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.
Similar content being viewed by others
References
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
Qureshi A, Pal S, Gosh S, Kapley A, Purohit HJ (2015) Antibiofouling biomaterials. Int J Recent Adv Multidiscip Res 2:677–684
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
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
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
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
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
Velkov VV (2001) Stress-induced evolution and the biosafety of genetically modified microorganisms released into the environment. J Biosci 26:667
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
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
Federle MJ (2009) Autoinducer-2-based chemical communication in bacteria: complexities of interspecies signalling. Bact Sens Signal 16:18–32
Weerasekara NA, Choo KH, Lee CH (2016) Biofouling control: bacterial quorum quenching versus chlorination in membrane bioreactors. Water Res 103:293–301
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
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
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
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
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
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
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
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
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
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
Ashhab A, Herzberg M, Gillor O (2014) Biofouling of reverse-osmosis membranes during tertiary wastewater desalination: microbial community composition. Water Res 50:341–349
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
O’toole GA, Kolter R (1998) Flagellar and twitching motility are necessary for Pseudomonas aeruginosa biofilm development. Mol Microbiol 30:295–304
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
Menzel P, Ng KL, Krogh A (2016) Fast and sensitive taxonomic classification for metagenomics with Kaiju. Nat Commun. https://doi.org/10.1038/ncomms11257
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
Bardou P, Mariette J, Escudié F, Djemiel C, Klopp C (2014) jvenn: an interactive Venn diagram viewer. BMC Bioinform 15:293
DeLano WL (2002) The PyMOL molecular graphics system. https://www.pymol.org.
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
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
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
Backman TW, Cao Y, Girke T (2011) ChemMine tools: an online service for analyzing and clustering small molecules. Nucleic Acids Res 39:W486–W491
Slobodníková L, Fialová S, Rendeková K, Kováč J, Mučaji P (2016) Antibiofilm activity of plant polyphenols. Molecules 21:1717
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
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
Pal S, Qureshi A, Purohit HJ (2018) Intercepting signalling mechanism to control environmental biofouling. 3 Biotech 8:364
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
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
Chew SC, Yang L (2017) Biofilms: microbial cities wherein flow shapes competition. Trends Microbiol 25:331–332
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
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
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
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
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
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
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
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
Bryers JD (2018) Modelling biofilm accumulation. Physiological models in microbiology. CRC Press, Baco Raton
Li Z, Nair SK (2012) Quorum sensing: how bacteria can coordinate activity and synchronize their response to external signals? Protein Sci 21:1403–1417
Bingham E, Cohrssen B, Powell CH (2001) Patty’s toxicology. Toxicological issues related to metals, neurotoxicology and radiation metals and metal compounds. Wiley, Hoboken
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
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
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
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
Ng WL, Bassler BL (2009) Bacterial quorum-sensing network architectures. Annu Rev Genet 43:197–222
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
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.
Author information
Authors and Affiliations
Contributions
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.
Corresponding author
Ethics declarations
Conflict of interest
All the authors declare that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
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 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
Rights and permissions
About this article
Cite this article
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
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00284-020-02003-5