAVIOLET‐B RADIATION vol.48, pp.3, 2011, https://doi.org/10.1111/j.1529-8817.2012.01162.x
  2. Purification, crystallization and preliminary crystallographic analysis of KatB, a manganese catalase from Anabaena PCC 7120 vol.69, pp.11, 2011, https://doi.org/10.1107/s1744309113028017
  3. FurA influences heterocyst differentiation in Anabaena sp. PCC 7120 vol.587, pp.16, 2013, https://doi.org/10.1016/j.febslet.2013.07.007
  4. The influence of soil and water physicochemical properties on the distribution of Nostoc sphaeroides (Cyanophyceae) in paddy fields and biochemical comparison with indoor cultured biomass vol.25, pp.6, 2013, https://doi.org/10.1007/s10811-013-0040-5
  5. Oxidative stress management in the filamentous, heterocystous, diazotrophic cyanobacterium, Anabaena PCC7120 vol.118, pp.1, 2011, https://doi.org/10.1007/s11120-013-9929-8
  6. Responses to iron limitation are impacted by light quality and regulated by RcaE in the chromatically acclimating cyanobacterium Fremyella diplosiphon vol.160, pp.5, 2011, https://doi.org/10.1099/mic.0.075192-0
  7. Enhanced Resistance to UV-B Radiation in Anabaena sp. PCC 7120 (Cyanophyceae) by Repeated Exposure vol.69, pp.1, 2011, https://doi.org/10.1007/s00284-014-0543-6
  8. The Tryptophan-Rich Sensory Protein (TSPO) is Involved in Stress-Related and Light-Dependent Processes in the Cyanobacterium Fremyella diplosiphon vol.6, pp.None, 2011, https://doi.org/10.3389/fmicb.2015.01393
  9. The Peptidoglycan-Binding Protein SjcF1 Influences Septal Junction Function and Channel Formation in the Filamentous Cyanobacterium Anabaena vol.6, pp.4, 2015, https://doi.org/10.1128/mbio.00376-15
  10. A single gene all3940 (Dps) overexpression in Anabaena sp. PCC 7120 confers multiple abiotic stress tolerance via proteomic alterations vol.16, pp.1, 2011, https://doi.org/10.1007/s10142-015-0467-7
  11. Extracellular Proteins: Novel Key Components of Metal Resistance in Cyanobacteria? vol.7, pp.None, 2011, https://doi.org/10.3389/fmicb.2016.00878
  12. Alr2954 of Anabaena sp. PCC 7120 with ADP-ribose pyrophosphatase activity bestows abiotic stress tolerance in Escherichia coli vol.17, pp.1, 2011, https://doi.org/10.1007/s10142-016-0531-y
  13. Impairment of ntcA gene revealed its role in regulating iron homeostasis, ROS production and cellular phenotype under iron deficiency in cyanobacterium Anabaena sp. PCC 7120 vol.33, pp.8, 2011, https://doi.org/10.1007/s11274-017-2323-5
  14. Reciprocal Effect of Copper and Iron Regulation on the Proteome of Synechocystis sp. PCC 6803 vol.9, pp.None, 2011, https://doi.org/10.3389/fbioe.2021.673402