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Metagenomic Insight Towards Vanillin-Mediated Membrane Biofouling Prevention: In Silico Docking Validation

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Abstract

Biofouling leads to water quality deterioration and higher maintenance cost for cleaning of membranes. The present study has demonstrated the application of a biomolecule (vanillin) in scrubbing and destabilizing biofilms of drinking water reverse osmosis (RO) membrane module in lab scale reactor set-up. Reverse osmosis membrane reactor was connected with tap water supply and subjected with optimal concentration of vanillin. The pressure drop was delayed by 17–20 days as compared to control reactor. Real-time PCR analysis of metagenome indicated the reduced copy number of functional biofilm-associated genes (bdlA, lasI, pgaC) in treated membrane. SEM and metagenome analysis revealed that the sticky biofilm communities shifted to loosely bound emboli after vanillin treatment. Metagenome sequence analysis revealed the inhibitory activity against major biofouling biota like members of Proteobacteria, Acidobacteria, Acnitobacteria, Bacteroidetes, Candidatus, Nitrospira, and Firmicutes. Biofouled membrane metagenome sequence was also compared with real-life (brackish water, waste water, domestic drinking water) biofouled membrane communities. In silico docking of vanillin to receptor proteins and chemical configuration simulation along with other phenolic derivatives were performed, which suggested that the autoiducer signal capability of vanillin was effective against representative broad spectrum biofilm population. Vanillin exhibited the quorum-quenching mode of action by virtue of docking towards similar amino acid (Thr 131, Ilu 214) responsible of autoinducer signal anchoring in the transcriptional regulatory proteins.

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References

  1. Waheed H, Hashmi I, Khan SJ, Kim SR, Arshad M, Nasir H (2016) Microbial population dynamics and profiling of quorum sensing agents in membrane bioreactor. Int Biodeterior Biodegrad 113:66–73. https://doi.org/10.1016/j.ibiod.2015.12.014

    Article  CAS  Google Scholar 

  2. Qureshi A, Pal S, Gosh S, Kapley A, Purohit HJ (2015) Antibiofouling biomaterials. Int J Recent Adv Multidiscip Res 2:677–684

    Google Scholar 

  3. Katebian L, Gomez E, Skillman L, Li D, Ho G, Jiang SC (2016) Inhibiting quorum sensing pathways to mitigate seawater desalination RO membrane biofouling. Desalination 393:135–143

    CAS  Google Scholar 

  4. Smolentseva O, Gusarov I, Gautier L, Shamovsky I, DeFrancesco AS, Losick R, Nudler E (2017) Mechanism of biofilm-mediated stress resistance and lifespan extension in C. elegans. Sci Rep 7:1–16

    CAS  Google Scholar 

  5. Brooke JS, Vo A, Watts P, Davis NA (2008) Mutation of a lipopolysaccharide synthesis gene results in increased biofilm of Stenotrophomonas maltophilia on plastic and glass surfaces. Ann Microbiol 58:35–40

    CAS  Google Scholar 

  6. Ghosh S, Qureshi A, Purohit HJ (2017) Enhanced expression of catechol 1, 2 dioxygenase gene in biofilm forming Pseudomonas mendocina EGD-AQ5 under increasing benzoate stress. Int Biodeterior Biodegrad 118:57–65

    CAS  Google Scholar 

  7. Vincent AT, Charette SJ, Barbeau J (2018) Unexpected diversity in the mobilome of a Pseudomonas aeruginosa strain isolated from a dental unit waterline revealed by SMRT Sequencing. Genome. https://doi.org/10.1139/gen-2017-0239

    Article  PubMed  Google Scholar 

  8. Velkov VV (2001) Stress-induced evolution and the biosafety of genetically modified microorganisms released into the environment. J Biosci 26:667

    PubMed  CAS  Google Scholar 

  9. Chede S, Anaya NM, Oyanedel-Craver V, Gorgannejad S, Harris TA, Al-Mallahi J, Abu-Dalo M, Qdais HA, Escobar IC (2017) Desalination using low biofouling nanocomposite membranes: from batch-scale to continuous-scale membrane fabrication. Desal. https://doi.org/10.1016/j.desal.2017.05.007

    Article  Google Scholar 

  10. Lade H, Paul D, Kweon J (2014) N-Acyl homoserine lactone-mediated quorum sensing with special reference to use of quorum quenching bacteria in membrane biofouling control. Biomed Res Int. https://doi.org/10.1155/2014/162584

    Article  PubMed  PubMed Central  Google Scholar 

  11. Federle MJ (2009) Autoinducer-2-based chemical communication in bacteria: complexities of interspecies signalling. Bact Sens Signal 16:18–32

    CAS  Google Scholar 

  12. Weerasekara NA, Choo KH, Lee CH (2016) Biofouling control: bacterial quorum quenching versus chlorination in membrane bioreactors. Water Res 103:293–301

    PubMed  CAS  Google Scholar 

  13. Oh HS, Kim SR, Cheong WS, Lee CH, Lee JK (2013) Biofouling inhibition in MBR by Rhodococcus sp. BH4 isolated from real MBR plant. Appl Microbiol Biotechnol 97:10223–10231

    PubMed  CAS  Google Scholar 

  14. Lee SH, Lee S, Lee K, Nahm CH, Kwon H, Oh HS, Won YJ, Choo KH, Lee CH, Park PK (2016) More efficient media design for enhanced biofouling control in a membrane bioreactor: quorum quenching bacteria entrapping hollow cylinder. Environ Sci Technol 50:8596–8604

    PubMed  CAS  Google Scholar 

  15. Pan Y, Wang Y, Yan X, Liu C, Wu B, He X, Liang Y (2019) Quorum quenching enzyme APTM01, an acylhomoserine-lactone acylase from marine bacterium of Pseudoalteromonas tetraodonis strain MQS005. Curr Microbiol 10:1–1

    Google Scholar 

  16. Jensen EC, Hornby JM, Pagliaccetti NE, Wolter CM, Nickerson KW, Atkin AL (2006) Farnesol restores wild-type colony morphology to 96% of Candida albicans colony morphology variants recovered following treatment with mutagens. Genome 49:346–353

    PubMed  CAS  Google Scholar 

  17. Tan B, Dong X, Sensen CW, Foght J (2013) Metagenomic analysis of an anaerobic alkane-degrading microbial culture: potential hydrocarbon-activating pathways and inferred roles of community members. Genome 56:599–611

    PubMed  CAS  Google Scholar 

  18. Teanpaisan R, Kawsud P, Pahumunto N, Puripattanavong J (2017) Screening for antibacterial and antibiofilm activity in Thai medicinal plant extracts against oral microorganisms. J Tradit Complement Med 7(2):172–177

    PubMed  Google Scholar 

  19. Chen L, Chong XY, Zhang YY, Lv YY, Hu YS (2019) Genome shuffling of Bacillus velezensis for enhanced surfactin production and variation analysis. Curr Microbiol 12:1–8

    Google Scholar 

  20. Fitzgerald DJ, Stratford M, Gasson MJ, Ueckert J, Bos A, Narbad A (2004) Mode of antimicrobial action of vanillin against Escherichia coli, Lactobacillus plantarum and Listeria innocua. J Appl Microbiol 97:104–113

    PubMed  CAS  Google Scholar 

  21. Ponnusamy K, Paul D, Kim YS, Kweon JH (2010) 2 (5H)-Furanone: a prospective strategy for biofouling-control in membrane biofilm bacteria by quorum sensing inhibition. Braz J Microbiol 41:227–234

    PubMed  PubMed Central  CAS  Google Scholar 

  22. Si X, Quan X (2017) Prevention of multi-species wastewater biofilm formation using vanillin and EPS disruptors through non-microbicidal mechanisms. Int Biodeterior Biodegrad 116:211–218

    CAS  Google Scholar 

  23. Ashhab A, Herzberg M, Gillor O (2014) Biofouling of reverse-osmosis membranes during tertiary wastewater desalination: microbial community composition. Water Res 50:341–349

    PubMed  Google Scholar 

  24. Pal S, Qureshi A, Purohit HJ (2016) Antibiofilm activity of biomolecules: gene expression study of bacterial isolates from brackish and fresh water biofouled membranes. Biologia 71:239–246

    CAS  Google Scholar 

  25. O’toole GA, Kolter R (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30:295–304

    PubMed  Google Scholar 

  26. Liu R, Huang X, Sun YF, Qian Y (2003) Hydrodynamic effect on sludge accumulation over membrane surfaces in a submerged membrane bioreactor. Process Biochem 39:157–216

    CAS  Google Scholar 

  27. Menzel P, Ng KL, Krogh A (2016) Fast and sensitive taxonomic classification for metagenomics with Kaiju. Nat Commun. https://doi.org/10.1038/ncomms11257

    Article  PubMed  PubMed Central  Google Scholar 

  28. Meyer F, Paarmann D, D'Souza M, Olson R, Glass EM, Kubal M, Paczian T, Rodriguez A, Stevens R, Wilke A, Wilkening J (2008) The metagenomics RAST server—a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinform 9:386

    CAS  Google Scholar 

  29. Bardou P, Mariette J, Escudié F, Djemiel C, Klopp C (2014) jvenn: an interactive Venn diagram viewer. BMC Bioinform 15:293

    Google Scholar 

  30. DeLano WL (2002) The PyMOL molecular graphics system. https://www.pymol.org.

  31. Schneidman-Duhovny D, Inbar Y, Nussinov R, Wolfson HJ (2005) PatchDock and SymmDock: servers for rigid and symmetric docking. Nucleic Acids Res 33:W363–W367

    PubMed  PubMed Central  CAS  Google Scholar 

  32. Pierce BG, Wiehe K, Hwang H, Kim BH, Vreven T, Weng Z (2014) ZDOCK server: interactive docking prediction of protein–protein complexes and symmetric multimers. Bioinformatics 30:1771–1773

    PubMed  PubMed Central  CAS  Google Scholar 

  33. Tikariha H, Pal RR, Qureshi A, Kapley A, Purohit HJ (2016) In silico analysis for prediction of degradative capacity of Pseudomonas putida SF1. Gene. https://doi.org/10.1016/j.gene.2016.06.028

    Article  PubMed  Google Scholar 

  34. Backman TW, Cao Y, Girke T (2011) ChemMine tools: an online service for analyzing and clustering small molecules. Nucleic Acids Res 39:W486–W491

    PubMed  PubMed Central  CAS  Google Scholar 

  35. Slobodníková L, Fialová S, Rendeková K, Kováč J, Mučaji P (2016) Antibiofilm activity of plant polyphenols. Molecules 21:1717

    PubMed Central  Google Scholar 

  36. You Y, Xie M, Vasseur L, You M (2018) Selecting and validating reference genes for quantitative real-time PCR in Plutella xylostella (L.). Genome. https://doi.org/10.1139/gen-2017-0176

    Article  PubMed  Google Scholar 

  37. An D, Brown D, Chatterjee I, Dong X, Ramos-Padron E, Wilson S, Bordenave S, Caffrey SM, Gieg LM, Sensen CW, Voordouw G (2013) Microbial community and potential functional gene diversity involved in anaerobic hydrocarbon degradation and methanogenesis in an oil sands tailings pond. Genome 56:612–618

    PubMed  CAS  Google Scholar 

  38. Pal S, Qureshi A, Purohit HJ (2018) Intercepting signalling mechanism to control environmental biofouling. 3 Biotech 8:364

    PubMed  PubMed Central  Google Scholar 

  39. Husain FM, Ahmad I, Asif M, Tahseen Q (2013) Influence of clove oil on certain quorum-sensing-regulated functions and biofilm of Pseudomonas aeruginosa and Aeromonas hydrophila. J Biosci 38:835–844

    PubMed  CAS  Google Scholar 

  40. Yi L, Wang Y, Ma Z, Zhang H, Li Y, Zheng JX, Yang YC, Fan HJ, Lu CP (2014) Biofilm formation of Streptococcus equi ssp. zooepidemicus and comparative proteomic analysis of biofilm and planktonic cells. Curr Microbiol 69:227–233

    PubMed  CAS  Google Scholar 

  41. Chew SC, Yang L (2017) Biofilms: microbial cities wherein flow shapes competition. Trends Microbiol 25:331–332

    PubMed  CAS  Google Scholar 

  42. Feng LJ, Mu J, Sun JY, Kong Y, Wang J, Lv ZH, Zhu L, Xu XY, Yang GF (2017) Kinetic characteristics and bacterial structures in biofilm reactors with pre-cultured biofilm for source water pretreatment. Int Biodeterior Biodegrad 121:26–34

    CAS  Google Scholar 

  43. Liu H, Tan S, Sheng Z, Yu T, Liu Y (2015) Impact of oxygen on the coexistence of nitrification, denitrification, and sulfate reduction in oxygen-based membrane aerated biofilm. Can J Microbiol 61:237–242

    PubMed  CAS  Google Scholar 

  44. Myszka K, Schmidt MT, Majcher M, Juzwa W, Olkowicz M, Czaczyk K (2016) Inhibition of quorum sensing-related biofilm of Pseudomonas fluorescens KM121 by Thymus vulgare essential oil and its major bioactive compounds. Int Biodeterior Biodegrad 114:252–259

    CAS  Google Scholar 

  45. Baqueiro-Peña I, Contreras-Jácquez V, Kirchmayr MR, Mateos-Díaz JC, Valenzuela-Soto EM, Asaff-Torres A (2019) Isolation and characterization of a new ferulic-acid-biotransforming Bacillus megaterium from maize alkaline wastewater (nejayote). Curr Microbiol 76:1215–1224

    PubMed  Google Scholar 

  46. Raut JS, Rajput SB, Shinde RB, Surwase BS, Karuppayil SM (2013) Vanillin inhibits growth, morphogenesis and biofilm formation by Candida albicans. J Biol Active Prod Nat 3:130–138

    CAS  Google Scholar 

  47. Cheong WS, Kim SR, Oh HS, Lee SH, Yeon KM, Lee CH, Lee JK (2014) Design of quorum quenching microbial vessel to enhance cell viability for biofouling control in membrane bioreactor. J Microbiol Biotechnol 24:97–105

    PubMed  CAS  Google Scholar 

  48. Maqbool T, Khan SJ, Waheed H, Lee CH, Hashmi I, Iqbal H (2015) Membrane biofouling retardation and improved sludge characteristics using quorum quenching bacteria in submerged membrane bioreactor. J Membr Sci 483:75–83

    CAS  Google Scholar 

  49. Barnharst T, Rajendran A, Hu B (2018) Bioremediation of synthetic intensive aquaculture wastewater by a novel feed-grade composite biofilm. Int Biodeterior Biodegrad 126:131–142

    CAS  Google Scholar 

  50. Bryers JD (2018) Modelling biofilm accumulation. Physiological models in microbiology. CRC Press, Baco Raton

    Google Scholar 

  51. Li Z, Nair SK (2012) Quorum sensing: how bacteria can coordinate activity and synchronize their response to external signals? Protein Sci 21:1403–1417

    PubMed  PubMed Central  CAS  Google Scholar 

  52. Bingham E, Cohrssen B, Powell CH (2001) Patty’s toxicology. Toxicological issues related to metals, neurotoxicology and radiation metals and metal compounds. Wiley, Hoboken

    Google Scholar 

  53. Char CD, Guerrero SN, Alzamora SM (2010) Mild thermal process combined with vanillin plus citral to help shorten the inactivation time for Listeria innocua in orange juice. Food Bioprocess Technol 3:752–761

    Google Scholar 

  54. Nowatzki PJ, Koepsel RR, Stoodley P, Min K, Harper A, Murata H, Donfack J, Hortelano ER, Ehrlich GD, Russell AJ (2012) Salicylic acid-releasing polyurethane acrylate polymers as anti-biofilm urological catheter coatings. Acta Biomater 8:1869–1880

    PubMed  CAS  Google Scholar 

  55. Yemiş GP, Pagotto F, Bach S, Delaquis P (2011) Effect of vanillin, ethyl vanillin, and vanillic acid on the growth and heat resistance of Cronobacter species. J food protection 74:2062–2069

    Google Scholar 

  56. Zhao R, Zhang H, Zou X, Yang F (2016) Effects of inhibiting acylated homoserine lactones (AHLs) on anammox activity and stability of granules’. Curr Microbiol 73(1):108–114

    PubMed  CAS  Google Scholar 

  57. Ng WL, Bassler BL (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222

    PubMed  PubMed Central  CAS  Google Scholar 

  58. Humphries J, Xiong L, Liu J, Prindle A, Yuan F, Arjes HA, Tsimring L, Süel GM (2017) Species-independent attraction to biofilms through electrical signaling. Cell 168:200–209

    PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgements

The authors wish to thank CSIR NEERI (KRC NO: CSIR-NEERI/KRC/2017/Nov/EBGD1), ESC0306 Clean Water; Sustainable Options: 12th plan Council of Scientific & Industrial Research network project and Department of Science and Technology (DST) Govt. of India (Indo-Egypt project), AcSIR, and Department of Science & Technology Inspire Fellowship.

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SP and AQ comprehended the idea and developed the theory. SP performed the data generation, analysis, and configured the manuscript. AQ and HJP sanctioned the grants, verified the analytical methods, encouraged to investigation, and supervised the findings of this work. All authors discussed the results and contributed to the final manuscript.

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Correspondence to Asifa Qureshi.

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Supplementary file1 (TIF 4017 kb)

Supplementary file2 (TIF 4767 kb)

Supplementary figure 1: Flow diagram of bioinformatics used in the study

Supplementary file3 (TIF 1391 kb)

Supplementary figure 2: Dose optimization of vanillin by treating biofilm consortia, Asterisks (*) represent p < 0.05, i.e statistical significant differences from the control. Error bars represent the standard deviations of nine replicates

Supplementary file4 (TIF 2309 kb)

Supplementary figure 3: qPCR analysis of biofouling genes followed by cycle threshold graph; higher Ct value indicates lower copy no of genes.

Supplementary file5 (TIF 1618 kb)

Supplementary figure 4: Bar diagram representing comparative account of taxonomic changes of Raw Membrane (RM) and Treated Membrane (TM).

Supplementary file6 (TIF 2054 kb)

Supplementary figure 5: Annotated Figfam distribution of functional biofouling proteins in RM and TM where bar plots represents cumulative proteins associated with specific category and donate graph represents individual sets of Fig families. Inner round of donate-graphs are RM category and outside circles represent TM category.

Supplementary file7 (TIF 4717 kb)

Supplementary figure 6,7 : chemical configuration mimicry of vanillin with autoinducer molecule based on physic chemical descriptors and multidimensional scaling cluster.

Supplementary file8 (TIF 3182 kb)

Supplementary file9 (TIF 4213 kb)

Supplementary figure 8: Ramachandran energy distribution revealed that vanillin could block signalling transduction

Supplementary file10 (TIF 3948 kb)

Supplementary figure 9: graphical representation of quorum-quenching mode of antibiofouling action of vanillin

Electronic supplementary material 11 (DOCX 17 kb)

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Pal, S., Qureshi, A. & Purohit, H.J. Metagenomic Insight Towards Vanillin-Mediated Membrane Biofouling Prevention: In Silico Docking Validation. Curr Microbiol 77, 2233–2247 (2020). https://doi.org/10.1007/s00284-020-02003-5

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