Effect of arsenic on tolerance mechanisms of two plant growth-promoting bacteria used as biological inoculants

Journal of Environmental Sciences (China)

Volumn 33, Issue , 2015, Pages 203-210

  Armendariz, Ana L ^a   Talano, Melina A ^a   Wevar Oller, Ana L ^a   Medina, María I ^a   Agostini, Elizabeth ^a  

^a DEPARTAMENTO DE QUÍMICA   (Argentina)

Author keywords

Accumulation; Arsenic; Biofilm; Colonization; Exopolysaccharides; Plant growth promoting rhizobacteria

Indexed keywords

ARSENIC; BIOFILMS; SOIL POLLUTION; SOILS;

ACCUMULATION; AZOSPIRILLUM BRASILENSE; BRADYRHIZOBIUM JAPONICUM; COLONIZATION; EXOPOLYSACCHARIDES; PLANT GROWTH PROMOTING BACTERIUM; PLANT GROWTH PROMOTING RHIZOBACTERIA; TOLERANCE MECHANISMS;

BACTERIA;

ARSENIC; CONTAMINATED LAND; GROWTH RATE; GROWTH RESPONSE; INOCULATION; MICROBIAL ACTIVITY; PLANT; POLLUTION TOLERANCE; RHIZOBACTERIUM; RHIZOSPHERE; SOIL POLLUTION;

AZOSPIRILLUM; AZOSPIRILLUM BRASILENSE; BACTERIA (MICROORGANISMS); BRADYRHIZOBIUM; BRADYRHIZOBIUM JAPONICUM; GLYCINE MAX; RHIZOBIALES;

ARSENIC; SOIL POLLUTANT;

AZOSPIRILLUM BRASILENSE; BIOFILM; BIOMASS; BRADYRHIZOBIUM; CHEMISTRY; DRUG EFFECTS; METABOLISM; MICROBIAL VIABILITY; MOVEMENT (PHYSIOLOGY); SOIL POLLUTANT; TOXICITY;

ARSENIC; AZOSPIRILLUM BRASILENSE; BIOFILMS; BIOMASS; BRADYRHIZOBIUM; MICROBIAL VIABILITY; MOVEMENT; SOIL POLLUTANTS;

EID: 84937560570     PISSN: 10010742     EISSN: 18787320     Source Type: Journal    
DOI: 10.1016/j.jes.2014.12.024     Document Type: Article

References (49)

1. Achour A.R., Bauda P., Billard P. Diversity of arsenite transporter genes from arsenic-resistant soil bacteria. Res. Microbiol. 2007, 158(2):128-137.
2. Andres J., Arsène-Ploetze F., Barbe V., Brochier-Armanet C., Cleiss-Arnold J., Coppée J.Y., et al. Life in an arsenic-containing gold mine, genome and physiology of the autotrophic arsenite-oxidizing bacterium Rhizobium sp. NT-26. Genome Biol. Evol. 2013, 5(5):934-953.
3. Borucki M.K., Peppin J.D., White D., Loge F., Call D.R. Variation in biofilm formation among strains of Listeria monocytogenes. Appl. Environ. Microbiol. 2003, 69(12):7336-7342.
4. T. BMC Microbiol. 2008, 8:95.
5. Burdman S., Okon Y., Jurkevitch E. Surface characteristics of Azospirillum brasilense in relation to cell aggregation and attachment to plant roots. Crit. Rev. Microbiol. 2000, 26(2):91-110.
6. Carlin A., Shi W., Dey S., Rosen B.P. The ars operon of Escherichia coli confers arsenical and antimonial resistance. J. Bacteriol. 1995, 177(4):981-986.
7. Cassán F.D., Perrig D.S., Sgroy V., Masciarelli O., Penna C., Luna V. Azospirillum brasilense Az39 and Bradyrhizobium japonicum E109, inoculated singly or in combination, promote seed germination and early seedling growth in corn (Zea mays L.) and soybean (Glycine max L.). Eur. J. Soil Biol. 2009, 45(1):28-35.
8. Chang J.S., Yoon I.H., Lee J.H., Kim K.R., An J., Kim K.W. Arsenic detoxification potential of aox genes in arsenite-oxidizing bacteria isolated from natural and constructed wetlands in the Republic of Korea. Environ. Geochem. Health 2010, 32(2):95-105.
9. Chauhan N.S., Ranjan R., Purohit H.J., Kalia V.C., Sharma R. Identification of genes conferring arsenic resistance to Escherichia coli from an effluent treatment plant sludge metagenomic library. FEMS Microbiol. Ecol. 2009, 67(1):130-139.
10. Costerton J.W., Stewart P.S., Greenberg E.P. Bacterial biofilm: a common cause of persistent infections. Science 1999, 284(5418):1318-1322.
11. Das H.K., Mitra A.K., Sengupta P.K., Hossain A., Islam F., Rabbani G.H. Arsenic concentrations in rice, vegetables, and fish in Bangladesh, a preliminary study. Environ. Int. 2004, 30(3):383-387.
12. Díaz-Zorita M., Grove J. Wheat grain response to nitrogen fertilization and field inoculation with a liquid formulation of Azospirillum brasilense, ASA-CSSA-SSSA. Abstracts of International Annual Meetings, Indianapolis, U.S.A. 2006, 25031.
13. Díaz-Zorita M., Baliña R.M., Fernández-Canigia M.V., Penna C., Perticari A. Field inoculation of wheat and maize with a liquid formulation of Azospirillum brasilense in the Pampas, Argentina, ASA-CSSA-SSSA. Abstracts of International Annual Meetings, Seattle, U.S.A. 2004, 4898.
14. Dische Z. General color reactions. Methods Carbohydr. Chem. 1962, 1:477-479.
15. Drenkard E. Antimicrobial resistance of Pseudomonas aeruginosa biofilms. Micr. Infect. 2003, 5(13):1213-1219.
16. Farías S.S., Casa V.A., Vázquez C., Ferpozzi L., Pucci G.N., Cohen I.M. Natural contamination with arsenic and other trace elements in ground waters of Argentine Pampean Plain. Sci. Total Environ. 2003, 309(1-3):187-199.
17. Fujishige N.A., Kapadia N.N., De Hoff P.L., Hirsch A.M. Investigations of Rhizobium biofilm formation. FEMS Microbiol. Ecol. 2006, 56(2):195-206.
18. Gihring T.M., Banfield J.F. Arsenite oxidation and arsenate respiration by a new Thermus isolate. FEMS Microbiol. Lett. 2001, 204(2):335-340.
19. Guibaud G., van Hullebusch E., Bordas F. Lead and cadmium biosorption by extracellular polymeric substances (EPS) extracted from activated sludges, pH-sorption edge tests and mathematical equilibrium modeling. Chemosphere 2006, 64(11):1955-1962.
20. Harrison J.J., Ceri H., Turner R.J. Multimetal resistance and tolerance in microbial biofilms. Nat. Rev. Microbiol. 2007, 5(12):928-938.
21. Hibbing M.E., Fuqua C., Parsek M.R., Peterson S.B. Bacterial competition, surviving and thriving in the microbial jungle. Nat. Rev. Microbiol. 2010, 8(1):15-25.
22. Hume D.J., Blair D.H. Effect of numbers of Bradyrhizobium japonicum applied in commercial inoculants on soybean yield in Ontario. Can. J. Microbiol. 1992, 38(6):588-593.
23. Islam F.S., Gault A.G., Boothman C., Polya D.A., Charnock J.M., Chatterjee D., et al. Role of metal-reducing bacteria in arsenic release from Bengal delta sediments. Nature 2004, 430(6995):68-71.
24. Kanbe M., Yagasaki J., Zehner S., Göttfert M., Aizawa S.I. Characterization of two sets of subpolar flagella in Bradyrhizobium japonicum. J. Bacteriol. 2007, 189(3):1083-1089.
25. Kashyap D.R., Botero L.M., Franck W.L., Hassett D.J., McDermott T.R. Complex regulation of arsenite oxidation in Agrobacterium tumefaciens. J. Bacteriol. 2006, 188(3):1081-1088.
26. Kearns D.B. A field guide to bacterial swarming motility. Nat. Rev. Microbiol. 2010, 8(9):634-644.
27. Lyubun Y.V., Fritzsche A., Chernyshova M.P., Dudel E.G., Fedorov E.E. Arsenic transformation by Azospirillum brasilense Sp245 in association with wheat (Triticum aestivum L.) roots. Plant Soil 2006, 286(1-2):219-227.
28. Marchal M., Briandet R., Koechler S., Kammerer B., Bertin P.N. Effect of arsenite on swimming motility delays surface colonization in Herminiimonas arsenicoxydans. Microbiology 2010, 156(8):2336-2342.
29. Marchal M., Briandet R., Halter D., Koechler S., DuBow M.S., Lett M.C., et al. Subinhibitory arsenite concentrations lead to population dispersal in Thiomonas sp. PLoS One 2011, 6(8):e23181.
30. Mueller K., González J.E. Complex regulation on symbiotic functions is coordinated by MucR and quorum sensing in Sinorhizobium meliloti. J. Bacteriol. 2011, 193:485-496.
31. Muller D., Médigue C., Koechler S., Barbe V., Barakat M., Talla E., et al. A tale of two oxidation states, bacterial colonization of arsenic-rich environments. PLoS Genet. 2007, 3(4):e53.
32. O'Toole G.A., Kolter R. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signaling pathways: a genetic analysis. Mol. Microbiol. 1998, 28(3):449-461.
33. Oremland R.S., Stolz J.F. The ecology of arsenic. Science 2003, 300(5621):939-944.
34. Oremland R.S., Kulp T.R., Blum J.S., Hoeft S.E., Baesman S., Miller L.G., et al. A microbial arsenic cycle in a salt-saturated, extreme environment. Science 2005, 308(5726):1305-1308.
35. Park K.M., So J.S. Altered cell surface hydrophobicity of lipopolysaccharide-deficient mutant of Bradyrhizobium japonicum. J. Microbiol. Methods 2000, 41(3):219-226.
36. Ressia J.M., Lázaro L., Lett L.C., Mendivil G.O., Portela G.R., Balbuena R.H. Tillage systems and inoculation in soybean effects on growth and yield. Agrociencia 2003, 37:167-176.
37. Rosen B.P. Biochemistry of arsenic detoxification. FEBS Lett. 2002, 529(1):86-92.
38. Sheng G.P., Yu H.Q., Yue Z.B. Production of extracellular polymeric substances from Rhodopseudomonas acidophila in the presence of toxic substances. Appl. Microbiol. Biotechnol. 2005, 69(2):216-222.
39. Silver S., Phung L.T. Genes and enzymes involved in bacterial oxidation and reduction of inorganic arsenic. Appl. Environ. Microbiol. 2005, 71(2):599-608.
40. Silver S., Budd K., Leahy K.M., Shaw W.V., Hammond D., Novick R.P., et al. Inducible plasmid-determined resistance to arsenate, arsenite, and antimony (III) in Escherichia coli and Staphylococcus aureus. J. Bacteriol. 1981, 146(3):983-996.
41. Smedley P.L., Kinniburgh D.G. A review of the source, behavior and distribution of arsenic in natural waters. Appl. Geochem. 2002, 17(5):517-568.
42. Somasegaran P., Hoben H.J. General microbiology of rhizobia-evaluating symbiotic potential of rhizobia. Handbook for Rhizobia 1994, 171-176. Springer, New York. P. Somasegaran, H.J. Hoben (Eds.).
43. Srivastava S., Sharma Y.K. Altered growth, photosynthetic machinery and induced oxidative stress in spinach in response to arsenic stress. J. Plant Physiol. Pathol. 2013, 1:4.
44. Stoodley P., Cargo R., Rupp C.J., Wilson S., Klapper I. Biofilm material properties as related to shear-induced deformation and detachment phenomena. J. Ind. Microbiol. Biotechnol. 2002, 29(6):361-367.
45. Sutherland I.W. Biofilm exopolysaccharides: a strong and sticky framework. Microbiology 2001, 147(1):3-9.
46. Talano M.A., Cejas R.B., González P.S., Agostini E. Arsenic effect on the model crop symbiosis Bradyrhizobium-soybean. Plant Physiol. Biochem. 2013, 63:8-14.
47. Teitzel G.M., Parsek M.R. Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. Appl. Environ. Microbiol. 2003, 69(4):2313-2320.
48. Vorontsov I.I., Minasov G., Brunzelle J.S., Shuvalova L., Kiryukhina O., Collart F.R., et al. Crystal structure of an apo form of Shigella flexneri ArsH protein with an NADPH-dependent FMN reductase activity. Prot. Sci. 2007, 16(11):2483-2490.
49. Ye J., Yang H.C., Rosen B.P., Bhattacharjee H. Crystal structure of the flavoprotein ArsH from Sinorhizobium meliloti. FEBS Lett. 2007, 581(21):3996-4000.