Elevated level of the second messenger c-di-GMP in Comamonas testosteroni enhances biofilm formation and biofilm-based biodegradation of 3-chloroaniline

Applied Microbiology and Biotechnology

Volumn 99, Issue 4, 2015, Pages 1967-1976

  Wu, Yichao ^a,b   Ding, Yuanzhao ^b,c   Cohen, Yehuda ^b   Cao, Bin ^a,b  

^a NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^b NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

^c NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

Biodegradation; Biofilm; c di GMP; Xenobiotic compound

Indexed keywords

AZO DYES; BIOFILMS; ESCHERICHIA COLI;

BIOFILM DEVELOPMENT; BIOFILM FORMATION; COMAMONAS TESTOSTERONI; HIGH SURFACE-TO-VOLUME RATIO; NOVEL STRATEGIES; SECOND MESSENGER; SUBMERGED BIOFILM REACTOR; XENOBIOTIC COMPOUNDS;

BIODEGRADATION;

3 CHLOROANILINE; ANILINE; CONGO RED; CYCLIC GMP; UNCLASSIFIED DRUG; XENOBIOTIC AGENT; 3-CHLOROANILINE; ANILINE DERIVATIVE; BIS(3',5')-CYCLIC DIGUANYLIC ACID; DIGUANYLATE CYCLASE; ESCHERICHIA COLI PROTEIN; LYASE; RECOMBINANT PROTEIN;

ARTICLE; BACTERIAL GROWTH; BIOFILM; BIOPROCESS; COMAMONAS TESTOSTERONI; CONTROLLED STUDY; ESCHERICHIA COLI; MICROBIAL DEGRADATION; NONHUMAN; PLANKTON; SECOND MESSENGER; SURFACE PROPERTY; WILD TYPE; ANALOGS AND DERIVATIVES; BIOREACTOR; BIOTRANSFORMATION; ENZYMOLOGY; GENE EXPRESSION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MICROBIOLOGY; PHYSIOLOGY;

ANILINE COMPOUNDS; BIOFILMS; BIOREACTORS; BIOTRANSFORMATION; COMAMONAS TESTOSTERONI; CYCLIC GMP; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION; PHOSPHORUS-OXYGEN LYASES; RECOMBINANT PROTEINS; SECOND MESSENGER SYSTEMS;

EID: 84925505634     PISSN: 01757598     EISSN: 14320614     Source Type: Journal    
DOI: 10.1007/s00253-014-6107-7     Document Type: Article

References (65)

1. Andersson S, Kuttuva Rajarao G, Land CJ, Dalhammar G (2008) Biofilm formation and interactions of bacterial strains found in wastewater treatment systems. FEMS Microbiol Lett 283(1):83–90
2. Ariesyady HD, Ito T, Okabe S (2007) Functional bacterial and archaeal community structures of major trophic groups in a full-scale anaerobic sludge digester. Water Res 41(7):1554–1568
3. Boon N, Goris J, De Vos P, Verstraete W, Top EM (2000) Bioaugmentation of activated sludge by an indigenous 3-chloroaniline-degrading Comamonas testosteroni strain, I2gfp. Appl Environ Microbiol 66(7):2906–2913
4. Boon N, De Gelder L, Lievens H, Siciliano SD, Top EM, Verstraete W (2002) Bioaugmenting bioreactors for the continuous removal of 3-chloroaniline by a slow release approach. Environ Sci Technol 36(21):4698–4704
5. Boon N, Top EM, Verstraete W, Siciliano SD (2003) Bioaugmentation as a tool to protect the structure and function of an activated-sludge microbial community against a 3-chloroaniline shock load. Appl Environ Microbiol 69(3):1511–1520
6. Bossier P, Verstraete W (1996) Comamonas testosteroni colony phenotype influences exopolysaccharide production and coaggregation with yeast cells. Appl Environ Microbiol 62(8):2687–2691
7. Cao B, Loh KC (2008) Catabolic pathways and cellular responses of Pseudomonas putida P8 during growth on benzoate with a proteomics approach. Biotechnol Bioeng 101(6):1297–1312
8. Cao B, Nagarajan K, Loh K (2009) Biodegradation of aromatic compounds: current status and opportunities for biomolecular approaches. Appl Microbiol Biotechnol 85(2):207–228
9. Cao B, Majors PD, Ahmed B, Renslow RS, Silvia CP, Shi L, Kjelleberg S, Fredrickson JK, Beyenal H (2012) Biofilm shows spatially stratified metabolic responses to contaminant exposure. Environ Microbiol 14(11):2901–2910
10. Chen CY, Nace GW, Irwin PL (2003) A 6 × 6 drop plate method for simultaneous colony counting and MPN enumeration of Campylobacter jejuni, Listeria monocytogenes, and Escherichia coli. J Microbiol Methods 55(2):475–479
11. Da Re S, Ghigo J (2006) A CsgD-independent pathway for cellulose production and biofilm formation in Escherichia coli. J Bacteriol 188(8):3073–3087
12. Dejonghe W, Berteloot E, Goris J, Boon N, Crul K, Maertens S, Hofte M, De Vos P, Verstraete W, Top EM (2003) Synergistic degradation of linuron by a bacterial consortium and isolation of a single linuron-degrading Variovorax strain. Appl Environ Microbiol 69(3):1532–1541
13. Ding Y, Peng N, Du Y, Ji L, Cao B (2014) Disruption of putrescine biosynthesis in Shewanella oneidensis enhances biofilm cohesiveness and performance in Cr(VI) immobilization. Appl Environ Microbiol 80(4):1498–1506
14. Donlan RM (2002) Biofilms: microbial life on surfaces. Emerg Infect Dis 8(9):881–890
15. Ducey TF, Vanotti MB, Shriner AD, Szogi AA, Ellison AQ (2010) Characterization of a microbial community capable of nitrification at cold temperature. Bioresour Technol 101(2):491–500
16. Flemming H-C, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8(9):623–633
17. Friedman L, Kolter R (2004) Genes involved in matrix formation in Pseudomonas aeruginosa PA14 biofilms. Mol Microbiol 51(3):675–690
18. Gjermansen M, Ragas P, Tolker-Nielsen T (2006) Proteins with GGDEF and EAL domains regulate Pseudomonas putida biofilm formation and dispersal. FEMS Microbiol Lett 265(2):215–224
19. Gjermansen M, Nilsson M, Yang L, Tolker-Nielsen T (2010) Characterization of starvation-induced dispersion in Pseudomonas putida biofilms: genetic elements and molecular mechanisms. Mol Microbiol 75(4):815–826
20. Gupta K, Liao J, Petrova OE, Cherny K, Sauer K (2014) Elevated levels of the second messenger c-di-GMP contribute to antimicrobial resistance of Pseudomonas aeruginosa. Mol Microbiol 92(3):488–506
21. Haagensen JA, Hansen SK, Johansen T, Molin S (2002) In situ detection of horizontal transfer of mobile genetic elements. FEMS Microbiol Ecol 42(2):261–268
22. Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2(2):95–108
23. Hengge R (2009) Principles of c-di-GMP signalling in bacteria. Nat Rev Microbiol 7(4):263–273
24. Henriques ID, Holbrook RD, Kelly RT II, Love NG (2005) The impact of floc size on respiration inhibition by soluble toxicants—a comparative investigation. Water Res 39(12):2559–2568
25. Hickman JW, Tifrea DF, Harwood CS (2005) A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc Natl Acad Sci U S A 102(40):14422–14427
26. Jenal U, Malone J (2006) Mechanisms of cyclic-di-GMP signaling in bacteria. Annu Rev Genet 40:385–407
27. Juang YC, Adav SS, Lee DJ, Lai JY (2010) Influence of internal biofilm growth on residual permeability loss in aerobic granular membrane bioreactors. Environ Sci Technol 44(4):1267–1273
28. Kearney PC, Kaufman DD (1988) Herbicides: chemistry, degradation, and mode of action, vol 3. CRC Press, New York
29. Kim L, Pagaling E, Zuo YY, Yan T (2014) Impact of substratum surface on microbial community structure and treatment performance in biological aerated filters. Appl Environ Microbiol 80(1):177–183
30. Kirisits MJ, Prost L, Starkey M, Parsek MR (2005) Characterization of colony morphology variants isolated from Pseudomonas aeruginosa biofilms. Appl Environ Microbiol 71(8):4809–4821
31. Król J, Penrod J, McCaslin H, Rogers L, Yano H, Stancik A, Dejonghe W, Brown C, Parales R, Wuertz S (2012) Role of IncP-1β plasmids pWDL7::rfp and pNB8c in chloroaniline catabolism as determined by genomic and functional analyses. Appl Environ Microbiol 78(3):828–838
32. Kuchma S, Ballok A, Merritt J, Hammond J, Lu W, Rabinowitz J, O’Toole GA (2010) Cyclic-di-GMP-mediated repression of swarming motility by Pseudomonas aeruginosa: the pilY1 gene and its impact on surface-associated behaviors. J Bacteriol 192(12):2950–2964
33. Linares M, Pruneda-Paz JL, Reyna L, Genti-Raimondi S (2008) Regulation of testosterone degradation in Comamonas testosteroni. J Steroid Biochem Mol Biol 112(1–3):145–150
34. Liu Z, Yang H, Huang Z, Zhou P, Liu S-J (2002) Degradation of aniline by newly isolated, extremely aniline-tolerant Delftia sp. AN3. Appl Microbiol Biotechnol 58(5):679–682
35. Louvet J-N, Giammarino C, Potier O, Pons M-N (2010) Adverse effects of erythromycin on the structure and chemistry of activated sludge. Environ Pollut 158(3):688–693
36. Luo H, Xu P, Ren Z (2012) Long-term performance and characterization of microbial desalination cells in treating domestic wastewater. Bioresour Technol 120:187–193
37. Lyons CD, Katz S, Bartha R (1984) Mechanisms and pathways of aniline elimination from aquatic environments. Appl Environ Microbiol 48(3):491–496
38. Ma Y, Zhang Y, Zhang J, Chen D, Zhu Y, Zheng H, Wang S, Jiang C, Zhao G, Liu S (2009) The complete genome of Comamonas testosteroni reveals its genetic adaptations to changing environments. Appl Environ Microbiol 75(21):6812–6819
39. Mah TFC, O’Toole GA (2001) Mechanisms of biofilm resistance to antimicrobial agents. Trends Microbiol 9(1):34–39
40. Murray TS, Kazmierczak BI (2008) Pseudomonas aeruginosa exhibits sliding motility in the absence of type IV pili and flagella. J Bacteriol 190(8):2700–2708
41. Nicastro GG, Kaihami GH, Pereira TO, Meireles DA, Groleau MC, Déziel E, Baldini RL (2014) Cyclic-di-GMP levels affect Pseudomonas aeruginosa fitness in the presence of imipenem. Environ Microbiol 16(5):1321–1333
42. Nicolella C, van Loosdrecht MCM, Heijnen SJ (2000) Particle-based biofilm reactor technology. Trends Biotechnol 18(7):312–320
43. Parsek MR, Greenberg E (2005) Sociomicrobiology: the connections between quorum sensing and biofilms. Trends Microbiol 13(1):27–33
44. Principi P, Villa F, Bernasconi M, Zanardini E (2006) Metal toxicity in municipal wastewater activated sludge investigated by multivariate analysis and in situ hybridization. Water Res 40(1):99–106
45. Pruneda-Paz JL, Linares M, Cabrera JE, Genti-Raimondi S (2004) TeiR, a LuxR-type transcription factor required for testosterone degradation in Comamonas testosteroni. J Bacteriol 186(5):1430–1437
46. Reardon KF, Mosteller DC, Rogers JDB (2000) Biodegradation kinetics of benzene, toluene, and phenol as single and mixed substrates for Pseudomonas putida F1. Biotechnol Bioeng 69(4):385–400
47. Sanchez-Torres V, Hu H, Wood TK (2011) GGDEF proteins YeaI, YedQ, and YfiN reduce early biofilm formation and swimming motility in Escherichia coli. Appl Microbiol Biotechnol 90(2):651–658
48. Simm R, Morr M, Kader A, Nimtz M, Romling U (2004) GGDEF and EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol 53(4):1123–1134
49. Singh R, Paul D, Jain RK (2006) Biofilms: implications in bioremediation. Trends Microbiol 14(9):389–397
50. Sivakumar K, Wang VB, Chen X, Bazan GC, Kjelleberg S, Loo SCJ, Cao B (2014) Membrane permeabilization underlies the enhancement of extracellular bioactivity in Shewanella oneidensis by a membrane-spanning conjugated oligoelectrolyte. Appl Microbiol Biotechnol. doi:10.1007/s00253-014-5973-3
51. Snaidr J, Amann R, Huber I, Ludwig W, Schleifer K-H (1997) Phylogenetic analysis and in situ identification of bacteria in activated sludge. Appl Environ Microbiol 63(7):2884–2896
52. Spangler C, Böhm A, Jenal U, Seifert R, Kaever V (2010) A liquid chromatography-coupled tandem mass spectrometry method for quantitation of cyclic di-guanosine monophosphate. J Microbiol Methods 81(3):226–231
53. Spurbeck RR, Tarrien RJ, Mobley HL (2012) Enzymatically active and inactive phosphodiesterases and diguanylate cyclases are involved in regulation of motility or sessility in Escherichia coli CFT073. MBiol 3(5):e00307–e00312
54. Suja E, Nancharaiah YV, Venugopalan VP (2012) p-Nitrophenol biodegradation by aerobic microbial granules. Appl Biochem Biotechnol 167(6):1569–1577
55. Thangaraj K, Kapley A, Purohit HJ (2008) Characterization of diverse Acinetobacter isolates for utilization of multiple aromatic compounds. Bioresour Technol 99(7):2488–2494
56. Ueda A, Wood TK (2009) Connecting quorum sensing, c-di-GMP, pel polysaccharide, and biofilm formation in Pseudomonas aeruginosa through tyrosine phosphatase TpbA (PA3885). PLoS Pathog 5(6):e1000483
57. Valle A, Bailey MJ, Whiteley AS, Manefield M (2004) N-acyl-l-homoserine lactones (AHLs) affect microbial community composition and function in activated sludge. Environ Microbiol 6(4):424–433
58. Wakimoto N, Nishi J, Sheikh J, Nataro JP, Sarantuya J, Iwashita M, Manago K, Tokuda K, Yoshinaga M, Kawano Y (2004) Quantitative biofilm assay using a microtiter plate to screen for enteroaggregative Escherichia coli. Am J Trop Med Hyg 71(5):687–690
59. Wan C, Zhang P, Lee D-J, Yang X, Liu X, Sun S, Pan X (2013) Disintegration of aerobic granules: role of second messenger cyclic di-GMP. Bioresour Technol 146:330–335
60. Willems A, Vos P (2006) Comamonas. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes. Springer, New York, pp 723–736
61. Wolfe AJ, Visick KL (2008) Get the message out: cyclic-Di-GMP regulates multiple levels of flagellum-based motility. J Bacteriol 190(2):463–475
62. Ye L, Shao M, Zhang T, Tong AHY, Lok S (2011) Analysis of the bacterial community in a laboratory-scale nitrification reactor and a wastewater treatment plant by 454-pyrosequencing. Water Res 45(15):4390–4398
63. Yong Y, Zhong J (2013) Regulation of aromatics biodegradation by rhl quorum sensing system through induction of catechol meta-cleavage pathway. Bioresour Technol 136:761–765
64. Zhang T, Shao M, Ye L (2011) 454 Pyrosequencing reveals bacterial diversity of activated sludge from 14 sewage treatment plants. ISME J 6(6):1137–1147
65. Zhang Y, Ng CK, Cohen Y, Cao B (2014) Cell growth and protein expression of Shewanella oneidensis in biofilms and hydrogel-entrapped cultures. Mol Biosyst 10(5):1035–1042