Journal of Microbiology and Biotechnology
The Korean Society for Microbiology and Biotechnology publishes the Journal of Microbiology and Biotechnology.

2014 ; Vol.24-8: 1015~1025

AuthorMehboob Ahmed, Lucas J. Stal, Shahida Hasnain
Place of dutyDepartment of Microbiology and Molecular Genetics, University of the Punjab, Lahore-54590, Pakistan,Department of Marine Microbiology, Royal Netherlands Institute for Sea Research (NIOZ), NL-4400 AC Yerseke, The Netherlands
TitleBiofilm Formation and Indole-3-Acetic Acid Production by Two Rhizospheric Unicellular Cyanobacteria
PublicationInfo J. Microbiol. Biotechnol.2014 ; Vol.24-8
AbstractMicroorganisms that live in the rhizosphere play a pivotal role in the functioning and maintenance of soil ecosystems. The study of rhizospheric cyanobacteria has been hampered by the difficulty to culture and maintain them in the laboratory. The present work investigated the production of the plant hormone indole-3-acetic acid (IAA) and the potential of biofilm formation on the rhizoplane of pea plants by two cyanobacterial strains, isolated from rice rhizosphere. The unicellular cyanobacteria Chroococcidiopsis sp. MMG-5 and Synechocystis sp. MMG-8 that were isolated from a rice rhizosphere, were investigated. Production of IAA by Chroococcidiopsis sp. MMG-5 and Synechocystis sp. MMG-8 was measured under experimental conditions (pH and light). The bioactivity of the cyanobacterial auxin was demonstrated through the alteration of the rooting pattern of Pisum sativum seedlings. The increase in the concentration of L-tryptophan and the time that this amino acid was present in the medium resulted in a significant enhancement of the synthesis of IAA (r > 0.900 at p = 0.01). There was also a significant correlation between the concentration of IAA in the supernatant of the cyanobacteria cultures and the root length and number of the pea seedlings. Observations made by confocal laser scanning microscopy revealed the presence of cyanobacteria on the surface of the roots and also provided evidence for the penetration of the cyanobacteria in the endorhizosphere. We show that the synthesis of IAA by Chroococcidiopsis sp. MMG-5 and Synechocystis sp. MMG-8 occurs under different environmental conditions and that the auxin is important for the development of the seedling roots and for establishing an intimate symbiosis between cyanobacteria and host plants.
Full-Text
Key_wordAuxin, Bioassay, Cyanobacterial biofilms, Chroococcidiopsis sp, Synechocystis sp, Indole 3-Acetic Acid
References
  1. Ahmed M. 2011. Cyanobacterial secondary metabolites: their impact on plant growth and fertility status of soil. Ph.D. Thesis. University of the Punjab, Lahore, Pakistan.
  2. Ahmed M, Stal LJ, Hasnain S. 2010. Association of nonheterocystous cyanobacteria with crop plants. Plant Soil 336:363-375.
    CrossRef
  3. Ahmed M, Stal LJ, Hasnain S. 2010. Production of indole-3acetic acid by the cyanobacterium Arthrospira platensis strain MMG-9. J. Microbiol. Biotechnol. 20: 1259-1265.
    CrossRef
  4. Ahmed M, Stal LJ, Hasnain S. 2011. DTAF: an efficient probe to study cyanobacterial-plant interaction using confocal laser scanning microscopy (CLSM). J. Ind. Microbiol. Biotechnol. 38: 249-255.
    CrossRef
  5. Amzallag GN, Vaisman J. 2006. Influence of brassinosteroids on initiation of the root gravitropic response in Pisum sativum seedlings. Biol. Plant 50: 283-286.
    CrossRef
  6. Badri DV, Weir TL, van der Lelie D, Vivanco JM. 2009. Rhizosphere chemical dialogues: plant–microbe interactions. Curr. Opin. Biotechnol. 20: 642-650.
    CrossRef
  7. Bais H P, W eir T L, P erry L G, Gilroy S, V ivanco JM. 2 006. The role of root exudates in rhizosphere interactions with plants and other organisms. Annu. Rev. Plant Biol. 57: 233266.
  8. Barazani O, Friedman J. 1999. Is IAA the major root growth factor secreted from plant-growth-mediating bacteria? J. Chem. Ecol. 25: 2397-2406.
    CrossRef
  9. Berendsen RL, Pieterse CM, Bakker PA. 2012. The rhizosphere microbiome and plant health. Trends Plant Sci. 17: 478-486.
    CrossRef
  10. Bergman B, Zheng WW, Klint J, Ran L. 2008. On the origin of plants and relations to contemporary cyanobacterial-plant symbioses. Plant Biotechnol. 25: 213-220.
    CrossRef
  11. Bladergroen MR, Spaink HP. 1998. Genes and signal molecules involved in the rhizobia-leguminoseae symbiosis. Curr. Opin. Plant Biol. 1: 353-359.
    CrossRef
  12. Callis J. 2005. Plant biology: auxin action. Nature 435: 436437.
    CrossRef
  13. Davies K, Whitbread R. 1989. Factors affecting the colonisation of a root system by fluorescent pseudomonads: the effects of water, temperature and soil microflora. Plant Soil 116:247-256.
    CrossRef
  14. Dey R, Pal KK, Tilak KVBR. 2012. Influence of soil and plant types on diversity of rhizobacteria. Proc. Natl. Acad. Sci. India B Biol. Sci. 82: 341-352.
  15. Dunlap JR, Robacker KM. 1988. Nutrient salts promote light-induced degradation of indole-3-acetic-acid in tissueculture media. Plant Physiol. 88: 379-382.
    CrossRef
  16. Fierer N, Jackson RB. 2006. The diversity and biogeography of soil bacterial communities. Proc. Natl. Acad. Sci. USA 103:626-631.
    CrossRef
  17. Gaudes A, Sabater S, Vilalta E, Munoz I. 2006. The nematode community in cyanobacterial biofilms in the river Llobregat, Spain. Nematology 8: 909-919.
    CrossRef
  18. Glickmann E, Dessaux Y. 1995. A critical examination of the specificity of the Salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl. Environ. Microbiol. 61: 793-796.
  19. Guevara E, Jiménez VM, Herrera J, Bangerth F. 2008. Effect of hydrogen cyanamide on the endogenous hormonal content of pea seedlings (Pisum sativum L.). Braz. J. Plant Physiol. 20:159-163.
    CrossRef
  20. Gutierrez CK, Matsui GY, Lincoln DE, Lovell CR. 2009. Production of the phytohormone indole-3-acetic acid by estuarine species of the genus Vibrio. Appl. Environ. Microbiol. 75: 2253-2258.
    CrossRef
  21. Halliday KJ, Martinez-Garcia JF, Josse EM. 2009. Integration of light and auxin signaling. Cold Spring Harb. Perspect. Biol. 1: 1-11.
    CrossRef
  22. Höckelmann C, Jüttner F. 2004. Volatile organic compound (VOC) analysis and sources of limonene, cyclohexanone and straight chain aldehydes in axenic cultures of Calothrix and Plectonema. Water Sci. Technol. 49: 47.
  23. Hussain A, Hasnain S. 2011. Phytostimulation and biofertilization in wheat by cyanobacteria. J. Ind. Microbiol. Biotechnol. 38: 85-92.
    CrossRef
  24. Hussain A, Hasnain S. 2012. Comparative assessment of the efficacy of bacterial and cyanobacterial phytohormones in plant tissue culture. World J. Microbiol. Biotechnol. 28: 14591466.
    CrossRef
  25. Khalid A, Arshad M, Zahir ZA. 2006. Phytohormones:microbial production and applications, pp. 207-220. In Uphoff N, Ball AS, Fernandes E, Herren H, Husson O, Laing M, et al. (eds.). Biological Approaches to Sustainable Soil Systems. Taylor & Francis/CRC, Boca Raton, Florida
  26. Klock J-H, Wieland A, Seifert R, Michaelis W. 2007. Extracellular polymeric substances (EPS) from cyanobacterial mats: characterisation and isolation method optimisation. Mar. Biol. 152: 1077-1085.
    CrossRef
  27. Kusaka N, Maisch J, Nick P, Hayashi K, Nozaki H. 2009. Manipulation of intracellular auxin in a single cell by light with esterase-resistant caged auxins. Chembiochem 10: 21952202.
  28. Lambers H, Mougel C, Jaillard B, Hinsinger P. 2009. Plantmicrobesoil interactions in the rhizosphere: an evolutionary perspective. Plant Soil 321: 83-115.
    CrossRef
  29. Lambers H, Pons TL, Chapin FS. 2008. Plant Physiological Ecology. Springer, New York.
    CrossRef
  30. Lau S, Jurgens G, De Smet I. 2008. The evolving complexity of the auxin pathway. Plant Cell 20: 1738-1746.
    CrossRef
  31. Mazhar S, Cohen JD, Hasnain S. 2013. Auxin producing non-heterocystous Cyanobacteria and their impact on the growth and endogenous auxin homeostasis of wheat. J. Basic Microbiol. 53: 996-1003.
    CrossRef
  32. McNear Jr DH. 2013. The rhizosphere — roots, soil and everything in between. Nature Educ. Knowledge 4: 1.
  33. Morgan JAW, Bending GD, White PJ. 2005. Biological costs and benefits to plant–microbe interactions in the rhizosphere. J. Exp. Bot. 56: 1729-1739.
    CrossRef
  34. Okon Y, Vanderleyden J. 1997. Root-associated Azospirillum species can stimulate plants. ASM News 63: 366-370.
  35. Ortiz-Castro R, Contreras-Cornejo HA, Macias-Rodriguez L, Lopez-Bucio J. 2 009. T he r ole of m icrobial s ignals i n plant growth and development. Plant Signal Behav. 4: 701-712.
  36. Pain R, Duggan PS, Adams DG. 2000. Creation of a tryptophan auxotroph to study the role of tryptophan in heterocyst development. Abstracts of the 10th International Symposium on Phototrophic Prokaryotes, Barcelona, Spain, August 26-31, 2000.
  37. Pentecost A, Whitton BA. 2012. Subaerial Cyanobacteria, pp. 291-316. In Whitton BA (ed.). Ecology of Cyanobacteria II:Their Diversity in Space and Time. Springer, The Netherlands
    CrossRef
  38. Prasanna R, Jaiswal P, Nayak S, Sood A, Kaushik BD. 2009. Cyanobacterial diversity in the rhizosphere of rice and its ecological significance. Indian J. Microbiol. 49: 89-97.
    CrossRef
  39. Rippka R, Herdman M. 1992. Pasteur Culture Collection of Cyanobacteria: Catalogue and Taxonomic Handbook. I. Catalogue of Strains, Institut Pasteur, Paris.
  40. Ryu RJ, Patten CL. 2008. Aromatic amino acid-dependent expression of indole-3-pyruvate decarboxylase is regulated by TyrR in Enterobacter cloacae UW5. J. Bacteriol. 190: 72007208.
    CrossRef
  41. Sabrine H, Afif H, Mohamed B, Hamadi B, Maria H. 2010. Effects of cadmium and copper on pollen germination and fruit set in pea (Pisum sativum L.). Sci. Horticult. 125: 551555.
    CrossRef
  42. Sergeeva E, Liaimer A, Bergman B. 2002. Evidence for production of the phytohormone indole-3-acetic acid by cyanobacteria. Planta 215: 229-238.
    CrossRef
  43. Smýkal P, Aubert G, Burstin J, Coyne CJ, Ellis NT, Flavell AJ, et al. 2012. Pea (Pisum sativum L.) in the genomic era. Agronomy 2: 74-115.
    CrossRef
  44. Spaepen S, Vanderleyden J, Remans R. 2007. Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol. Rev. 31: 425-448.
    CrossRef
  45. Tabei Y, Okada K, Makita N, Tsuzuki M. 2009. Lightinduced gene expression of fructose 1,6-bisphosphate aldolase during heterotrophic growth in a cyanobacterium, Synechocystis sp. PCC 6803. FEBS J. 276: 187-198.
    CrossRef
  46. Tandeau de Marsac N, Houmard J. 1988. Complementary chromatic adaptation: physiological conditions and action spectra. Methods Enzymol 167: 318-328.
    CrossRef
  47. Tao Y, Ferrer JL, Ljung K, Pojer F, Hong F, Long JA, et al. 2008. Rapid synthesis of auxin via a new tryptophandependent pathway is required for shade avoidance in plants. Cell 133: 164-176.
    CrossRef
  48. Yuan ZC, Liu P, Saenkham P, Kerr K, Nester EW. 2008. Transcriptome profiling and functional analysis of Agrobacterium tumefaciens reveals a general conserved response to acidic conditions (pH 5.5) and a complex acid-mediated signaling involved in Agrobacterium-plant interactions. J. Bacteriol. 190:494-507.
    CrossRef



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