Abstract
DNA-binding proteins (Dps) induced during starvation play an important role in gene regulation and maintaining homeostasis in bacteria. The nitrogen-fixing cyanobacterium, Anabaena PCC7120, has four genes annotated as coding for Dps; however, the information on their physiological roles is limiting. One of the genes coding for Dps, ‘all3940’ was found to be induced under different abiotic stresses in Anabaena and upon overexpression enhanced the tolerance of Anabaena to a multitude of stresses, which included salinity, heat, heavy metals, pesticide, and nutrient starvation. On the other hand, mutation in the gene resulted in decreased growth of Anabaena. The modulation in the levels of All3940 in Anabaena, achieved either by overexpression of the protein or mutation of the gene, resulted in changes in the proteome, which correlated well with the physiological changes observed. Proteins required for varied physiological activities, such as photosynthesis, carbon-metabolism, oxidative stress alleviation, exhibited change in protein profile upon modulation of All3940 levels in Anabaena. This suggested a direct or an indirect effect of All3940 on the expression of the above stress-responsive proteins, thereby enhancing tolerance in Anabaena PCC7120. Thus, All3940, though categorized as a Dps, is possibly a general stress protein having a global role in regulating tolerance to multitude of stresses in Anabaena.





Similar content being viewed by others
References
Agrawal C, Sen S, Singh S, Rai S, Singh PK, Singh VK, Rai LC (2014) Comparative proteomics reveals association of early accumulated proteins in conferring butachlor tolerance in three N2-fixing Anabaena spp. J Proteomics 96:271–290
Almiron M, Link AJ, Furlong D, Kolter R (1992) A novel DNA-binding protein with regulatory and protective roles in starved Escherichia coli. Genes Dev 6:2646–2654
Alqueres SMC, Oliveira JHM, Nogueira EM, Guedes HV, Oliveira PL, Camara F, Baldani JI, Martins OB (2010) Antioxidant pathways are up-regulated during biological nitrogen fixation to prevent ROS-induced nitrogenase inhibition in Gluconacetobacter diazotrophicus. Arch Microbiol 192:835–841
Apte SK (2001) Coping with salinity/water stress: cyanobacteria show the way. Proc Indian Natl Sci Acad 5:285–310
Apte SK, Fernandes T, Badran H, Ballal A (1998) Expression and possible role of stress-responsive proteins in Anabaena. J Biosci 23:399–406
Banerjee M, Raghavan PS, Ballal A, Rajaram H, Apte SK (2013) Oxidative stress management in the filamentous, heterocystous, diazotrophic cyanobacterium, Anabaena PCC7120. Photosynth Res 118:59–70
Bhargava P, Mishra Y, Srivastava AK, Narayan OP, Rai LC (2008) Excess copper induces anoxygenic photosynthesis in Anabaena doliolum: a homology based proteomic assessment of its survival strategy. Photosynth Res 96:61–74
Brock TD (1973) Evolutionary and ecological aspects of cyanophytes. In The Biology of Blue-Green Algae. pp. 487–500. Edited by NG. Carr and BA Whitton. Oxford: Blackwell.
Castenholz RW (1988) Culturing methods for cyanobacteria. Methods Enzymol 167:68–93
Chaurasia AK, Apte SK (2009) Overexpression of the groESL operon enhances the heat and salinity stress tolerance of the nitrogen-fixing cyanobacterium Anabaena sp. strain PCC7120. Appl Environ Microbiol 75:6008–6012
Chaurasia AK, Paranis A, Apte SK (2008) An integrative expression vector for strain improvement and environmental applications of the nitrogen fixing cyanobacterium Anabaena sp. strain PCC7120. J Micrbiol Methods 73:133–141
Chaurasia AK, Adhya TK, Apte SK (2013) Engineering bacteria for bioremediation of persistent organochlorine pesticide lindane (γ-hexachlorocyclohexane). Bioresour Technol 149:439–445
Ho KK (1984) Inorganic pyrophosphatase from Spirulina maxima. Plant Cell Physiol 25:851–854
Jain A, Verma D, Bagchi D (2006) Catalytic and regulatory property of sulphur metabolizing enzymes in cyanobacterium Synechococcus elongatus PCC7942. Ind J Experiment Biol 44:767–772
Koksharova OA, Wolk CP (2002) Novel DNA-binding proteins in the cyanobacterium Anabaena sp. strain PCC 7120. J Bacteriol 184:3931–3940
Kopriva S, Fritzemeier K, Wiedemann G, Reski R (2007) The putative moss 3-phosphoadenosine-5-phosphosulfate reductase is a novel form of adenosine-5-phosphosulfate reductase without an iron-sulfur cluster. J Biol Chem 282:22930–22938
Korn A, Ajlani G, Lagoutte B, Gall A, Sètif P (2009) Ferredoxin:NADP+ oxidoreductase association with phycocyanin modulates its properties. J Biol Chem 284:31789–31797
Kumar A, Biomolata W, Kannan M, Kirti PB, Qureshi IA, Ghazi IA (2015) Comparative proteomics reveals differential induction of both biotic and abiotic stress response associated proteins in rice during Xanthomonas oryzae pv. oryzae infection. Funct Integr Genomics 15:425–437
Kumari N, Narayan OP, Rai LC (2009) Understanding butachlor toxicity in Aulosira fertilissima using physiological, biochemical and proteomic approaches. Chemosphere 77:1501–1507
Larsen CM, Olsson T (1979) Firefly assay of adenine nucleotide from algae. Comparison of extraction methods. Plant Cell Physiol 2:145–155
Latifi A, Riuz M, Zang CC (2009) Oxidative stress in cyanobacteria. FEMS Microbiol Rev 33:258–278
Lithgow JK, Hayhurst EJ, Cohen G, Aharonowitz Y, Foster SJ (2004) Role of a cysteine synthase in Staphylococcus aureus. J Bacteriol 186:1579–1590
Mi H, Endo T, Ogawa T, Asada K (1995) Thylakoid membrane-bound, NADPH-specific pyridine nucleotide dehydrogenase complex mediates cyclic electron transport in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol 36:661–668
Nair S, Finkel SE (2004) Dps protects cells against multiple stresses during stationary phase. J Bacteriol 186:4192–4198
Narayan OP, Kumari N, Rai LC (2010) Heterologous expression of Anabaena PCC 7120 all3940 (a Dps family gene) protects Escherichia coli from nutrient limitation and abiotic stresses. Biochem Biophys Res Commun 394:163–169
Narayan OP, Kumari N, Rai LC (2011) Iron starvation-induced proteomic changes in Anabaena (Nostoc) sp. PCC 7120: exploring survival strategy. J Microbiol Biotechnol 21:136–146
Negri AS, Robotti E, Pronsi B, Espen L, Marengo E (2011) Proteins involved in biotic and abiotic stress responses as the most significant biomarker in the ripening of Pinot Noir skins. Funct Integr Genomics 11:341–355
Panda B, Basu B, Rajaram H, Apte SK (2014) Methyl viologen responsive proteome dynamics of Anabaena sp. strain PCC7120. Proteomics 14:1895–1904
Raghavan PS, Rajaram H, Apte SK (2011) Nitrogen status dependent oxidative stress tolerance conferred by overexpression of MnSOD and FeSOD proteins in Anabaena sp. strain PCC7120. Plant Mol Biol 77:407–417
Raghavan PS, Rajaram H, Apte SK (2015) Membrane targeting of MnSOD is essential for oxidative stress tolerance of nitrogen-fixing cultures of Anabaena sp. strain PCC7120. Plant Mol Biol 88:503–514
Rajaram H, Apte SK (2003) Heat-shock response and its contribution to thermotolerance of the nitrogen-fixing cyanobacterium Anabaena sp. strain L-31. Arch Microbiol 179:423–429
Rajaram H, Apte SK (2010) Differential regulation of groESL operon expression in response to heat and light in Anabaena. Arch Microbiol 192:729–738
Rajaram H, Chaurasia AK, Apte SK (2014) Cyanobacterial heat shock response: role and regulation of molecular chaperones. Microbiol 160:647–658
Sato N, Moriyama T, Toyoshima M, Mizusawa M, Tajima N (2012) The all0458/lti46.2 gene encodes a low temperature-induced Dps protein homologue in the cyanobacteria Anabaena sp. PCC 7120 and Anabaena variabilis M3. Microbiol 158:2527–2536
Singh RN (1950) Reclamation of ‘Usar’ lands in India through blue-green algae. Nature 165:325–326
Singh S, Datta P (2005) Growth and survival potentials of immobilized diazotrophic cyanobacterial isolates exposed to common ricefield herbicides. World J of Microbiol Biotechnol 21:441–446
Srivastava AK, Ara A, Bhargava P, Mishra Y, Rai SP, Rai LC (2007) A rapid and cost effective method of genomic DNA isolation from cyanobacterial mat and soil suitable for genomic fingerprinting and community analysis. J Appl Phycol 19:373–382
Stewart WDP, Fitzgerald GP, Burris RH (1968) Acetylene reduction by nitrogen fixing blue-green algae. Arch Microbiol 62(4):336–348
Tripathy BC, Mohanty P (1980) Zinc-inhibited electron transport of photosynthesis in isolated barley chloroplasts. Plant Physiol 66:1174–1178
Valverde F, Peleato ML, Fillat MF, Gómez-Moreno C, Losada M, Serrano A (2001) Simultaneous occurrence of two different glyceraldehyde-3-phosphate dehydrogenases in heterocystous N(2)-fixing cyanobacteria. Biochem Biophys Res Commun 283:356–363
Venkataraman GS (1979) Algal inoculation of rice fields. In: Nitrogen and Rice Symposium Proceedings. International Rice Research Institute, Los Banos, pp 311–321
Wei X, Mingjia H, Xiufeng L, Yang G, Qingyu W (2007) Identification and biochemical properties of Dps (starvation-induced DNA binding protein) from cyanobacterium Anabaena sp. PCC 7120. IUBMB Life 59:675–681
Zhang Z, Xin W, Wang S, Zhang X, Dai H, Sun R, Frazier T, Zhang B, Wang Q (2015) Xylem sap in cotton contains proteins that contribute to environmental stress response and cell wall development. Funct Integr Genomics 15:17–26
Acknowledgments
L. C. Rai is thankful to DAE-BRNS, Mumbai, for the financial support in the form of project and DST New Delhi for J C Bose National Fellowship. OPN and NK are thankful to ICAR and CSIR for senior research fellowships, respectively.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOCX 321 kb)
ESM 2
(DOC 355 kb)
ESM 3
(DOC 57 kb)
ESM 4
(DOC 56 kb)
ESM 5
(DOC 83 kb)
ESM 6
(DOC 52 kb)
ESM 7
(DOC 54 kb)
ESM 8
(DOC 51 kb)
ESM 9
(DOC 55 kb)
ESM 10
(DOC 53 kb)
ESM 11
(DOC 55 kb)
ESM 12
(DOC 59 kb)
ESM 13
(DOC 69 kb)
ESM 14
(DOC 55 kb)
ESM 15
(DOC 81 kb)
ESM 16
(DOC 84 kb)
ESM 17
(DOC 57 kb)
ESM 18
(DOC 57 kb)
ESM 19
(DOC 60 kb)
ESM 20
(DOC 58 kb)
ESM 21
(DOC 60 kb)
ESM 22
(DOC 84 kb)
ESM 23
(DOC 59 kb)
ESM 24
(DOC 82 kb)
ESM 25
(DOC 59 kb)
Rights and permissions
About this article
Cite this article
Narayan, O.P., Kumari, N., Bhargava, P. et al. A single gene all3940 (Dps) overexpression in Anabaena sp. PCC 7120 confers multiple abiotic stress tolerance via proteomic alterations. Funct Integr Genomics 16, 67–78 (2016). https://doi.org/10.1007/s10142-015-0467-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10142-015-0467-7


