Roles of extracellular polysaccharides and biofilm formation in heavy metal resistance of rhizobia

Materials

Volumn 9, Issue 6, 2016, Pages

  Nocelli, Natalia ^a   Bogino, Pablo C ^a   Banchio, Erika ^a   Giordano, Walter ^a  

^a DEPARTAMENTO DE QUÍMICA   (Argentina)

Author keywords

Bacterial rescue; Biofilm; Co culture; Exopolysaccharides; Metal toxicity; S. meliloti

Indexed keywords

BACTERIA; BIOFILMS; HEAVY METALS; METABOLITES; NITROGEN FIXATION; POLYSACCHARIDES;

BACTERIAL RESCUE; CO-CULTURES; EXOPOLYSACCHARIDES; METAL TOXICITY; S. MELILOTI;

MERCURY COMPOUNDS;

EID: 84975717687     PISSN: None     EISSN: 19961944     Source Type: Journal    
DOI: 10.3390/ma9060418     Document Type: Article

References (67)

1. Gage, D.J. Infection and invasion of roots by symbiotic, nitrogen-fixing rhizobia during nodulation of temperate legumes. Microbiol. Mol. Biol. Rev. 2004, 68, 280-300.
2. Jones, K.M.; Kobayashi, H.; Davies, B.W.; Taga, M.E.; Walker, G.C. How rhizobial symbionts invade plants: The Sinorhizobium-Medicago model. Nature Rev. Microbiol. 2007, 5, 619-633.
3. Janczarek, M. Environmental signals and regulatory pathways that influence exopolysaccharide production in rhizobia. Int. J. Mol. Sci. 2011, 12, 7898-7933.
4. Cheng, H.P.; Walker, G.C. Succinoglycan is required for initiation and elongation of infection threads during nodulation of alfalfa by Rhizobium meliloti. J. Bacteriol. 1998, 180, 5183-5191.
5. Reuber, T.L.;Walker, G.C. Biosynthesis of succinoglycan, a symbiotically important exopolysaccharide of Rhizobium meliloti. Cell 1993, 74, 269-280.
6. Spaink, H.P. Root nodulation and infection factors produced by rhizobial bacteria. Annu. Rev. Microbiol. 2000, 54, 257-288.
7. Skorupska, A.; Janczarek, M.; Marczak, M.; Mazur, A.; Król, J. Rhizobial exopolysaccharides: Genetic control and symbiotic functions. Microb. Cell Fact. 2006, 5, 7.
8. Pellock, B.J.; Teplitski, M.; Boinay, R.P.; Bauer, W.D.;Walker, G.C. A LuxR homolog controls production of symbiotically active extracellular polysaccharide II by Sinorhizobium meliloti. J. Bacteriol. 2002, 184, 5067-5076.
9. Glazebrook, J.; Walker, G.C. A novel exopolysaccharide can function in place of the calcofluor-binding exopolysaccharide in nodulation of alfalfa by Rhizobium meliloti. Cell 1989, 56, 661-672.
10. Davey, M.E.; O'Toole, G.A. Microbial biofilms: From ecology to molecular genetics. Microbiol. Mol. Biol. Rev. 2000, 64, 847-867.
11. Branda, S.S.; Vik, S.; Friedman, L.; Kolter, R. Biofilms: The matrix revisited. Trends Microbiol. 2005, 13, 20-26.
12. Costerton, J.W.; Lewandowski, Z.; Caldwell, D.E.; Korber, D.R.; Lappin-Scott, H.M. Microbial biofilms. Annu. Rev. Microbiol. 1995, 49, 711-745.
13. Rinaudi, L.V.; Giordano, W. An integrated view of biofilm formation in rhizobia. FEMS Microbiol. Lett. 2010, 304, 1-11.
14. Rinaudi, L.; Fujishige, N.A.; Hirsch, A.M.; Banchio, E.; Zorreguieta, A.; Giordano, W. Effects of nutritional and environmental conditions on Sinorhizobium meliloti biofilm formation. Res. Microbiol. 2006, 157, 867-875.
15. Fujishige, N.A.; Kapadia, N.N.; De Hoff, P.L.; Hirsch, A.M. Investigations of Rhizobium biofilm formation. FEMS Microbiol. Ecol. 2006, 56, 195-206.
16. Rinaudi, L.V.; González, J.E. The low-molecular-weight fraction of the exopolysaccharide II from Sinorhizobium meliloti is a crucial determinant of biofilm formation. J. Bacteriol. 2009, 191, 7216-7224.
17. Sorroche, F.G.; Rinaudi, L.V.; Zorreguieta, A.; Giordano, W. EPS II-dependent autoaggregation of Sinorhizobium meliloti planktonic cells. Curr. Microbiol. 2010, 61, 465-470.
18. Sorroche, F.G.; Spesia, M.B.; Zorreguieta, A.; Giordano, W. A positive correlation between bacterial autoaggregation and biofilm formation in native Sinorhizobium meliloti isolates from Argentina. Appl. Environ. Microbiol. 2012, 78, 4092-4101.
19. Ledin, M. Accumulation of metals by microorganisms-processes and importance for soil systems. Earth Sci. Rev. 2000, 51, 1-31.
20. Kazy, S.K.; Sar, P.; Singh, S.P.; Sen Asish, K.; D'Souza, S.F. Extracellular polysaccharides of a copper-sensitive and a copper-resistant Pseudomonas aeruginosa strain: Synthesis, chemical nature and copper binding. World J. Microbiol. Biotechnol. 2002, 18, 583-588.
21. González, A.G.; Shirokova, L.S.; Pokrovsky, O.S.; Emnova, E.E.; Martínez, R.E.; Santana-Casiano, J.M.; González-Dávila, M.; Pokrovski, G.S. Adsorption of copper on Pseudomonas aureofaciens: Protective role of surface exopolysaccharides. J. Colloid Interface Sci. 2010, 350, 305-314.
22. Corzo, J.; León-Barrios, M.; Hernando-Rico, V.; Gutierrez-Navarro, A.M. Precipitation of Metallic Cations by the Acidic Exopolysaccharides from Bradyrhizobium japonicum and Bradyrhizobium (Chamaecytisus) Strain BGA-1. Appl. Environ. Microbiol. 1994, 12, 4531-4536.
23. Foster, L.J.R.; Moy, Y.P.; Rogers, P.L. Metal binding capabilities of Rhizobium etli and its extracellular polymeric substances. Biotechnol. Lett. 2000, 22, 1757-1760.
24. Slaveykova, V.I.; Parthasarathy, N.; Dedieu, K.; Toescher, D. Role of extracellular compounds in Cd-sequestration relative to Cd uptake by bacterium Sinorhizobium meliloti. Environ. Pollut. 2010, 158, 2561-2565.
25. Avelar Ferreira, P.A.; Bomfeti, C.A.; Lima Soares, B.; de Souza Moreira, F.M. Efficient nitrogen-fixing Rhizobium strains isolated from amazonian soils are highly tolerant to acidity and aluminium. World J. Microbiol. Biotechnol. 2012, 28, 1947-1959.
26. Chang, W.C.; Hu, G.S.; Chiang, S.M.; Su, M.C. Heavy metal removal from aqueous solution by wasted biomass from a combined AS-biofilm process. Bioresour. Technol. 2006, 97, 1503-1508.
27. Younis, M. Responses of Lablab purpureus-Rhizobium symbiosis to heavy metals in pot and field experiments. World J. Agric. Sci. 2007, 3, 111-122.
28. Paul, D.; Poddar, S.; Sar, P. Characterization of arsenite-oxidizing bacteria isolated from arsenic-contaminated groundwater ofWest Bengal. J. Environ. Sci. Heal. 2014, 49, 1481-1492.
29. Armendariz, A.L.; Talano, M.A.;Wevar Oller, A.L.; Medina, M.I.; Agostini, E. Effect of arsenic on tolerance mechanisms of two plant growth-promoting bacteria used as biological inoculants. J. Environ. Sci. 2015, 33, 203-210.
30. 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, 2336-2342.
31. Marchal, M.; Briandet, R.; Halter, D.; Koechler, S.; DuBow, M.S.; Lett, M.C. Subinhibitory arsenite concentrations lead to population dispersal in Thiomonas sp. PLoS ONE 2011, 6, e23181.
32. Barkay, T.; Miller, S.M.; Summers, A.O. Bacterial mercury resistance from atoms to ecosystems. FEMS Microbiol. Rev. 2003, 27, 355-384.
33. Schneiker, S.; Keller, M.; Dröge, M.; Lanka, E.; Pühler, A.; Selbitschka, W. The genetic organization and evolution of the broad host range mercury resistance plasmid pSB102 isolated from a microbial population residing in the rhizosphere of alfalfa. Nucleic Acids Res. 2001, 29, 5169-5181.
34. Norberg, P.; Bergström, M.; Hermansson, M. Complete nucleotide sequence and analysis of two conjugative broad host range plasmids from a marine microbial biofilm. PLoS ONE 2014, 9, e92321.
35. Yang, H.-C.; Cheng, J.; Finan, T.M.; Rosen, B.P.; Bhattacharjee, H. Novel pathway for arsenic detoxification in the legume symbiont Sinorhizobium meliloti. J. Bacteriol. 2005, 187, 6991-6997.
36. Ye, J.; Yang, H.C.; Rosen, B.P.; Bhattacharjee, H. Crystal structure of the flavoprotein ArsH from Sinorhizobium meliloti. FEBS Lett. 2007, 581, 3996-4000.
37. Li, Z.F.; Ma, Z.Q.; Hao, X.L.; Rensing, C.; Wei, G.H. Genes conferring copper resistance in Sinorhizobium meliloti CCNWSX0020 also promote the growth of Medicago lupulina in copper contaminated soil. Appl. Environ. Microbiol. 2014, 80, 1961-1971.
38. Letelier, M.E.; Sebastian, S.J.; Liliana, P.S.; Cortés-Troncoso, J.; Aracena-Parks, P. Mechanisms underlying iron and copper ions toxicity in biological systems: Pro-oxidant activity and protein-binding effects. Chem. Biol. Interact. 2010, 188, 220-227.
39. Li, Z.F.; Ma, Z.Q.; Hao, X.L.; Wei, G.H. Draft genome sequence of Sinorhizobium meliloti CCNWSX0020, a nitrogen-fixing symbiont with copper tolerance capability isolated from lead-zinc mine tailings. J. Bacteriol. 2012, 194, 1267-1268.
40. Raimunda, D.; Elso-Berberián, G. Functional characterization of the CDF transporter SMc02724 (SmYiiP) in Sinorhizobium meliloti: Roles in manganese homeostasis and nodulation. Biochim. Biophys. Acta 2014, 1838, 3203-3211.
41. Teitzel, G.M.; Parsek, M.R. Heavy metal resistance of biofilm and planktonic Pseudomonas aeruginosa. Appl. Environ. Microbiol. 2003, 69, 2313-2320.
42. Muller, D.; Médigue, C.; Koechler, S. A tale of two oxidation states: Bacterial colonization of arsenic-rich environments. PLoS Genet. 2007, 3, e53.
43. Weiss, S.; Carapito, C.; Cleiss, J.; Koechler, S.; Turlin, E.; Coppee, J.-Y.; Heymann, M.; Kugler, V.; Stauffert, M.; Cruveiller, S.; et al. Enhanced structural and functional genome elucidation of the arsenite-oxidizing strain Herminiimonas arsenicoxydans by proteomics data. Biochimie 2009, 91, 192-203.
44. Muller, D.; Lièvremont, D.; Simeonova, D.D.; Hubert, J.-C.; Lett, M.-C. Arsenite oxidase aox genes from a metal-resistant β-proteobacterium. J. Bacteriol. 2003, 185, 135-141.
45. Carapito, C.; Muller, D.; Turlin, E. Identification of genes and proteins involved in the pleiotropic response to arsenic stress in Caenibacter arsenoxydans, a metalloresistant β-proteobacterium with an unsequenced genome. Biochimie 2006, 88, 595-606.
46. Jiao, Y.; Cody, G.D.; Harding, A.K.; Wilmes, P.; Schrenk, M.; Wheeler, K.E.; Banfield, J.F.; Thelen, M.P. Characterization of extracellular polymeric substances from acidophilic microbial biofilms. Appl. Environ. Microbiol. 2010, 76, 2916-2922.
47. Burmølle, M.;Webb, J.S.; Rao, D.; Hansen, L.H.; Sørensen, S.J.; Kjelleberg, S. Enhanced biofilm formation and increased resistance towards antimicrobial agents and bacterial invasion are caused by synergistic interactions in multi-species biofilms. Appl. Environ. Microbiol. 2006, 72, 3916-3923.
48. Kawarai, T.; Furukawa, S.; Ogihara, H.; Yamasaki, M. Mixed-species biofilm formation by lactic acid bacteria and rice wine yeasts. Appl. Environ. Microbiol. 2007, 73, 4673-4676.
49. Palmer, R.J.; Stoodley, P. Biofilms 2007: Broadened horizons and new emphases. J. Bacteriol. 2007, 189, 7948-7960.
50. Filoche, S.K.; Anderson, S.A.; Sissons, C.H. Biofilm growth of Lactobacillus species is promoted by Actinomyces species and Streptococcus mutans. Oral Microbiol. Immun. 2004, 19, 322-326.
51. Yoshida, S.; Ogawa, N.; Fujii, T.; Tsushima, S. Enhanced biofilm formation and 3-chlorobenzoate degrading activity by the bacterial consortium of Burkholderia sp. NK8 and Pseudomonas aeruginosa PAO1. J. Appl. Microbiol. 2009, 106, 790-800.
52. An, D.; Danhorn, T.; Fuqua, C.; Parsek, M.R. Quorum sensing and motility mediate interactions between Pseudomonas aeruginosa and Agrobacterium tumefaciens in biofilm cocultures. Proc. Natl. Acad. Sci. USA 2006, 7, 3828-3833.
53. Singh, R.; Debarati, P.; Rakesh, K.J. Biofilms: Implications in bioremediation. Trends Microbiol. 2006, 14, 389-397.
54. Wagner-Döbler, I.; Lünsdorf, H.; Lübbehü Sen, T.; von Canstein, H.F.; Li, Y. Structure and species composition of mercury-reducing biofilms. Appl. Environ. Microbiol. 2000, 66, 4559-4563.
55. Von Canstein, H.; Li, Y.; Leonhauser, J.; Haase, E.; Felske, A.; Deckwer, W.D.; Wagner-Döbler, I. Spatially oscillating activity and microbial succession of mercury-reducing biofilms in a technical-scale bioremediation system. Appl. Environ. Microbiol. 2002, 68, 1938-1946.
56. Joshi, N.; Ngwenya, B.T.; French, C.E. Enhanced resistance to nanoparticle toxicity is conferred by overproduction of extracellular polymeric substances. J. Hazard. Mater. 2012, 241, 363-370.
57. Flemming, H.C.; Wingender, J. Relevance of microbial extracellular polymeric substances (EPSs). Part I. Structural and ecological aspects. Water Sci. Technol. 2001, 43, 1-8.
58. Denton, B. Advances in phytoremediation of heavy metals using plant growth promoting bacteria and fungi. Basic Biotechnol. 2007, 3, 1-5.
59. Gupta, G.; Bhaskaran, H.; Kananen, G.; Okoh, J. Biodegradation of 2, 4-dinitrotoluene using poultry litter leachate. J. Hazard Mater. 2004, 113, 137-140.
60. Wani, P.A.; Khan, M.S.; Zaidi, A. Chromium-reducing and plant growth-promoting Mesorhizobium improves chickpea growth in chromium-amended soil. Biotechnol. Lett. 2008, 30, 159-163.
61. Wani, P.A.; Khan, M.S.; Zaidi, A. Effect of metal-tolerant plant growth-promoting Rhizobium on the performance of pea grown in metal-amended soil. Arch. Environ. Contam. Toxicol. 2008, 55, 33-42.
62. Wani, P.A.; Khan, M.S.; Zaidi, A. Impact of zinc-tolerant plant growth-promoting rhizobacteria on lentil grown in zinc-amended soil. Agron. Sustain. Dev. 2008, 28, 449-455.
63. Jian, S.G.; Shen, W.J.; Yang, Z.Y. Enhanced adaptability of Sesbania rostrata to Pb/Zn tailings via stem nodulation. J. Environ. Sci. 2009, 21, 1135-1141.
64. Xie, P.; Hao, X.; Herzberg, M.; Luo, Y.; Nies, D.H.; Wei, G. Genomic analyses of metal resistance genes in three plant growth promoting bacteria of legume plants in Northwest mine tailings, China. J. Environ. Sci. 2015, 27, 179-187.
65. Beringer, J.E. R factor transfer in Rhizobium leguminosarum. J. Gen. Microbiol. 1974, 84, 188-198.
66. Somasegaran, P.; Hoben, H.J. Handbook for Rhizobia. Methods in Legume-Rhizobium Technology; Springer-Verlag Inc.: New York, NY, USA, 1994.
67. 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, 449-461.