Disentangling the Impact of Sulfur Limitation on Exopolysaccharide and Functionality of Alr2882 by In Silico Approaches in Anabaena sp. PCC 7120

Abstract

The wide applications, uniqueness, and high quality of cyanobacterial exopolysaccharides (EPSs) have attracted many biotechnologists. Despite it, the inducers and molecular determinants of EPS biosynthesis in cyanobacteria are lesser known. Although, studies revealed that environmental cues especially C/N ratio as the prime modulator, the factors like light, temperature, moisture, and nutrient availability, etc. have been overlooked. Due to this, the possibilities to modify cyanobacterial system for achieving higher quantity of EPS either by modifying growth medium or metabolic engineering are restricted to few optimisations. Therefore, the present work describes the impact of sulfate limitations on the EPS production and compositions in the cyanobacterium Anabaena sp. PCC 7120. Increased EPS production with enhanced expression of alr2882 was observed in lower sulfate supplementations; however, FTIR analysis depicted an altered composition of supramolecule. Furthermore, in silico analysis of Alr2882 depicted the presence of ExoD domain and three transmembrane regions, thereby indicating its membrane localisation and role in the EPS production. Additionally, the phylogeny and multiple sequence alignment showed vertical inheritance of exoD and conservation among cyanobacteria. The meta-threading template-based modelling and ab initio full atomic relaxation by LOMET and ModRefiner servers, respectively, also exhibited helical topology of Alr2882, with nine α-helices arranged antiparallel to the preceding one. Moreover, post-translational modifications predicted in Alr2882 indicated high order of molecular regulation underlining EPS production in Anabaena sp. PCC 7120. This study provides a foundation for understanding the EPS biosynthesis mechanism under sulfur limitation and the possible role of ExoD in cyanobacteria.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  1. 1.

    De Philippis, R., Margheri, M. C., Materassi, R., & Vincenzini, M. (1998). Potential of unicellular cyanobacteria from saline environments as exopolysaccharide producers. Applied and Environmental Microbiology, 64, 1130–1132.

    PubMed  PubMed Central  Google Scholar 

  2. 2.

    De Philippis, R., & Vincenzini, M. (2003). Outermost polysaccharidic investments of cyanobacteria: Nature, significance and possible applications. Recent Research Developments in Microbiology, 7, 13–22.

    Google Scholar 

  3. 3.

    Roberts, I. S. (1996). The biochemistry and genetics of capsular polysaccharide production in bacteria. Annual Review of Microbiology, 50, 285–315.

    CAS  PubMed  Google Scholar 

  4. 4.

    Parikh, A., & Madamwar, D. (2006). Partial characterization of extracellular polysaccharides from cyanobacteria. Bioresource Technology, 97, 1822–1827.

    CAS  PubMed  Google Scholar 

  5. 5.

    Pugh, N., Ross, A., Elsohly, H. N., Elsohly, M. A., & Pasco, D. (2001). Isolation of three high molecular weight polysaccharide preparations with potent immunostimulatory activity from Spirulina platensis, Aphanizomenon flos-aquae and Chlorella pyrenoidosa. Planta Medica, 67, 737–742.

    CAS  PubMed  Google Scholar 

  6. 6.

    Ghosh, T., Chattopadhyay, K., Marschall, M., Karmakar, P., Mandal, P., & Ray, B. (2009). Focus on antivirally active sulfated polysaccharides: From structure–activity analysis to clinical evaluation. Glycobiol., 19, 2–15.

    CAS  Google Scholar 

  7. 7.

    De Philippis, R., & Micheletti, E. (2009). Heavy metal removal with exopolysaccharide-producing cyanobacteria. In L. K. Wang, J. P. Chen, Y. T. Hung, & N. K. Shammas (Eds.), Heavy metals in the environment (pp. 89–122). Boca Raton: CRC Press.

    Google Scholar 

  8. 8.

    Sutherland, I. W. (2001). Biofilm exopolysaccharides: A strong and sticky framework. Microbiol., 147, 3–9.

    CAS  Google Scholar 

  9. 9.

    De Vuyst, L., DeVin, F., Vaningelgem, F., & Degeest, B. (2001). Recent developments in the biosynthesis and applications of heteropolysaccharides from lactic acid bacteria. International Dairy Journal, 11, 687–708.

    Google Scholar 

  10. 10.

    De Vuyst, L., & Degeest, B. (1999). Heteropolysaccharides from lactic acid bacteria. FEMS Microbiology Reviews, 23, 153–177.

    PubMed  Google Scholar 

  11. 11.

    Van Hijum, S. A. F. T., Kralj, S., Ozimek, L. K., Dijkhuizen, L., & Van GeelSchutten, I. G. H. (2006). Structure–function relationships of glucansucrase and fructansucrase enzymes from lactic acid bacteria. Microbiology and Molecular Biology Reviews, 70, 157–176.

    PubMed  PubMed Central  Google Scholar 

  12. 12.

    Arskold, E., Svensson, M., Grage, H., Roos, S., Radstrom, P., & van Niel, E. W. J. (2007). Environmental influences on exopolysaccharide formation in Lactobacillus reuteri ATCC 55730. International Journal of Food Microbiology, 116, 159–167.

    PubMed  Google Scholar 

  13. 13.

    Lama, L., Nicolaus, B., Calandrelli, V., Manca, M. C., Romano, I., & Gambacorta, A. (1996). Effect of growth conditions on endo-and exopolymer biosynthesis in Anabaena cylindrica 10 C. Phytochem., 42, 655–659.

    CAS  Google Scholar 

  14. 14.

    Ricciardi, A., Parente, E., Crudele, M. A., Zanetti, F., Scolari, G., & Mannazzu, I. (2002). Exopolysaccharide production by Streptococcus thermophilus SY: Production and preliminary characterization of the polymer. Journal of Applied Microbiology, 92, 297–306.

    CAS  PubMed  Google Scholar 

  15. 15.

    Fischer, S. E., Marioli, J. M., & Mori, G. (2003). Effect of root exudates on the exopolysaccharide composition and the lipopolysaccharide profile of Azospirillum brasilense Cd under saline stress. FEMS Microbiology Letters, 219, 53–62.

    CAS  PubMed  Google Scholar 

  16. 16.

    Bahat-Samet, E., Castro-Sowinski, S., & Okon, Y. (2004). Arabinose content of extracellular polysaccharide plays a role in cell aggregation of Azospirillum brasilense. FEMS Microbiology Letters, 237, 195–203.

    CAS  PubMed  Google Scholar 

  17. 17.

    Selbmann, L., Onofri, S., Fenice, M., Federici, F., & Petruccioli, M. (2002). Production and structural characterization of the exopolysaccharide of the Antarctic fungus Phoma herbarum CCFEE 5080. Research in Microbiology, 153, 585–592.

    CAS  PubMed  Google Scholar 

  18. 18.

    Pereira, S., Zille, A., Micheletti, E., Moradas-Ferreira, P., De Philippis, R., & Tamagnini, P. (2009). Complexity of cyanobacterial exopolysaccharides: Composition, structures, inducing factors and putative genes involved in their biosynthesis and assembly. FEMS Microbiology Reviews, 33, 917–941.

    CAS  PubMed  Google Scholar 

  19. 19.

    De Philippis, R., Sili, C., Paperi, R., & Vincenzini, M. (2001). Exopolysaccharide-producing cyanobacteria and their possible exploitation: a review. Journal of Applied Phycology, 13, 293–299.

    Google Scholar 

  20. 20.

    Hu, C., Zhang, D., Huang, Z., & Liu, Y. D. (2003b). The vertical microdistribution of cyanobacteria and green algae within desert crusts and the development of the algal crusts. Plant and Soil, 257, 97–111.

    CAS  Google Scholar 

  21. 21.

    Hu, C. W., Lin, M. H., Huang, H. C., Ku, W. C., Yi, T. H., Tsai, C. F., Chen, Y. J., Sugiyama, N., Ishihama, Y., Jaun, H. F., & Wu, S. H. (2012). Phosphoproteomic analysis of Rhodopseudomonas palustris reveals the role of pyruvate phosphate dikinase phosphorylation in lipid production. Journal of Proteome Research, 11, 5362–5375.

    CAS  PubMed  Google Scholar 

  22. 22.

    Flaibani, A., Olsen, Y., & Painter, T. J. (1989). Polysaccharides in desert reclamation: composition of exocellular proteoglycan complexes produced by filamentous blue-green and unicellular green edaphic algae. Carbohydrate Research, 190, 235–248.

    CAS  Google Scholar 

  23. 23.

    Marra, M., Palmeri, A., Ballio, A., Segre, A., & Slodki, M. E. (1990). Structural characterization of the exocellular polysaccharide from Cyanospira capsulata. Carbohydrate Research, 197, 338–344.

    CAS  Google Scholar 

  24. 24.

    Kawaguchi, T., & Decho, A. W. (2002). Isolation and biochemical characterization of extracellular polymeric secretions (eps) from modern soft marine stromatolites (Bahamas) and its inhibitory effect on CaCO3 precipitation. Preparative Biochemistry & Biotechnology, 32, 51–63.

    CAS  Google Scholar 

  25. 25.

    Phoenix, V. R., Adams, D. G., & Konhauser, K. O. (2000). Cyanobacterial viability during hydrothermal biomineralization. Chemical Geology, 169, 329–338.

    CAS  Google Scholar 

  26. 26.

    Tsuneda, S., Aikawa, H., Hayashi, H., Yuasa, A., & Hirata, A. (2003). Extracellular polymeric substances responsible for bacterial adhesion onto solid surface. FEMS Microbiology Letters, 223, 287–292.

    CAS  PubMed  Google Scholar 

  27. 27.

    Welman, A. D., & Maddox, I. S. (2003). Exopolysaccharides from lactic acid bacteria: perspectives and challenges. Trends in Biotechnology, 21, 269–274.

    CAS  PubMed  Google Scholar 

  28. 28.

    Benning, L. G., Phoenix, V. R., Yee, N., & Tobin, M. J. (2004). Molecular characterization of cyanobacterial silicification using synchrotron infrared micro-spectroscopy. Geochimica et Cosmochimica Acta, 68, 729–741.

    CAS  Google Scholar 

  29. 29.

    Tamaru, Y., Takani, Y., Yoshida, T., & Sakamoto, T. (2005). Crucial role of extracellular polysaccharides in desiccation and freezing tolerance in the terrestrial cyanobacterium Nostoc commune. Applied and Environmental Microbiology, 71, 7327–7333.

    CAS  PubMed  PubMed Central  Google Scholar 

  30. 30.

    Parker, D. L., Schram, B., Plude, J. L., & Moore, R. E. (1996). Effect of metal cations on the viscosity of a pectin-like capsular polysaccharide from the cyanobacterium Microcystis flosaquae C3-40. Applied and Environmental Microbiology, 62, 1208–1213.

    CAS  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Sutherland, I. W. (2001). Microbial polysaccharides from Gram negative bacteria. International Dairy Journal, 11, 663–674.

    CAS  Google Scholar 

  32. 32.

    Otero, A., & Vincenzini, M. (2004). Nostoc (Cyanophyceae) goes nude: Extracellular polysaccharides serve as a sink for reducing power under unbalanced C/N metabolism. Journal of Phycology, 40, 74–81.

    CAS  Google Scholar 

  33. 33.

    Singh, S., Verma, E., Tiwari, B., & Mishra, A. K. (2016). Exopolysaccharide production in Anabaena sp. PCC 7120 under different CaCl2 regimes. Physiol. Molecul. Biol. Plants, 22, 557–566.

    CAS  Google Scholar 

  34. 34.

    Green, L. S., & Grossman, A. R. (1988). Changes in sulfate transport characteristics and protein composition of Anacystis nidulans R2 during sulfate deprivation. Journal of Bacteriology, 170, 583–587.

    CAS  PubMed  PubMed Central  Google Scholar 

  35. 35.

    Laudenbach, D. E., & Grossman, A. R. (1991). Characterization and mutagenesis of sulfur-regulated genes in a cyanobacterium: Evidence for function in sulfate transport. Journal of Bacteriology, 173, 2739–2750.

    CAS  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Ariño, X., Ortega-Calvo, J. J., Hernandez-Marine, M., & Saiz-Jimenez, C. (1995). Effect of sulfur starvation on the morphology and ultrastructure of the cyanobacterium Gloeothece sp. PCC 6909. Archives of Microbiology, 163, 447–453.

    Google Scholar 

  37. 37.

    Schmidt, A., Erdle, I., & Köst, H. P. (1982). Changes of C-phycocyanin in Synechococcus6301 in relation to growth on various sulfur compounds materials and methods. Zeitschrift für Naturforschung. Section C, 37, 870–876.

    Google Scholar 

  38. 38.

    Wanner, G., Henkelmann, A., Schmidt, H., & Kost, P. (1986). Nitrogen and sulfur starvation of the cyanobacterium Synechococcus 6301. An ultrastructural, morphometrical, and biochemical comparison. Zeitschrift für Naturforschung, 41, 741–750.

    CAS  Google Scholar 

  39. 39.

    Laudenbach, D. E., Ehrhardt, D., Green, L., & Grossman, A. (1991). Isolation and characterization of a sulfur-regulated gene encoding a periplasmically localized protein with sequence similarity to rhodanese. Journal of Bacteriology, 173, 2751–2760.

    CAS  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Gutu, A., Alvey, R. M., Bashour, S., Zingg, D., & Kehoe, D. M. (2011). Sulfate-driven elemental sparing is regulated at the transcriptional and post transcriptional levels in a filamentous cyanobacterium. Journal of Bacteriology, 193, 1449–1460.

    CAS  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Zhang, Z., Pendse, N. D., Phillips, K. N., Cotner, J. B., & Khodursky, A. (2008). Gene expression patterns of sulfur starvation in Synechocystis sp. PCC 6803. BMC Genomics, 9, 344.

    PubMed  PubMed Central  Google Scholar 

  42. 42.

    Kharwar, S., & Mishra, A. K. (2020). Unraveling the complexities underlying sulfur deficiency and starvation in the cyanobacterium Anabaena sp. PCC 7120. Environmental and Experimental Botany, 172, 103966.

    Google Scholar 

  43. 43.

    Rippka, R., Deruelles, J., Waterbury, J. B., Herdman, M., & Stainer, R. Y. (1979). Genetic assignments, strain histories and properties of pure cultures of cyanobacteria. Journal of General Microbiology, 111, 1–61.

    Google Scholar 

  44. 44.

    Cérantola, S., Bounéry, J. D., Segonds, C., Marty, N., & Montrozier, H. (2000). Exopolysaccharide production by mucoid and non-mucoid strains of Burkholderia cepacia. FEMS Microbiology Letters, 185, 243–246.

    PubMed  Google Scholar 

  45. 45.

    Ozturk, S., & Aslim, B. (2010). Modification of exopolysaccharide composition and production by three cyanobacterial isolates under salt stress. Environmental Science and Pollution Research, 17, 595–602.

    CAS  PubMed  Google Scholar 

  46. 46.

    Dubois, M., Gilles, K. A., Hamilton, J. K., Rebers, P. A., & Smith, F. (1956). Colorimetric method for determination of sugars and related substances. Analytical Chemistry, 28, 350–356.

    CAS  Google Scholar 

  47. 47.

    Bradford, M. M. (1976). A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry, 72, 248–254.

    CAS  PubMed  Google Scholar 

  48. 48.

    Freitas, F., Alves, V. D., & Reis, M. A. M. (2011). Advances in bacterial exopolysaccharides from production to biotechnological applications. Trends in Biotechnology, 29, 388–398.

    CAS  PubMed  Google Scholar 

  49. 49.

    Cooper, D. G., & Goldenberg, B. G. (1987). Surface-active agents from two Bacillus species. Applied and Environmental Microbiology, 53, 224–229.

    CAS  PubMed  PubMed Central  Google Scholar 

  50. 50.

    Pinto, F., Pacheco, C. C., Ferreira, D., Moradas-Ferreira, P., & Tamagnini, P. (2012). Selection of suitable reference genes for RT-qPCR analyses in cyanobacteria. PLoS One, 7, e34983.

    CAS  PubMed  PubMed Central  Google Scholar 

  51. 51.

    Ren, J., Wen, L., Gao, X., Jin, C., Xue, Y., & Yao, X. (2009). DOG 1.0: illustrator of protein domain structures. Cell Research, 19, 271–273.

    CAS  PubMed  Google Scholar 

  52. 52.

    Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30, 2725–2729.

    CAS  PubMed  PubMed Central  Google Scholar 

  53. 53.

    Letunic, I., & Bork, P. (2011). Interactive Tree Of Life v2: Online annotation and display of phylogenetic trees made easy. Nucleic Acids Research, 39, 475–478.

    Google Scholar 

  54. 54.

    Willard, L., Ranjan, A., Zhang, H., Monzavi, H., Boyko, R. F., Sykes, B. D., & Wishart, D. S. (2013). VADAR: A web server for quantitative evaluation of protein structure quality. Nucleic Acids Research, 31, 3316–3319.

    Google Scholar 

  55. 55.

    Bhattacharjee, S., & Mishra, A. K. (2020). The tale of caspases-homologues and their evolutionary outlook: Deciphering programmed cell death in cyanobacteria. Journal of Experimental Botany, 71, 4639–4657.

    CAS  PubMed  PubMed Central  Google Scholar 

  56. 56.

    Borah, D., Rethinam, G., Gopalakrishnan, S., Rout, J., Alharbi, N. S., Alharbi, S. A., & Nooruddin, T. (2020). Ozone enhanced production of potentially useful exopolymers from the cyanobacterium Nostoc muscorum. Polymer Testing, 84, 106385.

    CAS  Google Scholar 

  57. 57.

    Chakraborty, T., Sen, A., & Pal, R. (2015). Stress induced enhancement in exopolysaccharide production in Spirulina subsalsa and its chemical characterization. Journal of Algal Biomass Utilization, 6, 24–38.

    Google Scholar 

  58. 58.

    Markou, G., Angelidaki, I., & Georgakakis, D. (2012). Microalgal carbohydrates: An overview of the factors influencing carbohydrates production, and of main bioconversion technologies for production of biofuels. Applied Microbiology and Biotechnology, 96, 631–645.

    CAS  PubMed  Google Scholar 

  59. 59.

    Dean, A. P., Estrada, B., Nicholson, J. M., & Sigee, D. C. (2008). Molecular response of Anabaena flos-aquae to differing concentrations of phosphorus: a combined Fourier transform infrared and X-ray microanalytical study. Phycological Research, 56, 193–201.

    CAS  Google Scholar 

  60. 60.

    Liu, J. R., Wang, S. Y., Lin, Y. Y., & Lin, C. W. (2002). Antitumor activity of milk, kefir and soya milk kefir in tumor bearing mice. Nutrition and Cancer, 44, 183–187.

    PubMed  Google Scholar 

  61. 61.

    Caiola, M. G., Billi, D., & Friedmann, E. I. (1996). Effect of desiccation on envelopes of the cyanobacterium Chroococcidiopsis sp. (Chroococcales). European Journal of Phycology, 31, 97–105.

    Google Scholar 

  62. 62.

    Kavita, K., Singh, V. K., Mishra, A., & Jha, B. (2014). Characterisation and anti-biofilm activity of extracellular polymeric substances from Oceanobacillus iheyensis. Carbohydrate Polymers, 101, 29–35.

    CAS  PubMed  Google Scholar 

  63. 63.

    Mihoubi, W., Sahli, E., Gargouri, A., & Amiel, C. (2017). FTIR spectroscopy of whole cells for the monitoring of yeast apoptosis mediated by p53 over-expression and its suppression by Nigella sativa extracts. PLoS One, 12, 1–16.

    Google Scholar 

  64. 64.

    Ahluwalia, S. S., & Goyal, D. (2005). Removal of heavy metals by waste tea leaves from aqueous solution. Engineering in Life Sciences, 5, 158–162.

    CAS  Google Scholar 

  65. 65.

    Lillo, L., Cabello, G., Cespedes, C. L., Caro, C. A., & Perez, J. (2014). Structural studies of the exopolysaccharide produced by a submerged culture of entomopathogenic fungus Metarhizium anisopliae. Boletin Latinoamericano y del Caribe de Plantas Medicinales y Aromaticas, 13, 359–365.

    Google Scholar 

  66. 66.

    Vijayabaskar, P., Babinastarlin, S., Shankar, T., Sivakumar, T., & Anandapandian, K. (2011). Quantification and characterization of exopolysaccharides from Bacillus subtilis (MTCC 121). Advances in Biology Research, 5, 71–76.

    CAS  Google Scholar 

  67. 67.

    Sardari, R. R., Kulcinskaja, E., Ron, E. Y., Björnsdóttir, S., Friðjónsson, Ó. H., Hreggviðsson, G. Ó., & Karlsson, E. N. (2017). Evaluation of the production of exopolysaccharides by two strains of the thermophilic bacterium Rhodothermus marinus. Carbohydrate Polymers, 56, 1–8.

    Google Scholar 

  68. 68.

    Rochas, C., Lahaye, M., & Yaphe, W. (1986). Sulfate content of carrageenan and agar determined by infrared spectroscopy. Botanica Marina, 23, 335–340.

    Google Scholar 

  69. 69.

    Flamm, D., & Blaschek, W. (2014). Exopolysaccharides of Synechocystis aquatilis are sulphated arabinofucans containing N-acetyl-fucosamine. Carbohydrate Polymers, 101, 301–306.

    CAS  PubMed  Google Scholar 

  70. 70.

    Raveendran, S., Palaninathan, V., Chauhan, N., Sakamoto, Y., Yoshida, Y., Maekawa, T., Mohanan, P. V., & Kumar, D. S. (2013). In vitro evaluation of antioxidant defense mechanism and hemocompatibility of mauran. Carbohydrate Polymers, 98, 108–115.

    CAS  PubMed  Google Scholar 

  71. 71.

    Pavlova, K., Koleva, L., Kratchanova, M., & Panchev, I. (2004). Production and isolation of exopolysaccharide by yeast. World Journal of Microbiology & Biotechnology, 20, 435–439.

    CAS  Google Scholar 

  72. 72.

    Sajna, K. V., Sukumaran, R. K., Gottumukkala, L. D., Jayamurthy, H., Dhar, K. S., & Pandey, A. (2013). Studies on structural and physical characteristics of novel exopolysaccharide from Pseudozyma sp. NII 08165. International Journal of Biological Macromolecules, 59, 84–89.

    CAS  PubMed  Google Scholar 

  73. 73.

    Sahana, T. G., Fathimath Sadiya, M. K., & Rekha, P. D. (2018). Emulsifying and cell proliferative abilities of the exopolysaccharide produced by leguminous plant nodule associated bacterium Cronobacter sp. Journal of Polymers and the Environment, 26, 3382–3388.

    CAS  Google Scholar 

  74. 74.

    Zhan, H. J., Gray, J. X., Levery, S. B., Rolfe, B. G., & Leigh, J. A. (1990). Functional and evolutionary relatedness of genes for exopolysaccharide synthesis in Rhizobium meliloti and Rhizobium sp. strain NGR234. Journal of Bacteriology, 172, 5245–5253.

    CAS  PubMed  PubMed Central  Google Scholar 

  75. 75.

    Zhang, Y., Hu, C., & Chen, M. (2018). Induced exopolysaccharide synthesis and the molecular mechanism in Synechocystis sp. PCC 6803 under clinorotation. Microgravity Science and Technology, 30, 857–864.

    CAS  Google Scholar 

  76. 76.

    Reed, J. W., & Walker, G. C. (1991). The exoD gene of Rhizobium meliloti encodes a novel function needed for alfalfa nodule invasion. Journal of Bacteriology, 173, 664–677.

    CAS  PubMed  PubMed Central  Google Scholar 

  77. 77.

    Pereira, S. B., Mota, R., Vieira, C. P., Vieira, J., & Tamagnini, P. (2015). Phylum-wide analysis of genes/proteins related to the last steps of assembly and export of extracellular polymeric substances (EPS) in cyanobacteria. Scientific Reports, 5, 14835.

    CAS  PubMed  PubMed Central  Google Scholar 

  78. 78.

    Szymanski, C. M., Burr, D. H., & Guerry, P. (2002). Campylobacter protein glycosylation affects host cell interactions. Infection and Immunity, 70, 2242–2244.

    CAS  PubMed  PubMed Central  Google Scholar 

  79. 79.

    Cain, J. A., Solis, N., & Cordwell, S. J. (2014). Beyond gene expression: the impact of protein post-translational modifications in bacteria. Journal of Proteomics, 97, 265–286.

    CAS  PubMed  Google Scholar 

  80. 80.

    Stöckel, J., Jacobs, J. M., Elvitigala, T. R., Liberton, M., Welsh, E. A., Polpitiya, A. D., Gritsenko, M. A., Nicora, C. D., Koppenaal, D. W., Smith, R. D., & Pakrasi, H. B. (2011). Diurnal rhythms result in significant changes in the cellular protein complement in the cyanobacterium Cyanothece 51142. PLoS One, 6, e16680.

    PubMed  PubMed Central  Google Scholar 

  81. 81.

    Zhang, C. C., Jang, J., Sakr, S., & Wang, L. (2005). Protein phosphorylation on Ser, Thr and Tyr residues in cyanobacteria. Journal of Molecular Microbiology and Biotechnology, 9, 154–166.

    CAS  PubMed  Google Scholar 

  82. 82.

    Sanders, C. E., Melis, A., & Allen, J. F. (1989). In vivo phosphorylation of proteins in the cyanobacterium Synechococcus 6301 after chromatic acclimation to photosystem I or photosystem II light. Biochimica et Biophysica Acta, 976, 168–172.

    CAS  Google Scholar 

  83. 83.

    Hagemann, M., Golldack, D., Biggins, J., & Erdmann, N. (1993). Salt-dependent protein phosphorylation in the cyanobacterium Synechocystis PCC 6803. FEMS Microbiology Letters, 113, 205–209.

    CAS  Google Scholar 

  84. 84.

    Macek, B., Mijakovic, I., Olsen, J. V., Gnad, F., Kumar, C., Jensen, P. R., & Mann, M. (2007). The serine/threonine/tyrosine phosphoproteome of the model bacterium Bacillus subtilis. Molecular & Cellular Proteomics, 6, 697–707.

    CAS  Google Scholar 

  85. 85.

    Ge, R. G., Sun, X. S., Xiao, C. L., Yin, X. F., Shan, W. R., Chen, Z., & He, Q. Y. (2011). Phosphoproteome analysis of the pathogenic bacterium Helicobacter pylori reveals over-representation of tyrosine phosphorylation and multiply phosphorylated proteins. Proteomics., 11, 1449–1461.

    CAS  PubMed  Google Scholar 

  86. 86.

    Lin, M. H., Hsu, T. L., Lin, S. Y., Pan, Y. J., Jan, J. T., Wang, J. T., Khoo, K. H., & Wu, S. H. (2009). Phosphoproteomics of Klebsiella pneumoniae NTUH-K2044 reveals a tight link between tyrosine phosphorylation and virulence. Molecular & Cellular Proteomics, 8, 2613–2623.

    CAS  Google Scholar 

  87. 87.

    Soufi, B., Gnad, F., Jensen, P. R., Petranovic, D., Mann, M., Mijakovic, I., & Macek, B. (2008). The Ser/Thr/Tyr phosphoproteome of Lactococcus lactis IL1403 reveals multiply phosphorylated proteins. Proteomics, 8, 3486–3493.

    CAS  PubMed  Google Scholar 

  88. 88.

    Cao, X. J., Dai, J., Xu, H., Nie, S., Chang, X., Hu, B. Y., Sheng, Q. H., Wang, L. S., Ning, Z. B., Li, Y. X., & Guo, X. K. (2010). High-coverage proteome analysis reveals the first insight of protein modification systems in the pathogenic spirochete Leptospira interrogans. Cell Research, 20, 197–210.

    CAS  PubMed  Google Scholar 

  89. 89.

    Prisic, S., Dankwa, S., Schwartz, D., Chou, M. F., Locasale, J. W., Kang, C. M., Bemis, G., Church, G. M., Steen, H., & Husson, R. N. (2010). Extensive phosphorylation with overlapping specificity by Mycobacterium tuberculosis serine/threonine protein kinases. Proceedings of the National Academy of Sciences, 107, 7521–7526.

    CAS  Google Scholar 

  90. 90.

    van Noort, V., Seebacher, J., Bader, S., Mohammed, S., Vonkova, I., Betts, M. J., Kuhner, S., Kumar, R., Maier, T., O’Flaherty, M., & Rybin, V. (2012). Cross-talk between phosphorylation and lysine acetylation in a genome-reduced bacterium. Molecular Systems Biology, 8, 571.

    PubMed  PubMed Central  Google Scholar 

  91. 91.

    Hu, C., Liu, Y., Paulsen, B. S., Petersen, D., & Klaveness, D. (2003). Extracellular carbohydrate polymers from five desert soil algae with different cohesion in the stabilization of fine sand grain. Carbohydrate Polymers, 54, 33–42.

    CAS  Google Scholar 

  92. 92.

    Sun, X. S., Ge, F., Xiao, C. L., Yin, X. F., Ge, R. G., Zhang, L. H., & He, Q. Y. (2010). Phosphoproteomic analysis reveals the multiple roles of phosphorylation in pathogenic bacterium Streptococcus pneumonia. Journal of Proteome Research, 9, 275–282.

    CAS  PubMed  Google Scholar 

  93. 93.

    Manteca, A., Ye, J., Sanchez, J., & Jensen, O. N. (2011). Phosphoproteome analysis of Streptomyces development reveals extensive protein phosphorylation accompanying bacterial differentiation. Journal of Proteome Research, 10, 5481–5492.

    CAS  PubMed  Google Scholar 

  94. 94.

    Nothaft, H., Liu, X., McNally, D. J., Li, J. J., & Szymanski, C. M. (2009). Study of free oligosaccharides derived from the bacterial N-glycosylation pathway. Proceedings of the National Academy of Sciences, 106, 15019–15024.

    CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Prof. C.P. Wolk for his kind gift of the Anabaena sp. PCC 7120. Central Instrumental Library (CIL), Department of Chemistry, BHU, Varanasi, is acknowledged for FTIR facility. The Head, Department of Botany, Banaras Hindu University, Varanasi, India, is gratefully acknowledged for providing laboratory facilities. Surbhi Kharwar is also thankful to University Grants Commission (UGC), New Delhi, for their financial support in the form of SRF. Samujjal Bhattacharjee is thankful to Council of Scientific and Industrial Research (CSIR) for awarding junior research fellowship.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Arun Kumar Mishra.

Ethics declarations

Ethics Approval and Consent to Participate

This article does not contain any studies with human participants or animals performed by any of the authors. All the authors have given consent to participate in the manuscript.

Consent for Publication

All the authors have given consent for the publication of the manuscript.

Competing Interests

The authors declare no competing interests.

Additional information

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

figure9

High Resolution Image (PNG 1338 kb)

figure10

High Resolution Image (PNG 537 kb)

ESM 1

(TIF 326 kb)

ESM 2

(TIF 103 kb)

ESM 3

(DOCX 14 kb)

ESM 4

(DOCX 23 kb)

ESM 5

(DOCX 15 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Kharwar, S., Bhattacharjee, S. & Mishra, A.K. Disentangling the Impact of Sulfur Limitation on Exopolysaccharide and Functionality of Alr2882 by In Silico Approaches in Anabaena sp. PCC 7120. Appl Biochem Biotechnol 193, 1447–1468 (2021). https://doi.org/10.1007/s12010-021-03501-3

Download citation

Keywords

  • Exopolysaccharides
  • Anabaena sp. PCC 7120
  • Fourier transform infrared spectroscopy
  • Post-translational modifications
  • RT-PCR
  • Alr2882
  • In silico analysis
  • Sulfate