Browse > Article
http://dx.doi.org/10.4014/jmb.1307.07041

Effects of Nutritional and Environmental Conditions on Planktonic Growth and Biofilm Formation of Citrobacter werkmanii BF-6  

Zhou, Gang (Guangdong Institute of Microbiology, State Key Laboratory of Applied Microbiology, South China (The Ministry-Province Joint Development))
Li, Long-Jie (Guangdong Institute of Microbiology, State Key Laboratory of Applied Microbiology, South China (The Ministry-Province Joint Development))
Shi, Qing-Shan (Guangdong Institute of Microbiology, State Key Laboratory of Applied Microbiology, South China (The Ministry-Province Joint Development))
Ouyang, You-Sheng (Guangdong Institute of Microbiology, State Key Laboratory of Applied Microbiology, South China (The Ministry-Province Joint Development))
Chen, Yi-Ben (Guangdong Institute of Microbiology, State Key Laboratory of Applied Microbiology, South China (The Ministry-Province Joint Development))
Hu, Wen-Feng (College of Food Science, South China Agricultural University)
Publication Information
Journal of Microbiology and Biotechnology / v.23, no.12, 2013 , pp. 1673-1682 More about this Journal
Abstract
Citrobacter sp. is a cause of significant opportunistic nosocomial infection and is frequently found in human and animal feces, soil, and sewage water, and even in industrial waste or putrefaction. Biofilm formation is an important virulence trait of Citrobacter sp. pathogens but the process and characteristics of this formation are unclear. Therefore, we employed in vitro assays to study the nutritional and environmental parameters that might influence biofilm formation of C. werkmanii BF-6 using 96-well microtiter plates. In addition, we detected the relative transcript levels of biofilm formation genes by RT-PCR. Our results indicated that the capacity of C. werkmanii BF-6 to form biofilms was affected by culture temperature, media, time, pH, and the osmotic agents glucose, sucrose, NaCl, and KCl. Confocal laser scanning microscopy results illustrated that the structure of biofilms and extracellular polysaccharide was influenced by 100 mM NaCl or 100 mM KCl. In addition, nine biofilm formation genes (bsmA, bssR, bssS, csgD, csgE, csgF, mrkA, mrkB, and mrkE) were found to contribute to planktonic and biofilm growth. Our data suggest that biofilm formation by C. werkmanii BF-6 is affected by nutritional and environmental factors, which could pave the way to the prevention and elimination of biofilm formation using proper strategies.
Keywords
Citrobacter werkmanii BF-6; biofilm formation; nutritional and environmental conditions; confocal laser scanning microscopy; real-time RT-PCR;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Stanley NR, Lazazzera BA. 2004. Environmental signals and regulatory pathways that influence biofilm formation. Mol. Microbiol. 52: 917-924.   DOI   ScienceOn
2 Stepanovic S, Vukovic D, Dakic I, Savic B, Svabic-Vlahovic M. 2000. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J. Microbiol. Methods 40: 175-179.   DOI   ScienceOn
3 Stoodley P, Sauer K, Davies D, Costerton J. 2002. Biofilms as complex differentiated communities. Annu. Rev. Microbiol. 56: 187-209.   DOI   ScienceOn
4 Tang QY, Feng MG. 2007. Statistical analysis of the test, pp. 59-142. In Yan DP, Zhao YC, Yang R (eds.). DPS Data Processing System: Experimental Design, Statistical Analysis and Data Mining. Science Press, Beijing.
5 Vallet I, Diggle SP, Stacey RE, Cámara M, Ventre I, Lory S, et al. 2004. Biofilm formation in Pseudomonas aeruginosa: fimbrial cup gene clusters are controlled by the transcriptional regulator MvaT. J. Bacteriol. 186: 2880-2890.   DOI
6 Weber MM, French CL, Barnes MB, Siegele DA, McLean RJ. 2010. A previously uncharacterized gene, yjfO (bsmA), influences Escherichia coli biofilm formation and stress response. Microbiology 156: 139-147.   DOI   ScienceOn
7 Wimpenny JW, Colasanti R. 1997. A unifying hypothesis for the structure of microbial biofilms based on cellular automaton models. FEMS Microbiol. Ecol. 22: 1-16.   DOI   ScienceOn
8 Wood TK. 2009. Insights on Escherichia coli biofilm formation and inhibition from whole-transcriptome profiling. Environ. Microbiol. 11: 1-15.   DOI   ScienceOn
9 Wu C, Labrie J, Tremblay YDN, Haine D, Mourez M, Jacques M. 2013. Zinc as an agent for the prevention of biofilm formation by pathogenic bacteria. J. Appl. Microbiol. 115: 30-40.   DOI   ScienceOn
10 Yadav MK, Chae SW, Song JJ. 2012. Effect of 5-azacytidine on in vitro biofilm formation of Streptococcus pneumoniae. Microb. Pathog. 53: 219-226.   DOI   ScienceOn
11 Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the $2^-^{\Delta}^{\Delta}^{Ct}$ method. Methods 25: 402-408.   DOI   ScienceOn
12 Macaskie LE, Empson RM, Lin F, Tolley MR. 1995. Enzymatically-mediated uranium accumulation and uranium recovery using a Citrobacter sp. immobilised as a biofilm within a plug-flow reactor. J. Chem. Technol. Biotechnol. 63: 1-16.   DOI   ScienceOn
13 O'Toole GA, Kolter R. 1998. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol. Microbiol. 28: 449-461.   DOI   ScienceOn
14 Ong CL, Beatson S, Totsika M, Forestier C, McEwan A, Schembri M. 2010. Molecular analysis of type 3 fimbrial genes from Escherichia coli, Klebsiella and Citrobacter species. BMC Microbiol. 10: 183.   DOI   ScienceOn
15 Ong CLY, Ulett GC, Mabbett AN, Beatson SA, Webb RI, Monaghan W, et al. 2008. Identification of type 3 fimbriae in uropathogenic Escherichia coli reveals a role in biofilm formation. J. Bacteriol. 190: 1054-1063.   DOI   ScienceOn
16 Shemesh M, Tam A, Steinberg D. 2007. Expression of biofilm-associated genes of Streptococcus mutans in response to glucose and sucrose. J. Med. Microbiol. 56: 1528-1535.   DOI   ScienceOn
17 Patrauchan M, Sarkisova S, Sauer K, Franklin M. 2005. Calcium influences cellular and extracellular product formation during biofilm-associated growth of a marine Pseudoalteromonas sp. Microbiology 151: 2885-2897.   DOI   ScienceOn
18 Rinaudi L, Fujishige NA, Hirsch AM, Banchio E, Zorreguieta A, Giordano W. 2006. Effects of nutritional and environmental conditions on Sinorhizobium meliloti biofilm formation. Res. Microbiol. 157: 867-875.   DOI   ScienceOn
19 Ryu JH, Kim H, Frank J, Beuchat L. 2004. Attachment and biofilm formation on stainless steel by Escherichia coli O1 57: H7 as affected by curli production. Lett. Appl. Microbiol. 39: 359-362.   DOI   ScienceOn
20 Shukla SK, Rao TS. 2013. Effect of calcium on Staphylococcus aureus biofilm architecture: a confocal laser scanning microscopic study. Colloids Surf. B. 103: 448-454.   DOI   ScienceOn
21 Song B, Leff LG. 2006. Influence of magnesium ions on biofilm formation by Pseudomonas fluorescens. Microbiol. Res. 161: 355-361.   DOI   ScienceOn
22 Fujishige NA, Kapadia NN, De Hoff PL, Hirsch AM. 2006. Investigations of Rhizobium biofilm formation. FEMS Microbiol. Ecol. 56: 195-206.   DOI   ScienceOn
23 Hamanaka D, Onishi M, Genkawa T, Tanaka F, Uchino T. 2011. Effects of temperature and nutrient concentration on the structural characteristics and removal of vegetableassociated Pseudomonas biofilm. Food Control 24: 165-170.
24 Hodges GR, Degener CE, Barnes WG. 1978. Clinical significance of Citrobacter isolates. Am. J. Clin. Pathol. 70: 37-40.
25 Howard-Flanders P, Theriot L. 1966. Mutants of Escherichia coli K-12 defective in DNA repair and in genetic recombination. Genetics 53: 1137-1150.
26 Karatan E, Watnick P. 2009. Signals, regulatory networks, and materials that build and break bacterial biofilms. Microbiol. Mol. Biol. Rev. 73: 310-347.   DOI   ScienceOn
27 Huang CY, Hsieh SP, Kuo PA, Jane WN, Tu J, Wang YN, et al. 2009. Impact of disinfectant and nutrient concentration on growth and biofilm formation for a Pseudomonas strain and the mixed cultures from a fine papermachine system. Int. Biodeterior. Biodegrad. 63: 998-1007.   DOI   ScienceOn
28 Jackson DW, Simecka JW, Romeo T. 2002. Catabolite repression of Escherichia coli biofilm formation. J. Bacteriol. 184: 3406-3410.   DOI
29 Jeong BC, Hawes C, Bonthrone KM, Macaskie LE. 1997. Localization of enzymically enhanced heavy metal accumulation by Citrobacter sp. and metal accumulation in vitro by liposomes containing entrapped enzyme. Microbiology 143: 2497-2507.   DOI   ScienceOn
30 Labbate M, Queck SY, Koh KS, Rice SA, Givskov M, Kjelleberg S. 2004. Quorum sensing-controlled biofilm development in Serratia liquefaciens M G1 . J. Bacteriol. 186: 692-698.   DOI
31 Leme AP, Koo H, Bellato C, Bedi G, Cury J. 2006. The role of sucrose in cariogenic dental biofilm formation - new insight. J. Dent. Res. 85: 878-887.   DOI   ScienceOn
32 Lipsky BA, Hook EW, Smith AA, Plorde JJ. 1980. Citrobacter infections in humans: experience at the Seattle Veterans Administration Medical Center and a review of the literature. Rev. Infect. Dis. 2: 746-760.   DOI
33 Dong L, Tong Z, Linghu D, Lin Y, Tao R, Liu J, et al. 2012. Effects of sub-minimum inhibitory concentrations of antimicrobial agents on Streptococcus mutans biofilm formation. Int. J. Antimicrob. Agents 39: 390-395.   DOI   ScienceOn
34 Booth SC, George IF, Zannoni D, Cappelletti M, Duggan GE, Ceri H, et al. 2013. Effect of aluminium and copper on biofilm development of Pseudomonas pseudoalcaligenes KF707 and P. fluorescens as a function of different media compositions. Metallomics 5: 723-735.   DOI   ScienceOn
35 Costerton JW, Lewandowski Z, Caldwell DE, Korber DR, Lappin-Scott HM. 1995. Microbial biofilms. Annu. Rev. Microbiol. 49: 711-745.   DOI   ScienceOn
36 Domka J, Lee J, Wood TK. 2006. YliH (BssR) and YceP (BssS) regulate Escherichia coli K-12 biofilm formation by influencing cell signaling. Appl. Environ. Microbiol. 72: 2449- 2459.   DOI   ScienceOn
37 Finlay JA, Allan VJM, Conner A, Callow ME, Basnakova G, Macaskie L E. 1 999. P hosphate r elease a nd h eavy m etal accumulation by biofilm-immobilized and chemically-coupled cells of a Citrobacter sp. pre-grown in continuous culture. Biotechnol. Bioeng. 63: 87-97.   DOI
38 Cruz LF, Cobine PA, De La Fuente L. 2012. Calcium increases Xylella fastidiosa surface attachment, biofilm formation, and twitching motility. Appl. Environ. Microbiol. 78: 1321 - 1331.   DOI
39 Yang L, Barken KB, Skindersoe ME, Christensen AB, Givskov M, Tolker-Nielsen T. 2007. Effects of iron on DNA release and biofilm development by Pseudomonas aeruginosa. Microbiology 153: 1318-1328.   DOI   ScienceOn
40 Petrova OE, Sauer K. 2009. A novel signaling network essential for regulating Pseudomonas aeruginosa biofilm development. PLOS Pathog. 5: e1000668.   DOI   ScienceOn
41 Labrie J, Pelletier-Jacques G, Deslandes V, Ramjeet M, Auger E, Nash JH, et al. 2010. Effects of growth conditions on biofilm formation by Actinobacillus pleuropneumoniae. Vet. Res. 41: 3.   DOI   ScienceOn