Effects of genetic and environmental variables on biofilm development dynamics in Achromobacter mucicolens
,
Abstract
Background and Objectives: The study aimed to investigate whether Achromobacter mucicolens IA strain biofilm formation, which contributes to antibiotic resistance, could be enhanced by readily available nutrient sources like carbohydrates and environmental factors such as pH and NaCl. Additionally, the study aimed to identify any inherent genes that support biofilm formation in this strain, which is an opportunistic pathogen that affects immunocompromised patients and is resistant to many antibiotics.
Materials and Methods: Biofilm growth in different carbohydrate, pH, and NaCl concentrated media was measured using crystal violet microtiter assay. All the treatments were subjected to biostatistics analysis for normality, Test of Homogeneity, one way ANOVA analysis. Whole-genome sequencing of our IA strain was conducted to identify various gene sequences.
Results: Biofilm formation was measured at different carbohydrate concentrations, and the optimum biofilm formation was observed at 3M glucose and 0.5M NaCl, while the lowest results were seen at 2M maltose concentration. Whole-genome sequencing identified potential genes involved in biofilm formation, pathogenicity, protein metabolism, flagellar motility, cell wall component synthesis, and a multidrug efflux pump.
Conclusion: These findings suggest that biofilm formation is influenced by extrinsic and intrinsic factors, which could aid in the development of effective treatments for resistant infections.
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8. Qin X, Razia Y, Johnson JR, Stapp JR, Boster DR, Tsosie T, et al. Ciprofloxacin-resistant gram-negative bacilli in the fecal microflora of children. Antimicrob Agents Chemother 2006; 50: 3325-3329.
9. Toyofuku M, Inaba T, Kiyokawa T, Obana N, Yawata Y, NomuraN. Environmental factors that shape biofilm formation. Biosci Biotechnol Biochem 2016; 80: 7-12.
10. Filipic B, Malesevic M, Vasiljevic Z, Lukic J, Novovic K, Kojic M, et al. Uncovering differences in virulence markers associated with Achromobacter species of CF and Non-CF origin. Front Cell Infect Microbiol 2017; 7: 224.
11. Boles BR, Horswill AR. Swimming cells promote a dynamic environment within biofilms. Proc Natl Acad Sci U S A 2012; 109: 12848-12849.
12. Shrout JD, Tolker-Nielsen T, Givskov M, Parsek MR. The contribution of cell-cell signaling and motility to bacterial biofilm formation. MRS Bull 2011; 36: 367-373.
13. Hoffman LR, D'argenio DA, Maccoss MJ, Zhang Z, Jones RA, Miller SI. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 2005; 436: 1171-1175.
14. Molin S, Tolker-Nielsen T. Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. Curr Opin Biotechnol 2003; 14: 255-261.
15. O'Toole GA. Microtiter dish biofilm formation assay. J Vis Exp 2011; (47): 2437.
16. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, et al. The RAST server: rapid annotations using S.ubsystems technology. BMC Genomics 2008; 9: 75.
17. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res 2014; 42: D206-14.
18. Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S, Olsen GJ, et al. RASTtk: A modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 2015; 5: 8365.
19. Al-Asadi SA, Al-Kahachi RES, Alwattar WMA, Bootwala J, Sabbah MA. Genomic insights into Achromobacter mucicolens IA antibiotic resistance. Microbiol Spectr 2022; 10(2): e0191621.
20. URL Link: https://www.graphpad.com/updates/prism-900-release-notes; 20-07-2022.
21. Li G, Zhang T, Yang L, Cao Y, Guo X, Qin J, et al. Complete genome sequence of Achromobacter insolitus type strain LMG 6003T, a pathogen isolated from leg wound. Pathog Dis 2017; 75: 10.1093/femspd/ftx037.
22. Nielsen SM, Penstoft LN, Nørskov-Lauritsen N. Motility, biofilm formation and antimicrobial efflux of sessile and planktonic cells of Achromobacter xylosoxidans. Pathogens 2019; 8: 14.
23. Nielsen SM, Meyer RL, Nørskov-Lauritsen N. Differences in Gene expression profiles between early and late isolates in Monospecies Achromobacter biofilm. Pathogens 2017; 6: 20.
24. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25: 1043-1055.
25. Jakobsen TH, Hansen MA, Jensen PØ, Hansen L, Riber L, Cockburn A, et al. Complete genome sequence of the cystic fibrosis pathogen Achromobacter xylosoxidans NH44784-1996 complies with important pathogenic phenotypes. PLoS One 2013; 8(7): e68484.
26. Felgate H, Giannopoulos G, Sullivan MJ, Gates AJ, Clarke TA, Baggs E, et al. The impact of copper, nitrate and carbon status on the emission of nitrous oxide by two species of bacteria with biochemically distinct denitrification pathways. Environ Microbiol 2012; 14: 1788-1800.
27. Hassanshahian M, Ahmadinejad M, Tebyanian H, Kariminik A. Isolation and characterization of alkane degrading bacteria from petroleum reservoir waste water in Iran (Kerman and Tehran provenances). Mar Pollut Bull 2013; 73: 300-305.
28. Majumder A, Bhattacharyya K, Bhattacharyya S, Kole SC. Arsenic-tolerant, arsenite-oxidising bacterial strains in the contaminated soils of West Bengal, India. Sci Total Environ 2013; 463-464: 1006-1014.
29. Flemming H-C, Wingender J. The biofilm matrix. Nat Rev Microbiol 2010; 8: 623-633.
30. Whitfield C. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 2006; 75: 39-68.
31. Alotaibi GF, Bukhari MA. Factors influencing bacterial biofilm formation and development. Am J Biomed Sci Res 2021; 12: 617-626.
32. Yang Y, Sreenivasan PK, Subramanyam R, Cummins D. Multiparameter assessments to determine the effects of sugars and antimicrobials on a polymicrobial oral biofilm. Appl Environ Microbiol 2006; 72: 6734-6742.
33. Jackson DW, Simecka JW, Romeo T. Catabolite repression of Escherichia coli biofilm formation. J Bacteriol 2002; 184: 3406-3410.
34. Roy PK, Ha AJ, Mizan MFR, Hossain MI, Ashrafudoulla M, Toushik SH, et al. Effects of environmental conditions (temperature, pH, and glucose) on biofilm formation of Salmonella enterica serotype Kentucky and virulence gene expression. Poult Sci 2021; 100: 101209.
35. Xu H, Zou Y, Lee H-Y, Ahn J. Effect of NaCl on the biofilm formation by foodborne pathogens. J Food Sci 2010; 75: M580-5.
36. Chai Y, Beauregard PB, Vlamakis H, Losick R, Kolter R. Galactose metabolism plays a crucial role in biofilm formation by Bacillus sub-tilis. mBio 2012; 3(4): e00184-12.
37. Marsh PD. Dental plaque as a biofilm: the significance of pH in health and caries. Compend Contin Educ Dent 2009; 30: 76-78, 80, 83-87.
38. Hatt JK, Rather PN. Role of bacterial biofilms in urinary tract infections. Curr Top Microbiol Immunol 2008; 322: 163-192.
39. Jana TK, Srivastava AK, Csery K, Arora DK. Influence of growth and environmental conditions on cell surface hydrophobicity of pseudomonas fluorescens in non-specific adhesion. Can J Microbiol 2000; 46: 28-37.
40. LiPuma JJ, Rathinavelu S, Foster BK, Keoleian JC, Makidon PE, Kalikin LM, et al. In vitro activities of a novel nano-emulsion against Burkholderia and other multidrug-resistant cystic fibrosis-associated bacterial species. Antimicrob Agents Chemother 2009; 53: 249-255.
41. Sadikot RT, Blackwell TS, Christman JW, Prince AS. Pathogen-host interactions in Pseudomonas aeruginosa pneumonia. Am J Respir Crit Care Med 2005; 171: 1209-1223.
42. Sommer LM, Marvig RL, Lujan A, Koza A, Pressler T, Molin S, et al. Is genotyping of single isolates sufficient for population structure analysis of Pseudomonas aeruginosa in cystic fibrosis airways? BMC Genomics 2016; 17: 589.
43. Philippot L. Denitrification in pathogenic bacteria: for better or worst? Trends Microbiol 2005; 13: 191-192.
44. Tiwari M, Panwar S, Tiwari V. Assessment of potassium ion channel during electric signalling in biofilm formation of Acinetobacter baumannii for finding antibiofilm molecule. Heliyon 2023; 9(1): e12837.
45. Lundberg ME, Becker EC, Choe S. MstX and a putative potassium channel facilitate biofilm formation in Bacillus subtilis. PLoS One 2013; 8(5): e60993.
46. Prindle A, Liu J, Asally M, Ly S, Garcia-Ojalvo J, Suel GM. Ion channels enable electrical communication in bacterial communities. Nature 2015; 527: 59-63.
47. Liu J, Prindle A, Humphries J, Gabalda-Sagarra M, Asally M, Lee DY, et al. Metabolic co-dependence gives rise to collective oscillations within biofilms. Nature 2015; 523: 550–554.
48. Van Acker H, Coenye T. The role of efflux and physiological adaptation in biofilm tolerance and resistance. J Biol Chem 2016; 291: 12565-12572.
49. Baugh S, Ekanayaka AS, Piddock LJ, Webber MA. Loss of or inhibition of all multidrug resistance efflux pumps of Salmonella enterica serovar Typhimurium results in impaired ability to form a biofilm. J Antimicrob Chemother 2012; 67: 2409-2417.
50. Lamers RP, Cavallari JF, Burrows LL. The efflux inhibitor phenylalanine-arginine beta-naphthylamide (PAbetaN) permeabilizes the outer membrane of gram-negative bacteria. PLoS One 2013; 8(3): e60666.
51. Kvist M, Hancock V, Klemm P. Inactivation of efflux pumps abolishes bacterial biofilm formation. Appl Environ Microbiol 2008; 74: 7376-7382.
52. Phelps HA, Neely MN. SalY of the Streptococcus pyogenes antibiotic locus is required for full virulence and intracellular survival in macrophages. Infect Immun 2007; 75: 4541-4551.
53. Bogomolnaya LM, Andrews KD, Talamantes M, Maple A, Ragoza Y, Vazquez-Torres A, et al. The ABC-type efflux pump MacAB protects Salmonella enterica serovar typhimurium from oxidative stress. mBio 2013; 4(6): e00630-13.
54. Morgan R, Kohn S, Hwang S-H, Hassett DJ, Sauer K. BdlA, a chemotaxis regulator essential for biofilm dispersion in Pseudomonas aeruginosa. J Bacteriol 2006; 188: 7335-7343.
55. García-Fontana C, Reyes-Darias JA, Muñoz-Martínez F, Alfonso C, Morel B, Ramos JL, et al. High Specificity in CheR Methyltransferase Function: CheR2 of Pseudomonas putida is essential for chemotaxis, whereas CheR1 is involved in biofilm formation. J Biol Chem 2013; 288: 18987-18999.
2. Amoureux L, Bador J, Fardeheb S, Mabille C, Couchot C, Massip C, et al. Detection of Achromobacter xylosoxidans in hospital, domestic, and outdoor environmental samples and comparison with human clinical isolates. Appl Environ Microbiol 2013; 79: 7142-7149.
3. Swenson CE, Sadikot RT. Achromobacter respiratory infections. Ann Am Thorac Soc 2015; 12: 252-258.
4. Aisenberg G, Rolston KV, Safdar A. Bacteremia caused by Achromobacter and species in 46 patients with cancer (1989-2003). Cancer 2004; 101: 2134-2140.
5. Amoureux L, Bador J, Verrier T, Mjahed H, DE Curraize C, Neuwirth C. Achromobacter xylosoxidans is the predominant Achromobacter species isolated from diverse non-respiratory samples. Epidemiol Infect 2016; 144: 3527-3530.
6. Li X, Hu Y, Gong J, Zhang L, Wang G. Comparative genome characterization of Achromobacter members reveals potential genetic determinants facilitating the adaptation to a pathogenic lifestyle. Appl Microbiol Biotechnol 2013; 97: 6413-6425.
7. Wiatr M, Morawska A, Składzień J, Kedzierska J. Alcaligenes xylosoxidans—a pathogen of chronic ear infection. Otolaryngol Pol 2005; 59: 277-280.
8. Qin X, Razia Y, Johnson JR, Stapp JR, Boster DR, Tsosie T, et al. Ciprofloxacin-resistant gram-negative bacilli in the fecal microflora of children. Antimicrob Agents Chemother 2006; 50: 3325-3329.
9. Toyofuku M, Inaba T, Kiyokawa T, Obana N, Yawata Y, NomuraN. Environmental factors that shape biofilm formation. Biosci Biotechnol Biochem 2016; 80: 7-12.
10. Filipic B, Malesevic M, Vasiljevic Z, Lukic J, Novovic K, Kojic M, et al. Uncovering differences in virulence markers associated with Achromobacter species of CF and Non-CF origin. Front Cell Infect Microbiol 2017; 7: 224.
11. Boles BR, Horswill AR. Swimming cells promote a dynamic environment within biofilms. Proc Natl Acad Sci U S A 2012; 109: 12848-12849.
12. Shrout JD, Tolker-Nielsen T, Givskov M, Parsek MR. The contribution of cell-cell signaling and motility to bacterial biofilm formation. MRS Bull 2011; 36: 367-373.
13. Hoffman LR, D'argenio DA, Maccoss MJ, Zhang Z, Jones RA, Miller SI. Aminoglycoside antibiotics induce bacterial biofilm formation. Nature 2005; 436: 1171-1175.
14. Molin S, Tolker-Nielsen T. Gene transfer occurs with enhanced efficiency in biofilms and induces enhanced stabilisation of the biofilm structure. Curr Opin Biotechnol 2003; 14: 255-261.
15. O'Toole GA. Microtiter dish biofilm formation assay. J Vis Exp 2011; (47): 2437.
16. Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, et al. The RAST server: rapid annotations using S.ubsystems technology. BMC Genomics 2008; 9: 75.
17. Overbeek R, Olson R, Pusch GD, Olsen GJ, Davis JJ, Disz T, et al. The SEED and the Rapid Annotation of microbial genomes using Subsystems Technology (RAST). Nucleic Acids Res 2014; 42: D206-14.
18. Brettin T, Davis JJ, Disz T, Edwards RA, Gerdes S, Olsen GJ, et al. RASTtk: A modular and extensible implementation of the RAST algorithm for building custom annotation pipelines and annotating batches of genomes. Sci Rep 2015; 5: 8365.
19. Al-Asadi SA, Al-Kahachi RES, Alwattar WMA, Bootwala J, Sabbah MA. Genomic insights into Achromobacter mucicolens IA antibiotic resistance. Microbiol Spectr 2022; 10(2): e0191621.
20. URL Link: https://www.graphpad.com/updates/prism-900-release-notes; 20-07-2022.
21. Li G, Zhang T, Yang L, Cao Y, Guo X, Qin J, et al. Complete genome sequence of Achromobacter insolitus type strain LMG 6003T, a pathogen isolated from leg wound. Pathog Dis 2017; 75: 10.1093/femspd/ftx037.
22. Nielsen SM, Penstoft LN, Nørskov-Lauritsen N. Motility, biofilm formation and antimicrobial efflux of sessile and planktonic cells of Achromobacter xylosoxidans. Pathogens 2019; 8: 14.
23. Nielsen SM, Meyer RL, Nørskov-Lauritsen N. Differences in Gene expression profiles between early and late isolates in Monospecies Achromobacter biofilm. Pathogens 2017; 6: 20.
24. Parks DH, Imelfort M, Skennerton CT, Hugenholtz P, Tyson GW. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res 2015; 25: 1043-1055.
25. Jakobsen TH, Hansen MA, Jensen PØ, Hansen L, Riber L, Cockburn A, et al. Complete genome sequence of the cystic fibrosis pathogen Achromobacter xylosoxidans NH44784-1996 complies with important pathogenic phenotypes. PLoS One 2013; 8(7): e68484.
26. Felgate H, Giannopoulos G, Sullivan MJ, Gates AJ, Clarke TA, Baggs E, et al. The impact of copper, nitrate and carbon status on the emission of nitrous oxide by two species of bacteria with biochemically distinct denitrification pathways. Environ Microbiol 2012; 14: 1788-1800.
27. Hassanshahian M, Ahmadinejad M, Tebyanian H, Kariminik A. Isolation and characterization of alkane degrading bacteria from petroleum reservoir waste water in Iran (Kerman and Tehran provenances). Mar Pollut Bull 2013; 73: 300-305.
28. Majumder A, Bhattacharyya K, Bhattacharyya S, Kole SC. Arsenic-tolerant, arsenite-oxidising bacterial strains in the contaminated soils of West Bengal, India. Sci Total Environ 2013; 463-464: 1006-1014.
29. Flemming H-C, Wingender J. The biofilm matrix. Nat Rev Microbiol 2010; 8: 623-633.
30. Whitfield C. Biosynthesis and assembly of capsular polysaccharides in Escherichia coli. Annu Rev Biochem 2006; 75: 39-68.
31. Alotaibi GF, Bukhari MA. Factors influencing bacterial biofilm formation and development. Am J Biomed Sci Res 2021; 12: 617-626.
32. Yang Y, Sreenivasan PK, Subramanyam R, Cummins D. Multiparameter assessments to determine the effects of sugars and antimicrobials on a polymicrobial oral biofilm. Appl Environ Microbiol 2006; 72: 6734-6742.
33. Jackson DW, Simecka JW, Romeo T. Catabolite repression of Escherichia coli biofilm formation. J Bacteriol 2002; 184: 3406-3410.
34. Roy PK, Ha AJ, Mizan MFR, Hossain MI, Ashrafudoulla M, Toushik SH, et al. Effects of environmental conditions (temperature, pH, and glucose) on biofilm formation of Salmonella enterica serotype Kentucky and virulence gene expression. Poult Sci 2021; 100: 101209.
35. Xu H, Zou Y, Lee H-Y, Ahn J. Effect of NaCl on the biofilm formation by foodborne pathogens. J Food Sci 2010; 75: M580-5.
36. Chai Y, Beauregard PB, Vlamakis H, Losick R, Kolter R. Galactose metabolism plays a crucial role in biofilm formation by Bacillus sub-tilis. mBio 2012; 3(4): e00184-12.
37. Marsh PD. Dental plaque as a biofilm: the significance of pH in health and caries. Compend Contin Educ Dent 2009; 30: 76-78, 80, 83-87.
38. Hatt JK, Rather PN. Role of bacterial biofilms in urinary tract infections. Curr Top Microbiol Immunol 2008; 322: 163-192.
39. Jana TK, Srivastava AK, Csery K, Arora DK. Influence of growth and environmental conditions on cell surface hydrophobicity of pseudomonas fluorescens in non-specific adhesion. Can J Microbiol 2000; 46: 28-37.
40. LiPuma JJ, Rathinavelu S, Foster BK, Keoleian JC, Makidon PE, Kalikin LM, et al. In vitro activities of a novel nano-emulsion against Burkholderia and other multidrug-resistant cystic fibrosis-associated bacterial species. Antimicrob Agents Chemother 2009; 53: 249-255.
41. Sadikot RT, Blackwell TS, Christman JW, Prince AS. Pathogen-host interactions in Pseudomonas aeruginosa pneumonia. Am J Respir Crit Care Med 2005; 171: 1209-1223.
42. Sommer LM, Marvig RL, Lujan A, Koza A, Pressler T, Molin S, et al. Is genotyping of single isolates sufficient for population structure analysis of Pseudomonas aeruginosa in cystic fibrosis airways? BMC Genomics 2016; 17: 589.
43. Philippot L. Denitrification in pathogenic bacteria: for better or worst? Trends Microbiol 2005; 13: 191-192.
44. Tiwari M, Panwar S, Tiwari V. Assessment of potassium ion channel during electric signalling in biofilm formation of Acinetobacter baumannii for finding antibiofilm molecule. Heliyon 2023; 9(1): e12837.
45. Lundberg ME, Becker EC, Choe S. MstX and a putative potassium channel facilitate biofilm formation in Bacillus subtilis. PLoS One 2013; 8(5): e60993.
46. Prindle A, Liu J, Asally M, Ly S, Garcia-Ojalvo J, Suel GM. Ion channels enable electrical communication in bacterial communities. Nature 2015; 527: 59-63.
47. Liu J, Prindle A, Humphries J, Gabalda-Sagarra M, Asally M, Lee DY, et al. Metabolic co-dependence gives rise to collective oscillations within biofilms. Nature 2015; 523: 550–554.
48. Van Acker H, Coenye T. The role of efflux and physiological adaptation in biofilm tolerance and resistance. J Biol Chem 2016; 291: 12565-12572.
49. Baugh S, Ekanayaka AS, Piddock LJ, Webber MA. Loss of or inhibition of all multidrug resistance efflux pumps of Salmonella enterica serovar Typhimurium results in impaired ability to form a biofilm. J Antimicrob Chemother 2012; 67: 2409-2417.
50. Lamers RP, Cavallari JF, Burrows LL. The efflux inhibitor phenylalanine-arginine beta-naphthylamide (PAbetaN) permeabilizes the outer membrane of gram-negative bacteria. PLoS One 2013; 8(3): e60666.
51. Kvist M, Hancock V, Klemm P. Inactivation of efflux pumps abolishes bacterial biofilm formation. Appl Environ Microbiol 2008; 74: 7376-7382.
52. Phelps HA, Neely MN. SalY of the Streptococcus pyogenes antibiotic locus is required for full virulence and intracellular survival in macrophages. Infect Immun 2007; 75: 4541-4551.
53. Bogomolnaya LM, Andrews KD, Talamantes M, Maple A, Ragoza Y, Vazquez-Torres A, et al. The ABC-type efflux pump MacAB protects Salmonella enterica serovar typhimurium from oxidative stress. mBio 2013; 4(6): e00630-13.
54. Morgan R, Kohn S, Hwang S-H, Hassett DJ, Sauer K. BdlA, a chemotaxis regulator essential for biofilm dispersion in Pseudomonas aeruginosa. J Bacteriol 2006; 188: 7335-7343.
55. García-Fontana C, Reyes-Darias JA, Muñoz-Martínez F, Alfonso C, Morel B, Ramos JL, et al. High Specificity in CheR Methyltransferase Function: CheR2 of Pseudomonas putida is essential for chemotaxis, whereas CheR1 is involved in biofilm formation. J Biol Chem 2013; 288: 18987-18999.
| Files | ||
| Issue | Vol 15 No 3 (2023) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v15i3.12902 | |
| Keywords | ||
| Achromobacter mucicolens; Biofilms; Carbohydrates; Genome Bacterial; Drug resistance; Bacterial; Pathogenicity | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Al-Kahachi R, Al-Asadi S, Ali Z, Rampurawala J. Effects of genetic and environmental variables on biofilm development dynamics in Achromobacter mucicolens. Iran J Microbiol. 2023;15(3):414-424.
