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Published in: Gut Pathogens 1/2017

Open Access 01-12-2017 | Research

Global gene expression in Escherichia coli, isolated from the diseased ocular surface of the human eye with a potential to form biofilm

Authors: Konduri Ranjith, Kotakonda Arunasri, Gundlapally Sathyanarayana Reddy, HariKrishna Adicherla, Savitri Sharma, Sisinthy Shivaji

Published in: Gut Pathogens | Issue 1/2017

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Abstract

Background

Escherichia coli, the gastrointestinal commensal, is also known to cause ocular infections such as conjunctivitis, keratitis and endophthalmitis. These infections are normally resolved by topical application of an appropriate antibiotic. But, at times these E. coli are resistant to the antibiotic and this could be due to formation of a biofilm. In this study ocular E. coli from patients with conjunctivitis, keratitis or endophthalmitis were screened for their antibiotic susceptibility and biofilm formation potential. In addition DNA-microarray analysis was done to identify genes that are involved in biofilm formation and antibiotic resistance.

Results

Out of 12 ocular E. coli isolated from patients ten isolates were resistant to one or more of the nine antibiotics tested and majority of the isolates were positive for biofilm formation. In E. coli L-1216/2010, the best biofilm forming isolate, biofilm formation was confirmed by scanning electron microscopy. Confocal laser scanning microscopic studies indicated that the thickness of the biofilm increased up to 72 h of growth. Further, in the biofilm phase, E. coli L-1216/2010 was 100 times more resistant to the eight antibiotics tested compared to planktonic phase. DNA microarray analysis indicated that in biofilm forming E. coli L-1216/2010 genes encoding biofilm formation such as cell adhesion genes, LPS production genes, genes required for biofilm architecture and extracellular matrix remodeling and genes encoding for proteins that are integral to the cell membrane and those that influence antigen presentation are up regulated during biofilm formation. In addition genes that confer antimicrobial resistance such as genes encoding antimicrobial efflux (mdtM and cycA), virulence (insQ, yjgK), toxin production (sat, yjgK, chpS, chpB and ygjN), transport of amino-acids and other metabolites (cbrB, cbrC, hisI and mglB) are also up regulated. These genes could serve as potential targets for developing strategies for hacking biofilms and overcoming antibiotic resistance.

Conclusions

This is the first study on global gene expression in antibiotic resistant ocular E. coli with a potential to form biofilm. Using native ocular isolates for antibiotic susceptibility testing, for biofilm formation and global gene expression is relevant and more acceptable than using type strains or non clinical strains which do not necessarily mimic the native isolate.
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Literature
1.
go back to reference Conway T, Cohen PS. Commensal and pathogenic Escherichia coli metabolism in the gut. Microbiol Spectr. 2015;3(3):10.PubMedCentral Conway T, Cohen PS. Commensal and pathogenic Escherichia coli metabolism in the gut. Microbiol Spectr. 2015;3(3):10.PubMedCentral
2.
go back to reference Stenutz R, Weintraub A, Widmalm G. The structures of Escherichia coli O-polysaccharide antigens. FEMS Microbiol Rev. 2006;30(3):382–403.CrossRefPubMed Stenutz R, Weintraub A, Widmalm G. The structures of Escherichia coli O-polysaccharide antigens. FEMS Microbiol Rev. 2006;30(3):382–403.CrossRefPubMed
3.
go back to reference Croxen MA, Law RJ, Scholz R, Keeney KM, Wlodarska M, Finlay BB. Recent advances in understanding enteric pathogenic Escherichia coli. Clin Microbiol Rev. 2013;26(4):822–80.CrossRefPubMedPubMedCentral Croxen MA, Law RJ, Scholz R, Keeney KM, Wlodarska M, Finlay BB. Recent advances in understanding enteric pathogenic Escherichia coli. Clin Microbiol Rev. 2013;26(4):822–80.CrossRefPubMedPubMedCentral
4.
go back to reference Kwon T, Kim W, Cho SH. Comparative genomic analysis of Shiga toxin-producing and non-Shiga toxin-producing Escherichia coli O157 isolated from outbreaks in Korea. Gut Pathogens. 2017;9:7.CrossRefPubMedPubMedCentral Kwon T, Kim W, Cho SH. Comparative genomic analysis of Shiga toxin-producing and non-Shiga toxin-producing Escherichia coli O157 isolated from outbreaks in Korea. Gut Pathogens. 2017;9:7.CrossRefPubMedPubMedCentral
5.
7.
go back to reference Abelson MB, McLaughlin J. Of biomes, biofilm and the ocular surface. Rev Ophthalmol. 2012;19:52–4. Abelson MB, McLaughlin J. Of biomes, biofilm and the ocular surface. Rev Ophthalmol. 2012;19:52–4.
8.
go back to reference Bharathi MJ, Ramakrishnan R, Meenakshi R, Padmavathy S, Shivakumar C, Srinivasan M. Microbial keratitis in south india: influence of risk factors, climate, and geographical variation. Ophthalmic Epidemiol. 2007;14(2):61–9.CrossRefPubMed Bharathi MJ, Ramakrishnan R, Meenakshi R, Padmavathy S, Shivakumar C, Srinivasan M. Microbial keratitis in south india: influence of risk factors, climate, and geographical variation. Ophthalmic Epidemiol. 2007;14(2):61–9.CrossRefPubMed
9.
go back to reference Ramage G, Mowat E, Jones B, William C. Our current understanding of fungal biofilms. Crit Rev Microbiol. 2009;35(4):340–55.CrossRefPubMed Ramage G, Mowat E, Jones B, William C. Our current understanding of fungal biofilms. Crit Rev Microbiol. 2009;35(4):340–55.CrossRefPubMed
10.
go back to reference Sengupta J, Saha S, Khetan A, Sarkar SK, Mandal SM. Effects of lactoferricin B against keratitis-associated fungal biofilms. J Infect Chemother. 2012;18(5):698–703.CrossRefPubMed Sengupta J, Saha S, Khetan A, Sarkar SK, Mandal SM. Effects of lactoferricin B against keratitis-associated fungal biofilms. J Infect Chemother. 2012;18(5):698–703.CrossRefPubMed
11.
go back to reference Graham JE, Moore JE, Jiru X, Moore JE, Goodall EA, Dooley JS, Hayes VE, Dartt DA, Downes CS, Moore TC. Ocular pathogen or commensal: a PCR-based study of surface bacterial flora in normal and dry eyes. Investig Ophthalmol Vis Sci. 2007;48(12):5616–23.CrossRef Graham JE, Moore JE, Jiru X, Moore JE, Goodall EA, Dooley JS, Hayes VE, Dartt DA, Downes CS, Moore TC. Ocular pathogen or commensal: a PCR-based study of surface bacterial flora in normal and dry eyes. Investig Ophthalmol Vis Sci. 2007;48(12):5616–23.CrossRef
12.
go back to reference Dong Q, Brulc JM, Iovieno A, Bates B, Garoutte A, Miller D, Revanna KV, Gao X, Antonopoulos DA, Slepak VZ, Shestopalov VI. Diversity of bacteria at healthy human conjunctiva. Investig Ophthalmol Vis Sci. 2011;52(8):5408–13.CrossRef Dong Q, Brulc JM, Iovieno A, Bates B, Garoutte A, Miller D, Revanna KV, Gao X, Antonopoulos DA, Slepak VZ, Shestopalov VI. Diversity of bacteria at healthy human conjunctiva. Investig Ophthalmol Vis Sci. 2011;52(8):5408–13.CrossRef
13.
go back to reference Schabereiter-Gurtner C, Maca S, Rolleke S, Nigl K, Lukas J, Hirschl A, Lubitz W, Barisani-Asenbauer T. 16S rDNA-based identification of bacteria from conjunctival swabs by PCR and DGGE fingerprinting. Investig Ophthalmol Vis Sci. 2001;42(6):1164–71. Schabereiter-Gurtner C, Maca S, Rolleke S, Nigl K, Lukas J, Hirschl A, Lubitz W, Barisani-Asenbauer T. 16S rDNA-based identification of bacteria from conjunctival swabs by PCR and DGGE fingerprinting. Investig Ophthalmol Vis Sci. 2001;42(6):1164–71.
14.
go back to reference Lee SH, Oh DH, Jung JY, Kim JC, Jeon CO. Comparative ocular microbial communities in humans with and without blepharitis. Investig Ophthalmol Vis Sci. 2012;53(9):5585–93.CrossRef Lee SH, Oh DH, Jung JY, Kim JC, Jeon CO. Comparative ocular microbial communities in humans with and without blepharitis. Investig Ophthalmol Vis Sci. 2012;53(9):5585–93.CrossRef
15.
go back to reference Willcox MD. Characterization of the normal microbiota of the ocular surface. Exp Eye. 2013;117:99–105.CrossRef Willcox MD. Characterization of the normal microbiota of the ocular surface. Exp Eye. 2013;117:99–105.CrossRef
16.
go back to reference Sharma S, Kunimoto DY, Garg P, Rao GN. Trends in antibiotic resistance of corneal pathogens: part I. An analysis of commonly used ocular antibiotics. Indian J Ophthalmol. 1999;47(2):95–100. Sharma S, Kunimoto DY, Garg P, Rao GN. Trends in antibiotic resistance of corneal pathogens: part I. An analysis of commonly used ocular antibiotics. Indian J Ophthalmol. 1999;47(2):95–100.
17.
go back to reference Hoyle BD, Wong CK, Costerton JW. Disparate efficacy of tobramycin on Ca(2+)-, Mg(2+)-, and HEPES-treated Pseudomonas aeruginosa biofilms. Can J Microbiol. 1992;38(11):1214–8.CrossRefPubMed Hoyle BD, Wong CK, Costerton JW. Disparate efficacy of tobramycin on Ca(2+)-, Mg(2+)-, and HEPES-treated Pseudomonas aeruginosa biofilms. Can J Microbiol. 1992;38(11):1214–8.CrossRefPubMed
18.
go back to reference Elder MJ, Stapleton F, Evans E, Dart JK. Biofilm-related infections in ophthalmology. Eye. 1995;9(1):102–9.CrossRefPubMed Elder MJ, Stapleton F, Evans E, Dart JK. Biofilm-related infections in ophthalmology. Eye. 1995;9(1):102–9.CrossRefPubMed
19.
go back to reference Zegans ME, Becker HI, Budzik J, O’Toole G. The role of bacterial biofilms in ocular infections. DNA Cell Biol. 2002;21(5–6):415–20.CrossRefPubMed Zegans ME, Becker HI, Budzik J, O’Toole G. The role of bacterial biofilms in ocular infections. DNA Cell Biol. 2002;21(5–6):415–20.CrossRefPubMed
20.
go back to reference Heilmann C, Götz F. Cell–cell communication and biofilm formation in Gram-positive bacteria. In: Krämer R, Jung K, editors. Bacterial signaling. Wiley: Weinheim; 2010. p. 1–22. Heilmann C, Götz F. Cell–cell communication and biofilm formation in Gram-positive bacteria. In: Krämer R, Jung K, editors. Bacterial signaling. Wiley: Weinheim; 2010. p. 1–22.
21.
go back to reference Katiyar R, Vishwakarma A, Kaistha SD. Analysis of biofilm formation and antibiotic resistance of microbial isolates from intraocular lens following conventional extracapsular cataract surgery. Int J Res Pure Appl Microbiol. 2012;2(2):20–4. Katiyar R, Vishwakarma A, Kaistha SD. Analysis of biofilm formation and antibiotic resistance of microbial isolates from intraocular lens following conventional extracapsular cataract surgery. Int J Res Pure Appl Microbiol. 2012;2(2):20–4.
22.
go back to reference Sherwal BL, Verma AK. Epidemiology of ocular infection due to bacteria and fungus—a prospective study. JK Sci. 2008;10(3):127–31. Sherwal BL, Verma AK. Epidemiology of ocular infection due to bacteria and fungus—a prospective study. JK Sci. 2008;10(3):127–31.
23.
go back to reference Gopinathan U, Sharma S, Garg P, Rao GN. Review of epidemiological features, microbiological diagnosis and treatment outcome of microbial keratitis: experience of over a decade. Indian J Ophthalmol. 2009;57(4):273–9.CrossRefPubMedPubMedCentral Gopinathan U, Sharma S, Garg P, Rao GN. Review of epidemiological features, microbiological diagnosis and treatment outcome of microbial keratitis: experience of over a decade. Indian J Ophthalmol. 2009;57(4):273–9.CrossRefPubMedPubMedCentral
24.
go back to reference Callegan MC, Engelbert M, Parke DW, Jet BD, Gilmore MS. Bacterial endophthalmitis: epidemiology, therapeutics, and bacterium-host interactions. Clin Microbiol Rev. 2002;15(1):111–24.CrossRefPubMedPubMedCentral Callegan MC, Engelbert M, Parke DW, Jet BD, Gilmore MS. Bacterial endophthalmitis: epidemiology, therapeutics, and bacterium-host interactions. Clin Microbiol Rev. 2002;15(1):111–24.CrossRefPubMedPubMedCentral
25.
go back to reference Jindal A, Pathengay A, Mithal K, Jalali S, Mathai A, Pappuru RR, Narayanan R, Chhablani J, Motukupally SR, Sharma S, Das T, Flynn HW. Endophthalmitis after open globe injuries: changes in microbiological spectrum and isolate susceptibility patterns over 14 years. J Ophthalmic Inflamm Infect. 2014;4:5.CrossRefPubMedPubMedCentral Jindal A, Pathengay A, Mithal K, Jalali S, Mathai A, Pappuru RR, Narayanan R, Chhablani J, Motukupally SR, Sharma S, Das T, Flynn HW. Endophthalmitis after open globe injuries: changes in microbiological spectrum and isolate susceptibility patterns over 14 years. J Ophthalmic Inflamm Infect. 2014;4:5.CrossRefPubMedPubMedCentral
26.
go back to reference Murthy TA, Rangappa P, Rao S, Rao K. ESBL E. coli urosepsis resulting in endogenous panophthalmitis requiring evisceration of the eye in a diabetic patient. Case Rep Infect Dis. 2015;2015:4. Murthy TA, Rangappa P, Rao S, Rao K. ESBL E. coli urosepsis resulting in endogenous panophthalmitis requiring evisceration of the eye in a diabetic patient. Case Rep Infect Dis. 2015;2015:4.
27.
go back to reference Stratton M, Capitena C, Christensen L, Paciuc-Beja M. Escherichia coli eyelid abscess in a patient with alcoholic cirrhosis. Case Rep Ophthalmol Med. 2015;2015:2. Stratton M, Capitena C, Christensen L, Paciuc-Beja M. Escherichia coli eyelid abscess in a patient with alcoholic cirrhosis. Case Rep Ophthalmol Med. 2015;2015:2.
28.
go back to reference Fux CA, Costerton JW, Stewart PS, Stoodley P. Survival strategies of infectious biofilms. Trends Microbiol. 2005;13(1):34–40.CrossRefPubMed Fux CA, Costerton JW, Stewart PS, Stoodley P. Survival strategies of infectious biofilms. Trends Microbiol. 2005;13(1):34–40.CrossRefPubMed
30.
go back to reference Ramli NSK, Eng Guan C, Nathan S, Vadivelu J. The effect of environmental conditions on biofilm formation of Burkholderia pseudomallei clinical isolates. PLoS ONE. 2012;7(9):e44104.CrossRefPubMedPubMedCentral Ramli NSK, Eng Guan C, Nathan S, Vadivelu J. The effect of environmental conditions on biofilm formation of Burkholderia pseudomallei clinical isolates. PLoS ONE. 2012;7(9):e44104.CrossRefPubMedPubMedCentral
31.
go back to reference CLSI, Performance Standards for Antimicrobial Disk Susceptibility Tests. Approved standard, 7th ed. CLSI document M02-A11. Clinical and Laboratory Standards Institute, 950 West Valley Road, Suite 2500, Wayne, Pennsylvania 19087, USA. 2012. CLSI, Performance Standards for Antimicrobial Disk Susceptibility Tests. Approved standard, 7th ed. CLSI document M02-A11. Clinical and Laboratory Standards Institute, 950 West Valley Road, Suite 2500, Wayne, Pennsylvania 19087, USA. 2012.
32.
go back to reference EUCAST, European Committee for Antimicrobial Susceptibility Testing (EUCAST) of the European Society of Clinical Microbiology and Infectious Diseases (ESCMID). Determination of minimum inhibitory concentrations (MICs) of antibacterial agents by broth dilution. Clin Microbiol Infect. 2003;9:ix–xv.CrossRef EUCAST, European Committee for Antimicrobial Susceptibility Testing (EUCAST) of the European Society of Clinical Microbiology and Infectious Diseases (ESCMID). Determination of minimum inhibitory concentrations (MICs) of antibacterial agents by broth dilution. Clin Microbiol Infect. 2003;9:ix–xv.CrossRef
33.
go back to reference Arunasri K, Adil M, VenuCharan K, Suvro C, Himabindu Reddy S, Shivaji S. Effect of simulated microgravity on E. coli K12 MG1655 growth and gene expression. PLoS ONE. 2013;8(3):e57860.CrossRefPubMedPubMedCentral Arunasri K, Adil M, VenuCharan K, Suvro C, Himabindu Reddy S, Shivaji S. Effect of simulated microgravity on E. coli K12 MG1655 growth and gene expression. PLoS ONE. 2013;8(3):e57860.CrossRefPubMedPubMedCentral
34.
go back to reference Brittnacher MJ, Fong C, Hayden HS, Jacobs MA, Radey M, Rohmer L. PGAT: a multi strain analysis resource for microbial genomes. Bioinformatics. 2011;27(17):2429–30.CrossRefPubMedPubMedCentral Brittnacher MJ, Fong C, Hayden HS, Jacobs MA, Radey M, Rohmer L. PGAT: a multi strain analysis resource for microbial genomes. Bioinformatics. 2011;27(17):2429–30.CrossRefPubMedPubMedCentral
35.
go back to reference Montojo J, Zuberi K, Rodriguez H, Kazi F, Wright G. GeneMANIA cytoscape plugin: fast gene function predictions on the desktop. Bioinformatics. 2010;26(22):2927–8.CrossRefPubMedPubMedCentral Montojo J, Zuberi K, Rodriguez H, Kazi F, Wright G. GeneMANIA cytoscape plugin: fast gene function predictions on the desktop. Bioinformatics. 2010;26(22):2927–8.CrossRefPubMedPubMedCentral
36.
go back to reference Mishra SK, Basukala P, Basukala O, Parajuli K, Pokhrel BM, Rijal BP. Detection of biofilm production and antibiotic resistance pattern in clinical isolates from indwelling medical devices. Curr Microbiol. 2015;70(1):128–34.CrossRefPubMed Mishra SK, Basukala P, Basukala O, Parajuli K, Pokhrel BM, Rijal BP. Detection of biofilm production and antibiotic resistance pattern in clinical isolates from indwelling medical devices. Curr Microbiol. 2015;70(1):128–34.CrossRefPubMed
37.
go back to reference Jassim SH, Sivaraman KR, Jimenez JC, Jaboori AH, Federle MJ, de la Cruz J, Cortina MS. Bacteria colonizing the ocular surface in eyes with boston type 1 keratoprosthesis: analysis of biofilm-forming capability and vancomycin tolerance. Investig Ophthalmol Vis Sci. 2015;56(8):4689–96.CrossRef Jassim SH, Sivaraman KR, Jimenez JC, Jaboori AH, Federle MJ, de la Cruz J, Cortina MS. Bacteria colonizing the ocular surface in eyes with boston type 1 keratoprosthesis: analysis of biofilm-forming capability and vancomycin tolerance. Investig Ophthalmol Vis Sci. 2015;56(8):4689–96.CrossRef
38.
go back to reference Qi L, Li H, Zhang C, Liang B, Li J, Wang L, Du X, Liu X, Qiu S, Song H. Relationship between antibiotic resistance, biofilm formation, and biofilm-specific resistance in Acinetobacter baumannii. Front Microbiol. 2016;7:483.PubMedPubMedCentral Qi L, Li H, Zhang C, Liang B, Li J, Wang L, Du X, Liu X, Qiu S, Song H. Relationship between antibiotic resistance, biofilm formation, and biofilm-specific resistance in Acinetobacter baumannii. Front Microbiol. 2016;7:483.PubMedPubMedCentral
39.
go back to reference Schembri MA, Kjaergaard K, Klemm P. Global gene expression in Escherichia coli biofilms. Mol Microbiol. 2003;48(1):253–67.CrossRefPubMed Schembri MA, Kjaergaard K, Klemm P. Global gene expression in Escherichia coli biofilms. Mol Microbiol. 2003;48(1):253–67.CrossRefPubMed
40.
go back to reference Beloin C, Valle J, Latour-Lambert P, Faure P, Kzreminski M, Balestrino D, Haagensen JA, Molin S, Prensier G, Arbeille B, Ghigo JM. Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol Microbiol. 2004;51(3):659–74.CrossRefPubMed Beloin C, Valle J, Latour-Lambert P, Faure P, Kzreminski M, Balestrino D, Haagensen JA, Molin S, Prensier G, Arbeille B, Ghigo JM. Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression. Mol Microbiol. 2004;51(3):659–74.CrossRefPubMed
41.
go back to reference Ren D, Bedzyk LA, Thomas SM, Ye RW, Wood TK. Gene expression in Escherichia coli biofilms. Appl Microbiol Biotechnol. 2004;64(4):515–24.CrossRefPubMed Ren D, Bedzyk LA, Thomas SM, Ye RW, Wood TK. Gene expression in Escherichia coli biofilms. Appl Microbiol Biotechnol. 2004;64(4):515–24.CrossRefPubMed
42.
go back to reference Domka J, Lee J, Wood TK. YliH (BssR) and YceP (BssS) regulate Escherichia coli K-12 biofilm formation by influencing cell signaling. Appl Environ Microbiol. 2006;72(4):2449–59.CrossRefPubMedPubMedCentral Domka J, Lee J, Wood TK. YliH (BssR) and YceP (BssS) regulate Escherichia coli K-12 biofilm formation by influencing cell signaling. Appl Environ Microbiol. 2006;72(4):2449–59.CrossRefPubMedPubMedCentral
43.
go back to reference Hancock V, Klemm P. Global gene expression profiling of asymptomatic bacteriuria Escherichia coli during biofilm growth in human urine. Infect Immun. 2007;75(2):966–76.CrossRefPubMed Hancock V, Klemm P. Global gene expression profiling of asymptomatic bacteriuria Escherichia coli during biofilm growth in human urine. Infect Immun. 2007;75(2):966–76.CrossRefPubMed
44.
go back to reference Wood TK, Gonzalez Barrios AF, Herzberg M, Lee J. Motility influences biofilm architecture in Escherichia coli. Appl Microbiol Biotechnol. 2006;72(2):361–7.CrossRefPubMed Wood TK, Gonzalez Barrios AF, Herzberg M, Lee J. Motility influences biofilm architecture in Escherichia coli. Appl Microbiol Biotechnol. 2006;72(2):361–7.CrossRefPubMed
46.
go back to reference Korea CG, Badouraly R, Prevost MC, Ghigo JM, Beloin C. Escherichia coli K-12 possesses multiple cryptic but functional chaperone-usher fimbriae with distinct surface specificities. Environ Microbiol. 2010;12(7):1957–77.CrossRefPubMed Korea CG, Badouraly R, Prevost MC, Ghigo JM, Beloin C. Escherichia coli K-12 possesses multiple cryptic but functional chaperone-usher fimbriae with distinct surface specificities. Environ Microbiol. 2010;12(7):1957–77.CrossRefPubMed
47.
go back to reference Reisner A, Haagensen JA, Schembri MA, Zechner EL, Molin S. Development and maturation of Escherichia coli K-12 biofilms. Mol Microbiol. 2003;48(4):933–46.CrossRefPubMed Reisner A, Haagensen JA, Schembri MA, Zechner EL, Molin S. Development and maturation of Escherichia coli K-12 biofilms. Mol Microbiol. 2003;48(4):933–46.CrossRefPubMed
48.
go back to reference Ren CP, Beatson SA, Parkhill J, Pallen MJ. The flag-2 locus, an ancestral gene cluster, is potentially associated with a novel flagellar system from Escherichia coli. J Bacteriol. 2005;187(4):1430–40.CrossRefPubMedPubMedCentral Ren CP, Beatson SA, Parkhill J, Pallen MJ. The flag-2 locus, an ancestral gene cluster, is potentially associated with a novel flagellar system from Escherichia coli. J Bacteriol. 2005;187(4):1430–40.CrossRefPubMedPubMedCentral
49.
go back to reference Prigent-Combaret C, Prensier G, Le Thi TT, Vidal O, Lejeune P, Dorel C. Developmental pathway for biofilm formation in curli-producing Escherichia coli strains: role of flagella, curli and colanic acid. Environ Microbiol. 2000;2(4):450–64.CrossRefPubMed Prigent-Combaret C, Prensier G, Le Thi TT, Vidal O, Lejeune P, Dorel C. Developmental pathway for biofilm formation in curli-producing Escherichia coli strains: role of flagella, curli and colanic acid. Environ Microbiol. 2000;2(4):450–64.CrossRefPubMed
50.
go back to reference Van der Woude MW. Re-examining the role and random nature of phase variation. FEMS Microbiol Lett. 2006;254(2):190–7.CrossRefPubMed Van der Woude MW. Re-examining the role and random nature of phase variation. FEMS Microbiol Lett. 2006;254(2):190–7.CrossRefPubMed
51.
go back to reference Simm R, Morr M, Kader A, Nimtz M, Romling U. GGDEF, EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol. 2004;53(4):1123–34.CrossRefPubMed Simm R, Morr M, Kader A, Nimtz M, Romling U. GGDEF, EAL domains inversely regulate cyclic di-GMP levels and transition from sessility to motility. Mol Microbiol. 2004;53(4):1123–34.CrossRefPubMed
52.
go back to reference Wolfe AJ, Chang DE, Walker JD, Seitz-Partridge JE, Vidaurri MD, Lange CF, Prüss BM, Henk MC, Larkin JC, Conway T. Evidence that acetyl phosphate functions as a global signal during biofilm development. Mol Microbiol. 2003;48(4):977–88.CrossRefPubMed Wolfe AJ, Chang DE, Walker JD, Seitz-Partridge JE, Vidaurri MD, Lange CF, Prüss BM, Henk MC, Larkin JC, Conway T. Evidence that acetyl phosphate functions as a global signal during biofilm development. Mol Microbiol. 2003;48(4):977–88.CrossRefPubMed
53.
go back to reference Whitfield C. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem. 2006;75:39–68.CrossRefPubMed Whitfield C. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem. 2006;75:39–68.CrossRefPubMed
54.
go back to reference Hanna A, Berg M, Stout V, Razatos A. Role of capsular colanic acid in adhesion of uropathogenic Escherichia coli. Appl Environ Microbiol. 2003;69(8):4474–81.CrossRefPubMedPubMedCentral Hanna A, Berg M, Stout V, Razatos A. Role of capsular colanic acid in adhesion of uropathogenic Escherichia coli. Appl Environ Microbiol. 2003;69(8):4474–81.CrossRefPubMedPubMedCentral
56.
go back to reference Paul N, Danese LA, Kolter PA. Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J bacteriol. 2000;182(12):3593–6.CrossRef Paul N, Danese LA, Kolter PA. Exopolysaccharide production is required for development of Escherichia coli K-12 biofilm architecture. J bacteriol. 2000;182(12):3593–6.CrossRef
57.
go back to reference Costa SB, Campos AC, Pereira AC, de Mattos-Guaraldi AL, Junior RH, Rosa AC, Asad LM. Adherence to abiotic surface induces SOS response in Escherichia coli K-12 strains under aerobic and anaerobic conditions. Microbiology. 2014;160(9):1964–73.CrossRefPubMed Costa SB, Campos AC, Pereira AC, de Mattos-Guaraldi AL, Junior RH, Rosa AC, Asad LM. Adherence to abiotic surface induces SOS response in Escherichia coli K-12 strains under aerobic and anaerobic conditions. Microbiology. 2014;160(9):1964–73.CrossRefPubMed
59.
go back to reference Chalabaev S, Chauhan A, Novikov A, Iyer P, Szczesny M, Beloin C, Caroff M, Ghigo J-M. Biofilms formed by Gram-negative bacteria undergo increased lipid a palmitoylation, enhancing in vivo survival. mBio. 2014;5(4):e01116–14.CrossRefPubMedPubMedCentral Chalabaev S, Chauhan A, Novikov A, Iyer P, Szczesny M, Beloin C, Caroff M, Ghigo J-M. Biofilms formed by Gram-negative bacteria undergo increased lipid a palmitoylation, enhancing in vivo survival. mBio. 2014;5(4):e01116–14.CrossRefPubMedPubMedCentral
60.
61.
go back to reference Bolstad HM, Botelho DJ, Wood MJ. Proteomic analysis of protein–protein interactions within the CSD Fe–S cluster biogenesis system. J Proteome Res. 2010;9(10):5358–69.CrossRefPubMedPubMedCentral Bolstad HM, Botelho DJ, Wood MJ. Proteomic analysis of protein–protein interactions within the CSD Fe–S cluster biogenesis system. J Proteome Res. 2010;9(10):5358–69.CrossRefPubMedPubMedCentral
62.
go back to reference Coler RN, Bertholet S, Moutaftsi M, Guderian JA, Windish HP, Baldwin SL, Laughlin EM, Duthie MS, Fox CB, Carter D, Friede M, Vedvick TS, Reed SG. Development and characterization of synthetic glucopyranosyl lipid adjuvant system as a vaccine adjuvant. PLoS ONE. 2011;6(1):e0016333.CrossRef Coler RN, Bertholet S, Moutaftsi M, Guderian JA, Windish HP, Baldwin SL, Laughlin EM, Duthie MS, Fox CB, Carter D, Friede M, Vedvick TS, Reed SG. Development and characterization of synthetic glucopyranosyl lipid adjuvant system as a vaccine adjuvant. PLoS ONE. 2011;6(1):e0016333.CrossRef
64.
go back to reference Dobrindt U, Agerer F, Michaelis K, Janka A, Buchrieser C, Samuelson M, Svanborg C, Gottschalk G, Karch H, Hacker J. Analysis of genome plasticity in pathogenic and commensal Escherichia coli isolates by use of DNA arrays. J Bacteriol. 2003;185(6):1831–40.CrossRefPubMedPubMedCentral Dobrindt U, Agerer F, Michaelis K, Janka A, Buchrieser C, Samuelson M, Svanborg C, Gottschalk G, Karch H, Hacker J. Analysis of genome plasticity in pathogenic and commensal Escherichia coli isolates by use of DNA arrays. J Bacteriol. 2003;185(6):1831–40.CrossRefPubMedPubMedCentral
65.
go back to reference Herold S, Siebert J, Huber A, Schmidt H. Global expression of prophage genes in Escherichia coli O157:H7 strain EDL933 in response to norfloxacin. Antimicrob Agents Chemother. 2005;49(3):931–44.CrossRefPubMedPubMedCentral Herold S, Siebert J, Huber A, Schmidt H. Global expression of prophage genes in Escherichia coli O157:H7 strain EDL933 in response to norfloxacin. Antimicrob Agents Chemother. 2005;49(3):931–44.CrossRefPubMedPubMedCentral
66.
go back to reference Singh AK, Pindi PK, Dube S, Sundareswaran VR, Shivaji S. Importance of trmE for growth of the psychrophile Pseudomonas syringae at low temperatures. Appl Environ Microbiol. 2009;75(13):4419–26.CrossRefPubMedPubMedCentral Singh AK, Pindi PK, Dube S, Sundareswaran VR, Shivaji S. Importance of trmE for growth of the psychrophile Pseudomonas syringae at low temperatures. Appl Environ Microbiol. 2009;75(13):4419–26.CrossRefPubMedPubMedCentral
67.
go back to reference Sundareswaran VR, Singh AK, Dube S, Shivaji S. Aspartate aminotransferase is involved in cold adaptation in psychrophilic Pseudomonas syringae. Arch Microbiol. 2010;192(8):663–72.CrossRefPubMed Sundareswaran VR, Singh AK, Dube S, Shivaji S. Aspartate aminotransferase is involved in cold adaptation in psychrophilic Pseudomonas syringae. Arch Microbiol. 2010;192(8):663–72.CrossRefPubMed
Metadata
Title
Global gene expression in Escherichia coli, isolated from the diseased ocular surface of the human eye with a potential to form biofilm
Authors
Konduri Ranjith
Kotakonda Arunasri
Gundlapally Sathyanarayana Reddy
HariKrishna Adicherla
Savitri Sharma
Sisinthy Shivaji
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2017
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-017-0164-2

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