Advertisement

Annals of Microbiology

, Volume 68, Issue 12, pp 953–962 | Cite as

Assessment of atrazine decontamination by epiphytic root bacteria isolated from emergent hydrophytes

  • Anina James
  • Dileep Kumar SinghEmail author
Original Article
  • 116 Downloads

Abstract

Aim of the study was to identify atrazine remediating bacteria that can potentially succeed in situ where they encounter varied environmental conditions. Three epiphytic root bacteria, genus Pseudomonas and Arthrobacter, were isolated from rhizoplanes of hydrophytes Acorus calamus, Typha latifolia, and Phragmites karka. Potential of these strains to decontaminate environmentally relevant concentrations of atrazine was determined in liquid atrazine medium (LAM) and Luria-Bertani (LB) medium at varying pH and temperature. There was an increase in decontamination by the strains with time upon exposure to 2.5 to 10 mg l−1 atrazine over a period of 15 days, notably, in both minimal and nutrient-rich media. Growth in terms of O.D.600 and biomass determined during the same period also showed a corresponding surge. Pseudomonas sp. strain AACB mitigated atrazine in a wide range of pH (5 to 8). Pseudomonas sp. strains AACB and TTLB decontaminated > 62% atrazine at 10 °C. All the strains exhibited plant growth–promoting traits in vitro, reported for the first time in the presence of atrazine. Strain AACB exhibits the novel trait of atrazine decontamination under harsh environmental conditions mimicked in lab. Strains isolated in the present study promise success in in situ remediation. Bioreactors and water treatment plants can be designed comprising the hydrophytes and the strains inoculated into their rhizospheres to improve efficacy of the treatment. They can be used to study plant-bacterium mutualistic symbiosis or other interactions occurring during atrazine mitigation.

Keywords

Arthrobacter Bioremediation Plant growth–promoting rhizobacteria (PGPR) Pseudomonas Rhizoremediation 

Notes

Acknowledgments

I am thankful to Mr. Souvik Sen Sharma, Cellular Endocrinology Lab, National Institute of Immunology, for his valuable input in data analysis and comments regarding the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

13213_2018_1404_MOESM1_ESM.docx (4.9 mb)
ESM 1 (DOCX 5033 kb)

References

  1. © World Health Organization (1993) Guidelines for drinking-water quality - WHO 1993. 1:11. doi:  https://doi.org/10.1017/CBO9781107415324.004
  2. Accinelli C, Dinelli G, Vicari A, Catizone P (2001) Atrazine and metolachlor degradation in subsoils. Biol Fertil Soils 33:495–500.  https://doi.org/10.1007/s003740100358 CrossRefGoogle Scholar
  3. Ames Gottfred NP, Christie BR, Jordan DC (1989) Use of the chrome azurol S agar plate technique to differentiate strains and field isolates of Rhizobium leguminosarum biovar trifolii. Appl Environ Microbiol 55:707–710PubMedPubMedCentralGoogle Scholar
  4. Assaf NA, Turco RF (1994) Accelerated biodegradation of atrazine by a microbial consortium is possible in culture and soil. Biodegradation 5:29–35.  https://doi.org/10.1007/BF00695211 CrossRefPubMedGoogle Scholar
  5. Bellini MI, Pinelli L, Dos Santos ME, Fernández Scavino A (2014) Bacterial consortia from raw water and sludges from water potabilization plants are able to degrade atrazine. Int Biodeterior Biodegrad 90:131–139.  https://doi.org/10.1016/j.ibiod.2014.02.011 CrossRefGoogle Scholar
  6. Boopathy R (2000) Factors limiting bioremediation technology. Bioresour Technol 74:63–67CrossRefGoogle Scholar
  7. Bureau of Indian Standards (2014) Indian standard packaged drinking water other than packaged natural mineralGoogle Scholar
  8. Cai B, Han Y, Liu B, Ren Y, Jiang S (2003) Isolation and characterization of an atrazine-degrading bacterium from industrial wastewater in China. Lett Appl Microbiol 36:272–276.  https://doi.org/10.1046/j.1472-765X.2003.01307.x CrossRefPubMedGoogle Scholar
  9. Cheng HP, Walker GC (1998) Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. J Bacteriol 180:5183–5191PubMedPubMedCentralGoogle Scholar
  10. Dey R, Pal KK, Bhatt DM, Chauhan SM (2004) Growth promotion and yield enhancement of peanut (Arachis hypogaea L.) by application of plant growth-promoting rhizobacteria. Microbiol Res 159:371–394.  https://doi.org/10.1016/j.micres.2004.08.004 CrossRefPubMedGoogle Scholar
  11. Dragana J, Kuzmanovic SPR, Bogic M (2006) The competitive ability of different Rhizobium leguminosarum bv. trifolii inoculant strains. Rom Biotechnol Lett 11:2637–2641Google Scholar
  12. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791CrossRefGoogle Scholar
  13. Fernandes AFT, da Silva MBP, Martins VV, Miranda CES, Stehling EG (2014) Isolation and characterization of a Pseudomonas aeruginosa from a virgin Brazilian Amazon region with potential to degrade atrazine. Environ Sci Pollut Res 21:13974–13978.  https://doi.org/10.1007/s11356-014-3316-7 CrossRefGoogle Scholar
  14. Fernández LA, Valverde C, Gómez MA (2013) Isolation and characterization of atrazine-degrading Arthrobacter sp. strains from Argentine agricultural soils. Ann Microbiol 63:207–214.  https://doi.org/10.1007/s13213-012-0463-2 CrossRefGoogle Scholar
  15. García-González V, Govantes F, Shaw LJ, Burns RG, Santero E (2003) Nitrogen control of atrazine utilization in Pseudomonas sp. strain ADP. Appl Environ Microbiol 69:6987–6993.  https://doi.org/10.1128/AEM.69.12.6987-6993.2003 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Gebendinger N, Radosevich M (1999) Inhibition of atrazine degradation by cyanazine and exogenous nitrogen in bacterial isolate M91-3. Appl Microbiol Biotechnol 51:375–381.  https://doi.org/10.1007/s002530051405 CrossRefPubMedGoogle Scholar
  17. Goldstein RM, Mallory LM, Alexander M (1985) Reasons for possible failure of inoculation to enhance biodegradation. Appl Environ Microbiol 50:977–983PubMedPubMedCentralGoogle Scholar
  18. Grigg BC, Bischoff M, Turco RF (1997) Cocontaminant effects on degradation of triazine herbicides by a mixed microbial culture. J Agric Food Chem 45:995–1000CrossRefGoogle Scholar
  19. Houot S, Topp E, Yassir A, Soulas G (2000) Dependence of accelerated degradation of atrazine on soil pH in French and Canadian soils. Soil Biol Biochem 32:615–625.  https://doi.org/10.1016/S0038-0717(99)00188-1 CrossRefGoogle Scholar
  20. James A, Singh DK, Khankhane PJ (2017) Enhanced atrazine removal by hydrophyte-bacterium associations and in vitro screening of the isolates for their plant growth promoting potential. Int J Phytoremediation:00–00.  https://doi.org/10.1080/15226514.2017.1337068 CrossRefGoogle Scholar
  21. Joseph B, Patra RR, Lawrence R (2007) Characterization of plant growth promoting rhizobacteria associated with chickpea (Cicer arietinum L.). Int J Plant Prod 1:141–151Google Scholar
  22. Komang Ralebitso T, Senior E, Van Verseveld HW (2002) Microbial aspects of atrazine degradation in natural environments. Biodegradation 13:11–19.  https://doi.org/10.1023/A:1016329628618 CrossRefGoogle Scholar
  23. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874CrossRefGoogle Scholar
  24. Kravchenko LV, Azarova TS, Makarova NMTI (2004) The effect of tryptophan of plant root metabolites on the phyto stimulating activity of rhizobacteria. Mikrobiologiia 73:195–198PubMedGoogle Scholar
  25. Liu M, González JE, Willis LB, Walker GC, Gonza JE (1998) A novel screening method for isolating exopolysaccharide-deficient mutants 64:4600–4602Google Scholar
  26. Lorck H (1948) Production of hydrocyanic acid by bacteria. Physiol Plant 1:142–146CrossRefGoogle Scholar
  27. Louden BC, Haarmann D, Lynne A (2011) Use of blue agar CAS assay for siderophore detection. J Microbiol Biol Educ 12:51–53.  https://doi.org/10.1128/jmbe.v12i1.249 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Marecik R, Bialas W, Cyplik P, Lawniczak L, Chrzanowski L (2012) Phytoremediation potential of three wetland plant species toward atrazine in environmentally relevant concentrations. Polish J Environ Stud 21:697–702Google Scholar
  29. Marecik R, Króliczak P, Czaczyk K, Białas W, Olejnik A, Cyplik P (2008) Atrazine degradation by aerobic microorganisms isolated from the rhizosphere of sweet flag (Acorus calamus L.). Biodegradation 19:293–301.  https://doi.org/10.1007/s10532-007-9135-5 CrossRefPubMedGoogle Scholar
  30. McKinlay RG, Kasperek K (1999) Observations on decontamination of herbicide-polluted water by marsh plant systems. Water Res 33:505–511.  https://doi.org/10.1016/S0043-1354(98)00244-9 CrossRefGoogle Scholar
  31. Mehta S, Nautiyal CS (2001) An efficient method for qualitative screening of phosphate-solubilizing bacteria. Curr Microbiol 43:51–56.  https://doi.org/10.1007/s002840010259 CrossRefPubMedGoogle Scholar
  32. Moore MT, Tyler HL, Locke MA (2013) Aqueous pesticide mitigation efficiency of Typha latifolia (L.), Leersia oryzoides (L.) Sw., and Sparganium americanum Nutt. Chemosphere 92:1307–1313.  https://doi.org/10.1016/j.chemosphere.2013.04.099 CrossRefPubMedGoogle Scholar
  33. Mueller TC, Steckel LE, Radosevich M (2010) Effect of soil pH and previous atrazine use history on atrazine degradation in a Tennessee field soil. Weed Sci 58:478–483.  https://doi.org/10.1614/WS-D-09-00041.1 CrossRefGoogle Scholar
  34. Paim S, Langenbach T (1996) Adsorption of S-triazine by soil componentsCrossRefGoogle Scholar
  35. Pick EF, van Dyk LP, Botha E (1992) Atrazine in ground and surface water in maize production areas of the Transvaal, South Africa. Chemosphere 25:335–341CrossRefGoogle Scholar
  36. Pritchard PH (1992) Use of inoculation in bioremediation. Curr Opin Biotechnol 3:232–243CrossRefGoogle Scholar
  37. Radosevich M, Traina SJ, Tuovinen OH (1996) Biodegradation of atrazine in surface soils and subsurface sediments collected from an agricultural research farm. Biodegradation 7:137–149.  https://doi.org/10.1007/BF00114626 CrossRefPubMedGoogle Scholar
  38. Ramadan MA, El-Tayeb OM, Alexander M (1990) Inoculum size as a factor limiting success of inoculation for biodegradation. Appl Environ Microbiol 56:1392–1396PubMedPubMedCentralGoogle Scholar
  39. Ribeiro CM, Cardoso EJBN (2012) Isolation, selection and characterization of root-associated growth promoting bacteria in Brazil pine (Araucaria angustifolia). Microbiol Res 167:69–78.  https://doi.org/10.1016/j.micres.2011.03.003 CrossRefPubMedGoogle Scholar
  40. Rodríguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339.  https://doi.org/10.1016/S0734-9750(99)00014-2 CrossRefPubMedGoogle Scholar
  41. Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  42. Sarwar M, Arshad M, Martens DA, Frankenberger WT (1992) Tryptophan-dependent biosynthesis of auxins in soil. Plant Soil 147:207–215.  https://doi.org/10.1007/BF00029072 CrossRefGoogle Scholar
  43. Shaheen K, Mukherjee S, Ningthoujam D (2017) Biocontrol and PGP potential of endophytic Actinobacteria from selected ethnomedicinal plants in 4:20–27. doi:  https://doi.org/10.15406/jbmoa.2017.04.00112
  44. Singh N, Megharaj M, Kookana RS, Naidu R, Sethunathan N (2004) Atrazine and simazine degradation in Pennisetum rhizosphere. Chemosphere 56:257–263.  https://doi.org/10.1016/j.chemosphere.2004.03.010 CrossRefPubMedGoogle Scholar
  45. Spiekermann P, Rehm BHA, Kalscheuer R, Baumeister D, Steinbüchel A (1999) A sensitive, viable-colony staining method using Nile red for direct screening of bacteria that accumulate polyhydroxyalkanoic acids and other lipid storage compounds. Arch Microbiol 171:73–80.  https://doi.org/10.1007/s002030050681 CrossRefPubMedGoogle Scholar
  46. Staudt AK, Wolfe LG, Shrout JD (2012) Variations in exopolysaccharide production by Rhizobium tropici. Arch Microbiol 194:197–206.  https://doi.org/10.1007/s00203-011-0742-5 CrossRefPubMedGoogle Scholar
  47. Goswami S, Singh DK (2009) Biodegradation of a and b endosulfan in broth medium and soil microcosm by bacterial strain Bordetella sp. B9. Biodegradation 20:199–207CrossRefGoogle Scholar
  48. Tappe W, Groeneweg J, Jantsch B (2002) Diffuse atrazine pollution in German aquifers. Biodegradation 13:3–10.  https://doi.org/10.1023/A:1016325527709 CrossRefPubMedGoogle Scholar
  49. Tamura K, Nei M, Kumar S (2004) Prospects for inferring very large phylogenies by using the neighbor-joining method. Proc Natl Acad Sci U S A 101:11030–11035CrossRefGoogle Scholar
  50. Wang Q, Que X, Zheng R, Pang Z (2015) Phytotoxicity assessment of atrazine on growth and physiology of three emergent plants. doi:  https://doi.org/10.1007/s11356-015-4104-8 CrossRefGoogle Scholar
  51. Wang Q, Zhang W, Li C, Xiao B (2012) Phytoremediation of atrazine by three emergent hydrophytes in a hydroponic system. Water Sci Tech- nol 66:1282–1288CrossRefGoogle Scholar
  52. Weyens N, van der Lelie D, Taghavi S, Newman L, Vangronsveld J (2009) Exploiting plant-microbe partnerships to improve biomass production and remediation. Trends Biotechnol 27:591–598.  https://doi.org/10.1016/j.tibtech.2009.07.006 CrossRefPubMedGoogle Scholar
  53. Yale RL, Sapp M, Sinclair CJ, Moir JWB (2017) Microbial changes linked to the accelerated degradation of the herbicide atrazine in a range of temperate soils. Environ Sci Pollut Res 24:7359–7374.  https://doi.org/10.1007/s11356-017-8377-y CrossRefGoogle Scholar
  54. Zevenhuizen LPTM (1997) Succinoglycan and galactoglucan. Carbohydr Polym 33:139–144.  https://doi.org/10.1016/S0144-8617(97)00054-4 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature and the University of Milan 2018

Authors and Affiliations

  1. 1.Soil Microbial Ecology and Environmental Toxicology Laboratory, Department of ZoologyUniversity of DelhiDelhiIndia

Personalised recommendations