Abstract
A biofilm is a layer of microbes that have aggregated to form a colony. The colony attaches to a surface with a slime layer which protects the microorganisms, promoting their growth and survival. Biofilms occur in various environments such as soils, sediments, wastewater, water pipelines, water purifying systems, cooling water systems, medical devices, archaeological monuments, marine vessels, and hospitals. Biofilms may induce adverse effects such as fostering drug-resistant strains. Here, we review biofilms with focus on their formation, occurrence in water systems, impact, microbial interactions, and characterization methods. Communication includes cell-to-cell interactions by quorum sensing, interactions mediated by flagella, gene, and signaling molecules, and interactions mediated by extracellular polymeric substances. Characterization methods comprise surface-enhanced Raman scattering spectroscopy, confocal laser scanning microscopy, scanning electron microscopy, fluorescence microscopy, sensors, and metagenomics analysis.
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References
Abd-Elhalim BT, Hemdan BA, El-Sayed SM et al (2023) Enhancing durability and sustainable preservation of Egyptian stone monuments using metabolites produced by Streptomyces exfoliatus. Sci Rep 13:1–13. https://doi.org/10.1038/s41598-023-36542-1
Afonso TB, Simões LC, Lima N (2021) Occurrence of filamentous fungi in drinking water: their role on fungal-bacterial biofilm formation. Res Microbiol 172:103791. https://doi.org/10.1016/j.resmic.2020.11.002
Al-Amshawee S, Yunus MYBM, Vo DVN, Tran NH (2020) Biocarriers for biofilm immobilization in wastewater treatments: a review. Environ Chem Lett 18:1925–1945. https://doi.org/10.1007/s10311-020-01049-y
Alshammari M, Ahmad A, Alkhulaifi M et al (2023) Reduction of biofilm formation of Escherichia coli by targeting quorum sensing and adhesion genes using the CRISPR/Cas9-HDR approach, and its clinical application on urinary catheter. J Infect Public Health 16:1174–1183. https://doi.org/10.1016/j.jiph.2023.05.026
Arun D, Vimala R, Devendranath Ramkumar K (2020) Investigating the microbial-influenced corrosion of UNS S32750 stainless-steel base alloy and weld seams by biofilm-forming marine bacterium Macrococcus equipercicus. Bioelectrochemistry 135:107546. https://doi.org/10.1016/j.bioelechem.2020.107546
Avelino-Jiménez IA, Hernández-Maya L, Larios-Serrato V et al (2023) Biofouling and biocorrosion by microbiota from a marine oil pipeline: a metagenomic and proteomic approach. J Environ Chem Eng 11:109413. https://doi.org/10.1016/j.jece.2023.109413
Belas R (2014) Biofilms, flagella, and mechanosensing of surfaces by bacteria. Trends Microbiol 22:517–527. https://doi.org/10.1016/j.tim.2014.05.002
Bhardwaj DK, Taneja NK, Taneja P, Patel P (2022) Phenotypic and genotypic characterization of multi-drug resistant, biofilm forming, human invasive strain of Salmonella typhimurium SMC25 isolated from poultry meat in India. Microb Pathog 173:105830. https://doi.org/10.1016/j.micpath.2022.105830
Bodelón G, Montes-garcía V, López-puente V et al (2016) Detection and imaging of quorum sensing in Pseudomonas aeruginosa biofilm communities by surface-enhanced resonance Raman scattering. Nat Mater 15:1203–1211. https://doi.org/10.1038/nmat4720
Brown LR, Caulkins RC, Schartel TE et al (2017) Increased zinc availability enhances initial aggregation and biofilm formation of Streptococcus pneumoniae. Front Cell Infect Microbiol 7:1–12. https://doi.org/10.3389/fcimb.2017.00233
Cattò C, Mu A, Moreau JW et al (2023) Biofilm colonization of stone materials from an Australian outdoor sculpture: importance of geometry and exposure. J Environ Manag 339:117948. https://doi.org/10.1016/j.jenvman.2023.117948
Chen W, Gu Y, Xu H et al (2017) Variation of microbial communities and functional genes during the biofilm formation in raw water distribution systems and associated effects on the transformation of nitrogen pollutants. Environ Sci Pollut Res 24:15347–15359. https://doi.org/10.1007/s11356-017-9125-z
Chen Z, Meng Y, Sheng B et al (2019) Linking exoproteome function and structure to anammox biofilm development. Environ Sci Technol 53:1490–1500. https://doi.org/10.1021/acs.est.8b04397
Chonova T, Labanowski J, Cournoyer B et al (2018) River biofilm community changes related to pharmaceutical loads emitted by a wastewater treatment plant. Environ Sci Pollut Res 25:9254–9264. https://doi.org/10.1007/s11356-017-0024-0
Crisafi F, Smedile F, Yakimov MM et al (2022) Bacterial biofilms on medical masks disposed in the marine environment: a hotspot of biological and functional diversity. Sci Total Environ 837:155731. https://doi.org/10.1016/j.scitotenv.2022.155731
De Gregoris TB, Khandeparker L, Anil AC et al (2012) Characterisation of the bacteria associated with barnacle, Balanus amphitrite, shell and their role in gregarious settlement of cypris larvae. J Exp Mar Bio Ecol 413:7–12. https://doi.org/10.1016/j.jembe.2011.11.014
Delacuvellerie A, Brusselman A, Cyriaque V et al (2023) Long-term immersion of compostable plastics in marine aquarium: microbial biofilm evolution and polymer degradation. Mar Pollut Bull 189:114711. https://doi.org/10.1016/j.marpolbul.2023.114711
Denk W, Strickler JH, Webb WW (1990) Two-photon laser scanning fluorescence microscopy. Science 248:73–76. https://doi.org/10.1126/science.23210
Diaz PI, Xie Z, Sobue T et al (2012) Synergistic interaction between Candida albicans and commensal oral Streptococci in a novel in vitro mucosal model. Infect Immun 80:620–632. https://doi.org/10.1128/IAI.05896-11
Dong F, Li C, Lin Q, Duan H (2019) Effect of pipe materials on disinfection by-products and bacterial communities during sulfamethazine chlorination in a pilot-scale water distribution system. Environ Chem Lett 17:1039–1044. https://doi.org/10.1007/s10311-018-00823-3
Dong Y, Feng D, Song G et al (2022) The effect of a Biofilm-forming bacterium Tenacibaculum mesophilum D-6 on the passive fi lm of stainless steel in the marine environment. Sci Total Environ 815:152909. https://doi.org/10.1016/j.scitotenv.2021.152909
Douterelo I, Sharpe RL, Boxall JB (2013) Influence of hydraulic regimes on bacterial community structure and composition in an experimental drinking water distribution system. Water Res 47:503–516. https://doi.org/10.1016/j.watres.2012.09.053
Douterelo I, Calero-preciado C, Soria-carrasco V, Boxall JB (2018) Whole metagenome sequencing of chlorinated drinking water distribution systems drinking water distribution systems. Environ Sci Water Res Technol 4:2080–2091. https://doi.org/10.1039/c8ew00395e
Dranguet P, Cosio C, Le FS et al (2017) Biofilm composition in the Olt River (Romania) reservoirs impacted by a chlor-alkali production plant. Environ Sci Process Impacts 19:687–695. https://doi.org/10.1039/C7EM00033B
Duan Y, Wu F, He D et al (2021) Bacterial and fungal communities in the sandstone biofilms of two famous Buddhist grottoes in China. Int Biodeterior Biodegrad 163:105267. https://doi.org/10.1016/j.ibiod.2021.105267
El-Shahat A, Minas H, Khomiara S (2014) Weathering of calcarenite monuments at roman and byzantine archaeological sites at Sabratha, northwestern Libya: a pilot study. African Archaeol Rev 31:45–58. https://doi.org/10.1007/s10437-014-9153-8
Eyssautier-Chuine S, Vaillant-Gaveau N, Charpentier E, Reffuveille F (2021) Comparison of biofilm development on three building and restoration stones used in French monuments. Int Biodeterior Biodegrad 165:105322. https://doi.org/10.1016/j.ibiod.2021.105322
Fan F, Liu Y, Liu Y et al (2022) Candida albicans biofilms: antifungal resistance, immune evasion, and emerging therapeutic strategies. Int J Antimicrob Agents 60:106673. https://doi.org/10.1016/j.ijantimicag.2022.106673
Farkas A, Song S, Degiuli N et al (2020) Impact of biofilm on the ship propulsion characteristics and the speed reduction. Ocean Eng 199:107033. https://doi.org/10.1016/j.oceaneng.2020.107033
Farkas A, Degiuli N, Martic I (2021) The impact of biofouling on the propeller performance. Ocean Eng 219:108376. https://doi.org/10.1016/j.oceaneng.2020.108376
Farkas A, Degiuli N, Martic I et al (2022) The impact of biofilm on marine current turbine performance. Renew Energy 190:584–595. https://doi.org/10.1016/j.renene.2022.03.134
Fish K, Osborn AM, Boxall J (2016) Characterising and understanding the impact of microbial biofilms and the extracellular polymeric substance (EPS) matrix in drinking water distribution systems. Environ Sci Water Res Technol 2:614–630. https://doi.org/10.1039/c6ew00039h
Flemming H, Wingender J (2010) The biofilm matrix. Nat Rev Microbiol 8:623–633. https://doi.org/10.1038/nrmicro2415
Fu Y, Peng H, Liu J et al (2021) Occurrence and quantification of culturable and viable but non-culturable (VBNC) pathogens in biofilm on different pipes from a metropolitan drinking water distribution system. Sci Total Environ 764:142851. https://doi.org/10.1016/j.scitotenv.2020.142851
Fysun O, Khorshid S, Rauschnabel J, Langowski H (2019) Electrochemical detection of a P. polymyxa biofilm and CIP cleaning solutions by voltammetric microsensors. Eng Agric Environ Food 12:232–243. https://doi.org/10.1016/j.eaef.2019.01.004
Gabriele F, Ranaldi R, Bruno L et al (2023) Biodeterioration of stone monuments: studies on the influence of bioreceptivity on cyanobacterial biofilm growth and on the biocidal efficacy of essential oils in natural hydrogel. Sci Total Environ 870:161901. https://doi.org/10.1016/j.scitotenv.2023.161901
Gaiser EE, Anderson EP, Castañeda-Moya E et al (2015) New perspectives on an iconic landscape from comparative international long-term ecological research. Ecosphere 6:181. https://doi.org/10.1890/ES14-00388.1
García-Diéguez L, Diaz-Tang G, Marin Meneses E et al (2023) Periodically disturbing biofilms reduces expression of quorum sensing-regulated virulence factors in Pseudomonas aeruginosa. iScience 26:106843. https://doi.org/10.1016/j.isci.2023.106843
George J, Anand SS, Senthil Kumar P et al (2022) Biocatalytic polymeric membranes to decrease biofilm fouling and remove organic contaminants in wastewater: a review. Environ Chem Lett 20:1897–1927. https://doi.org/10.1007/s10311-022-01413-0
González JE, Keshavan ND (2006) Messing with bacterial quorum sensing. Microbiol Mol Biol Rev 70:859–875. https://doi.org/10.1128/mmbr.00002-06
Goraj W, Pytlak A, Kowalska B et al (2021) Influence of pipe material on biofilm microbial communities found in drinking water supply system. Environ Res 196:110433. https://doi.org/10.1016/j.envres.2020.110433
Gregorio LD, Tandoi V, Congestri R et al (2017) Unravelling the core microbiome of biofilms in cooling tower systems. Biofouling 33:793–806. https://doi.org/10.1080/08927014.2017.1367386
Guillaume O, Butnarasu C, Visentin S, Reimhult E (2022) Interplay between biofilm microenvironment and pathogenicity of Pseudomonas aeruginosa in cystic fibrosis lung chronic infection. Biofilm 4:100089. https://doi.org/10.1016/j.bioflm.2022.100089
Gujinović L, Maravić A, Kalinić H et al (2022) Metagenomic analysis of pioneer biofilm-forming marine bacteria with emphasis on Vibrio gigantis adhesion dynamics. Colloids Surf B 217:112619. https://doi.org/10.1016/j.colsurfb.2022.112619
Guliy OI, Evstigneeva SS, Bunin VD (2022) Microfluidic bioanalytical system for biofilm formation indication. Talanta 247:123541. https://doi.org/10.1016/j.talanta.2022.123541
Guo L, Wan K, Zhu J et al (2021) Detection and distribution of vbnc/viable pathogenic bacteria in full-scale drinking water treatment plants. J Hazard Mater 406:124335. https://doi.org/10.1016/j.jhazmat.2020.124335
Habimana O, Semião AJC, Casey E (2014) The role of cell-surface interactions in bacterial initial adhesion and consequent biofilm formation on nanofiltration/reverse osmosis membranes. J Membr Sci 454:82–96. https://doi.org/10.1016/j.memsci.2013.11.043
Hadfield MG (2011) Biofilms and marine invertebrate larvae: What bacteria produce larvae use to choose settlement sites. Ann Rev Mar Sci 3:453–470. https://doi.org/10.1146/annurev-marine-120709-142753
Hadžić N, Gatin I, Uroić T, Ložar V (2022) Biofouling dynamic and its impact on ship powering and dry-docking. Ocean Eng 245:110522. https://doi.org/10.1016/j.oceaneng.2022.110522
Han F, Zhang M, Liu Z et al (2021) Dynamic characteristics of microbial community and soluble microbial products in partial nitrification biofilm system developed from marine sediments treating high salinity wastewater. J Environ Manag 290:112586. https://doi.org/10.1016/j.jenvman.2021.112586
Hansen SK, Rainey PB, Haagensen JAJ, Molin S (2007) Evolution of species interactions in a biofilm community. Nature 445:533–536. https://doi.org/10.1038/nature05514
He Y, Luckett J, Begines B et al (2022) Ink-jet 3D printing as a strategy for developing bespoke non-eluting biofilm resistant medical devices. Biomaterials 281:121350. https://doi.org/10.1016/j.biomaterials.2021.121350
Hu H, Johani K, Gosbell IB et al (2015) Intensive care unit environmental surfaces are contaminated by multidrug-resistant bacteria in biofilms: combined results of conventional culture, pyrosequencing, scanning electron microscopy, and confocal laser microscopy. J Hosp Infect 91:35–44. https://doi.org/10.1016/j.jhin.2015.05.016
Hu H, He J, Yu H et al (2017) A strategy to speed up formation and strengthen activity of biofilms at low temperature. RSC Adv 7:22788–22796. https://doi.org/10.1039/c7ra02223a
Hwang G, Dong T, Islam MS et al (2013) The impacts of ozonation on oil sands process-affected water biodegradability and biofilm formation characteristics in bioreactors. Bioresour Technol 130:269–277. https://doi.org/10.1016/j.biortech.2012.12.005
Inaba T, Hori T, Tsuchiya M et al (2023) Microscopic evidence of sandstone deterioration and damage by fungi isolated from the Angkor monuments in simulation experiments. Sci Total Environ 896:165265. https://doi.org/10.1016/j.scitotenv.2023.165265
Itoh Y, Rice JD, Goller C et al (2008) Roles of pgaABCD genes in synthesis, modification, and export of the Escherichia coli biofilm adhesin poly-β-1,6-N-acetyl-d-glucosamine. J Bacteriol 190:3670–3680. https://doi.org/10.1128/JB.01920-07
Jung H, Inaba Y, West AC, Banta S (2023) Overexpression of quorum sensing genes in Acidithiobacillus ferrooxidans enhances cell attachment and covellite bioleaching. Biotechnol Rep 38:e00789. https://doi.org/10.1016/j.btre.2023.e00789
Kamjunke N, Spohn U, Füting M et al (2012) Use of confocal laser scanning microscopy for biofilm investigation on paints under field conditions. Int Biodeterior Biodegrad 69:17–22. https://doi.org/10.1016/j.ibiod.2011.11.015
Karygianni L, Ren Z, Koo H, Thurnheer T (2020) Biofilm matrixome: extracellular components in structured microbial communities. Trends Microbiol 28:668–681. https://doi.org/10.1016/j.tim.2020.03.016
Keshari N, Das SK, Adhikary SP (2021) Colonization and survival of a stress tolerant cyanobacterium on a heritage monument of Santiniketan, India. Int Biodeterior Biodegrad 164:105294. https://doi.org/10.1016/j.ibiod.2021.105294
Khan S, Beattie TK, Knapp CW (2019) Rapid selection of antimicrobial-resistant bacteria in complex water systems by chlorine and pipe materials. Environ Chem Lett 17:1367–1373. https://doi.org/10.1007/s10311-019-00867-z
Kim H, Kim T, Aziz AA et al (2020) Structural heterogeneity yet high similarity of the microbial community on reverse osmosis membrane-driven biofilms during seawater desalination. Environ Sci Water Res Technol 6:3066–3079. https://doi.org/10.1039/d0ew00366b
Koo H, Yamada KM (2016) Dynamic cell–matrix interactions modulate microbial biofilm and tissue 3D microenvironments. Curr Opin Cell Biol 42:102–112. https://doi.org/10.1016/j.ceb.2016.05.005
Krishna KCB, Sathasivan A, Ginige MP (2021) An assessment of the persistence of putative pathogenic bacteria in chloraminated water distribution systems. Water Res 190:116677. https://doi.org/10.1016/j.watres.2020.116677
Krsmanovic M, Biswas D, Ali H et al (2021) Hydrodynamics and surface properties influence biofilm proliferation. Adv Colloid Interface Sci 288:102336. https://doi.org/10.1016/j.cis.2020.102336
Learbuch KLG, Smidt H, Van Der Wielen PWJJ (2023) Water and biofilm in drinking water distribution systems in the Netherlands. Sci Total Environ 831:154940. https://doi.org/10.1016/j.scitotenv.2022.154940
Lebeaux D, Chauhan A, Rendueles O, Beloin C (2013) From in vitro to in vivo models of bacterial biofilm-related infections. Pathogens 2:288–356. https://doi.org/10.3390/pathogens2020288
Li A, Hou B, Li M (2015) Cell adhesion, ammonia removal and granulation of autotrophic nitrifying sludge facilitated by N-acyl-homoserine lactones. Bioresour Technol 196:550–558. https://doi.org/10.1016/j.biortech.2015.08.022
Li W, Zhang Y, Wu N et al (2019) Colonization characteristics of bacterial communities on plastic debris influenced by environmental factors and polymer types in the Haihe Estuary of Bohai Bay, China. Environ Sci Technol 53:10763–10773. https://doi.org/10.1021/acs.est.9b03659
Li J, Deng M, Gao L et al (2021) The active microbes and biochemical processes contributing to deterioration of Angkor sandstone monuments under the tropical climate in Cambodia—a review. J Cult Herit 47:218–226. https://doi.org/10.1016/j.culher.2020.10.010
Li Z, Wang X, Wang J et al (2022) Bacterial biofilms as platforms engineered for diverse applications. Biotechnol Adv 57:107932. https://doi.org/10.1016/j.biotechadv.2022.107932
Liang X, Meng S, He Z et al (2023) Higher abundance of ammonia-oxidizing bacteria than ammonia-oxidizing archaea in biofilms and the microbial community composition of Kaiping Diaolou of China. Int Biodeterior Biodegrad 184:105647. https://doi.org/10.1016/j.ibiod.2023.105647
Liao JC, Zou SJ, Deng YL et al (2023) Multivariate analysis of liquid biopsies for real-time detection of patients with biofilm-associated infections (BAI). Chem Eng J 453:139595. https://doi.org/10.1016/j.cej.2022.139595
Liu D, Rong C, Jin J et al (2018) Characteristics of biofilm community structure in a reclaimed water cast iron pipeline. Environ Sci Water Res Technol 4:1489–1500. https://doi.org/10.1039/C8EW00240A
Liu X, Qian Y, Wu F et al (2022) Microbiology forum monuments: Biodeterioration or bioprotection? Trends Microbiol 30:816–819. https://doi.org/10.1016/j.tim.2022.05.012
Luengthamchat N, Koontongkaew S, Utispan K (2022) Bitter taste perception and dental biofilm cariogenicity in orthodontics. Int Dent J 72:805–810. https://doi.org/10.1016/j.identj.2022.07.003
Ma C, Yu S, Shi W et al (2013) Effect of different temperatures on performance and membrane fouling in high concentration PAC-MBR system treating micro-polluted surface water. Bioresour Technol 141:19–24. https://doi.org/10.1016/j.biortech.2013.02.025
Mandal S, Rath J (2013) Algal colonization and its ecophysiology on the fine sculptures of terracotta monuments of Bishnupur, West Bengal, India. Int Biodeterior Biodegrad 84:291–299. https://doi.org/10.1016/j.ibiod.2012.05.034
Mao G, Wang Y, Hammes F (2018) Short-term organic carbon migration from polymeric materials in contact with chlorinated drinking water. Sci Total Environ 613–614:1220–1227. https://doi.org/10.1016/j.scitotenv.2017.09.166
Martínez-García S, Ortiz-García CI, Cruz-Aguilar M et al (2019) Competition/antagonism associations of biofilm formation among Staphylococcus epidermidis Agr groups I, II, and III. J Microbiol 57:143–153. https://doi.org/10.1007/s12275-019-8322-5
Mcfadden R, Quinn J, Buchanan F et al (2023) An effective laser surface treatment method to reduce biofilm coverage of multiple bacterial species associated with medical device infection. Surf Coat Technol 453:129092. https://doi.org/10.1016/j.surfcoat.2022.129092
Medina WRM (2020) Sewer biofilm microbiome and antibiotic resistance genes as function of pipe material, source of microbes, and disinfection: field and laboratory studies. Environ Sci Water Res Technol 6:2122–2137. https://doi.org/10.1039/d0ew00265h
Mihajlovski A, Seyer D, Benamara H et al (2015) An overview of techniques for the characterization and quantification of microbial colonization on stone monuments. Ann Microbiol 65:1243–1255. https://doi.org/10.1007/s13213-014-0956-2
Mihajlovski A, Gabarre A, Seyer D et al (2017) Bacterial diversity on rock surface of the ruined part of a French historic monument: the Chaalis abbey. Int Biodeterior Biodegrad 120:161–169. https://doi.org/10.1016/j.ibiod.2017.02.019
Muhammad MH, Idris AL, Fan X et al (2020) Beyond risk: bacterial biofilms and their regulating approaches. Front Microbiol 11:928. https://doi.org/10.3389/fmicb.2020.00928
Nakamura Y, Yamamoto N, Kino Y et al (2016) Establishment of a multi-species biofilm model and metatranscriptomic analysis of biofilm and planktonic cell communities. Appl Microbiol Biotechnol 100:7263–7279. https://doi.org/10.1007/s00253-016-7532-6
Okuda S, Tsuchiya Y, Kiriyama C et al (2012) Virtual metagenome reconstruction from 16S rRNA gene sequences. Nat Commun 3:1203. https://doi.org/10.1038/ncomms2203
Özdemir A, Erguven GO, Adar E, Nuhoglu Y (2020) Investigation on microbial biodeterioration of the stone monuments in Yildiz Technical University—Yildiz campus—Istanbul—Turkey. Curr Microbiol 77:3288–3299. https://doi.org/10.1007/s00284-020-02171-4
Pan M, Li H, Han X et al (2022) Effects of hydrodynamic conditions on the composition, spatiotemporal distribution of different extracellular polymeric substances and the architecture of biofilms. Chemosphere 307:135965. https://doi.org/10.1016/j.chemosphere.2022.135965
Parker AE, Christen JA, Lorenz L et al (2020) Optimal surface estimation and thresholding of confocal microscope images of biofilms using Beer’s Law. J Microbiol Methods 174:105943. https://doi.org/10.1016/j.mimet.2020.105943
Pereira J, de Nooy S, Sleutels T, ter Heijne A (2022) Opportunities for visual techniques to determine characteristics and limitations of electro-active biofilms. Biotechnol Adv 60:108011. https://doi.org/10.1016/j.biotechadv.2022.108011
Perez C, Lors C, Erable B (2022) Methodological approaches for the structural, chemical, and microbial analysis of microbial biofilms developed on the surface of cementitious materials: overview and future prospects. Int Biodeterior Biodegrad 175:105485. https://doi.org/10.1016/j.ibiod.2022.105485
Periakaruppan P, Abraham R, Mahendran K, Ramanathan M (2018) Simple synthesis of hydrazones with quorum quenching activity at room temperature in water. Environ Chem Lett 16:1063–1067. https://doi.org/10.1007/s10311-018-0720-0
Pfendler S, Borderie F, Bousta F et al (2018a) Comparison of biocides, allelopathic substances and UV-C as treatments for biofilm proliferation on heritage monuments. J Cult Herit 33:117–124. https://doi.org/10.1016/j.culher.2018.03.016
Pfendler S, Munch T, Bousta F et al (2018b) Bleaching of biofilm-forming algae induced by UV-C treatment: a preliminary study on chlorophyll degradation and its optimization for an application on cultural heritage. Environ Sci Pollut Res 25:14097–14105. https://doi.org/10.1007/s11356-018-1654-6
Preciado CC, Husband S, Boxall J et al (2021) Intermittent water supply impacts on distribution system biofilms and water quality. Water Res 201:117372. https://doi.org/10.1016/j.watres.2021.117372
Proctor CR, Gächter M, Kötzsch S, Rölli F et al (2016) Biofilms in shower hoses—choice of pipe material influences bacterial growth and communities. Environ Sci Water Res Technol 2:670–682. https://doi.org/10.1039/C6EW00016A
Quiñones B, Dulla G, Lindow SE (2005) Quorum sensing regulates exopolysaccharide production, motility, and virulence in Pseudomonas syringae. Mol Plant Microbe Interact 18:682–693. https://doi.org/10.1094/MPMI-18-0682
Rahimpour M, Montero M, Almagro G et al (2013) GlgS, described previously as a glycogen synthesis control protein, negatively regulates motility and biofilm formation in Escherichia coli. Biochem J 452:559–573. https://doi.org/10.1042/BJ20130154
Rajitha K, Nancharaiah YV, Venugopalan VP (2020) Insight into bacterial biofilm-barnacle larvae interactions for environmentally benign antifouling strategies. Int Biodeterior Biodegrad 149:104937. https://doi.org/10.1016/j.ibiod.2020.104937
Rasmussen TB, Skindersoe ME, Bjarnsholt T et al (2005) Identity and effects of quorum-sensing inhibitors produced by Penicillium species. Microbiology 151:1325–1340. https://doi.org/10.1099/mic.0.27715-0
Ren H, Wang W, Liu Y et al (2015) Pyrosequencing analysis of bacterial communities in biofilms from different pipe materials in a city drinking water distribution system of East China. Appl Microbiol Biotechnol 99:10713–10724. https://doi.org/10.1007/s00253-015-6885-6
Rho H, Yu P, Zhao Z et al (2022) Inhibition of biofouling on reverse osmosis membrane surfaces by germicidal ultraviolet light side-emitting optical fibers. Water Res 224:119094. https://doi.org/10.1016/j.watres.2022.119094
Rilstone V, Vignale L, Craddock J et al (2021) The role of antibiotics and heavy metals on the development, promotion, and dissemination of antimicrobial resistance in drinking water biofilms. Chemosphere 282:131048. https://doi.org/10.1016/j.chemosphere.2021.131048
Robuschi L, Tomba JP, Pablo J (2017) Proving Geobacter biofilm connectivity with confocal raman microscopy. J Electroanal Chem 793:99–103. https://doi.org/10.1016/j.jelechem.2016.11.005
Rumbaugh KP, Trivedi U, Watters C et al (2012) Kin selection, quorum sensing and virulence in pathogenic bacteria. Proc R Soc B Biol Sci 279:3584–3588. https://doi.org/10.1098/rspb.2012.0843
Sanmartín P, Rodríguez A, Aguiar U (2020) Medium-term field evaluation of several widely used cleaning-restoration techniques applied to algal biofilm formed on a granite-built historical monument. Int Biodeterior Biodegrad 147:104870. https://doi.org/10.1016/j.ibiod.2019.104870
Schlafer S, Meyer RL (2017) Confocal microscopy imaging of the biofilm matrix. J Microbiol Methods 138:50–59. https://doi.org/10.1016/j.mimet.2016.03.002
Schwering M, Song J, Louie M et al (2013) Multi-species biofilms defined from drinking water microorganisms provide increased protection against chlorine disinfection. Biofouling 29:917–928. https://doi.org/10.1080/08927014.2013.816298
Sengupta P, Surwase SS, Prasad BLV (2018) Modification of porous polyethylene scaffolds for cell attachment and proliferation. Int J Nanomed 13:87–90. https://doi.org/10.2147/IJN.S125000
Seo H, Kim J, Jung J et al (2012) Complexity of cell-cell interactions between Pseudomonas sp. AS1 and Acinetobacter oleivorans DR1: metabolic commensalism, biofilm formation and quorum quenching. Res Microbiol 163:173–181. https://doi.org/10.1016/j.resmic.2011.12.003
Siedlecka A, Wolf-Baca M, Piekarska K (2021) Microbial communities of biofilms developed in a chlorinated drinking water distribution system: a field study of antibiotic resistance and biodiversity. Sci Total Environ 774:145113. https://doi.org/10.1016/j.scitotenv.2021.145113
Singh BP, Ghosh S, Chauhan A (2021) Development, dynamics and control of antimicrobial-resistant bacterial biofilms: a review. Environ Chem Lett 19:1983–1993. https://doi.org/10.1007/s10311-020-01169-5
Song J, Li Y, Ke D et al (2022) In situ graphene-modified carbon microelectrode array biosensor for biofilm impedance analysis. Electrochim Acta 403:139570. https://doi.org/10.1016/j.electacta.2021.139570
Song Y, Wang R, Pan Y et al (2023) An integrated quorum quenching biocatalytic nanoplatform for synergistic chemo-photothermal eradication of P. aeruginosa biofilm infections. Acta Biomater 171:532–542. https://doi.org/10.1016/j.actbio.2023.09.021
Sousa ML, Chow F, Pompêo MLM (2019) Community-level changes in periphytic biofilm caused by copper contamination. J Appl Phycol 31:2401–2410. https://doi.org/10.1007/s10811-019-1734-0
Souza JGS, Costa RC, Sampaio AA et al (2022) Cross-kingdom microbial interactions in dental implant-related infections: is Candida albicans a new villain? iScience 25:103994. https://doi.org/10.1016/j.isci.2022.103994
Stewart PS, Bjarnsholt T (2020) Risk factors for chronic biofilm-related infection associated with implanted medical devices. Clin Microbiol Infect 26:1034–1038. https://doi.org/10.1016/j.cmi.2020.02.027
Suihko ML, Alakomi HL, Gorbushina A et al (2007) Characterization of aerobic bacterial and fungal microbiota on surfaces of historic Scottish monuments. Syst Appl Microbiol 30:494–508. https://doi.org/10.1016/j.syapm.2007.05.001
Tan CH, Oh H, Sheraton VM et al (2020) Convection and the extracellular matrix dictate inter- and intra-biofilm quorum sensing communication in environmental systems. Environ Sci Technol 54(11):6730–6740. https://doi.org/10.1021/acs.est.0c00716
Taylor P, Mieszkin S, Callow ME, Callow JA (2013) Interactions between microbial biofilms and marine fouling algae: a mini review. Biofouling 29:1097–1113. https://doi.org/10.1080/08927014.2013.828712
Tejedor-Sanz S, Ortiz JM, Esteve-Núñez A (2017) Merging microbial electrochemical systems with electrocoagulation pretreatment for achieving a complete treatment of brewery wastewater. Chem Eng J 330:1068–1074. https://doi.org/10.1016/j.cej.2017.08.049
Theerthagiri J, Park J, Das HT et al (2022) Electrocatalytic conversion of nitrate waste into ammonia: a review. Environ Chem Lett 20:2929–2949. https://doi.org/10.1007/s10311-022-01469-y
Theerthagiri J, Karuppasamy K, Mahadi AH et al (2023a) Electrochemical reduction of gaseous nitric oxide into ammonia: a review. Environ Chem Lett. https://doi.org/10.1007/s10311-023-01655-6
Theerthagiri J, Karuppasamy K, Park J et al (2023b) Electrochemical conversion of biomass-derived aldehydes into fine chemicals and hydrogen: a review. Environ Chem Lett 21:1555–1583. https://doi.org/10.1007/s10311-022-01543-5
Tichy J, Waldherr M, Ortbauer M et al (2023) Pretty in pink? Complementary strategies for analysing pink biofilms on historical buildings. Sci Total Environ 904:166737. https://doi.org/10.1016/j.scitotenv.2023.166737
Venkata HNN, Nomura N, Shigeto S (2011) Leucine pools in Escherichia coli biofilm discovered by Raman imaging. J Raman Spectrosc 42:1913–1915. https://doi.org/10.1002/jrs.2952
Vernon JJ, Mostafa E, Aw J et al (2022) Dental implant surfaces and their interaction with the oral microbiome. Dent Rev 2:100060. https://doi.org/10.1016/j.dentre.2022.100060
Vidakovic L, Mikhaleva S, Jeckel H et al (2023) Biofilm formation on human immune cells is a multicellular predation strategy of Vibrio cholerae. Cell 186:2690-2704.e20. https://doi.org/10.1016/j.cell.2023.05.008
Vlasov DY, Zelenskaya MS, Sazanova KV et al (2023) Diversity and significance of lithobiotic communities at the tomskaya pisanitsa rock art site. Contemp Probl Ecol 16:173–188. https://doi.org/10.1134/S1995425523020130
Wagner M, Ivleva NP, Haisch C et al (2009) Combined use of confocal laser scanning microscopy (CLSM) and Raman microscopy (RM): investigations on EPS–matrix. Water Res 43:63–76. https://doi.org/10.1016/j.watres.2008.10.034
Wang H, Masters S, Edwards MA et al (2014) Effect of disinfectant, water age, and pipe materials on bacterial and eukaryotic community structure in drinking water biofilm. Environ Sci Technol 48:1426–1435. https://doi.org/10.1021/es402636u
Wang J, Li G, Yin H, An T (2020) Bacterial response mechanism during biofilm growth on different metal material substrates: EPS characteristics, oxidative stress and molecular regulatory network analysis. Environ Res 185:109451. https://doi.org/10.1016/j.envres.2020.109451
Wang J, Yang X, Cui M et al (2022) A high-sensitive and durable electrochemical sensor based on Geobacter-dominated biofilms for heavy metal toxicity detection. Biosens Bioelectron 206:114146. https://doi.org/10.1016/j.bios.2022.114146
Wang X, Ma K, Zhang C et al (2023) The interaction among Kluyveromyces marxianus G-Y4, Lacticaseibacillus paracasei GL1, and Lactobacillus helveticus SNA12 and signaling molecule AI-2 participate in the formation of biofilm. Food Microbiol 116:104369. https://doi.org/10.1016/j.fm.2023.104369
Wasim M, Shoaib S, Mubarak NM et al (2018) Factors influencing corrosion of metal pipes in soils. Environ Chem Lett 16:861–879. https://doi.org/10.1007/s10311-018-0731-x
Waters CM, Bassler BL (2005) Quorum sensing: cell-to-cell communication in bacteria. Annu Rev Cell Dev Biol 21:319–346. https://doi.org/10.1146/annurev.cellbio.21.012704.131001
Watson F, Swann M, Zimmer A et al (2022) Aspects of biofilms on medical devices. In: Kungwani NA, Das S (eds) Understanding microbial biofilms. Academic Press, Cambridge, pp 91–105
Wijesundara NM, Lee SF, Rupasinghe HPV (2022) Carvacrol inhibits Streptococcus pyogenes biofilms by suppressing the expression of genes associated with quorum-sensing and reducing cell surface hydrophobicity. Microb Pathog 169:105684. https://doi.org/10.1016/j.micpath.2022.105684
Wilson C, Lukowicz R, Merchant S et al (2017) Quantitative and qualitative assessment methods for biofilm growth: a mini-review. Res Rev J Eng Technol 6:1–25
Won S, Phillips KS, Gu H, Kazemzadeh-narbat M (2021) How microbes read the map: effects of implant topography on bacterial adhesion and biofilm formation. Biomaterials 268:120595. https://doi.org/10.1016/j.biomaterials.2020.120595
Wu Y, Xia L, Yu Z et al (2014a) In situ bioremediation of surface waters by periphytons. Bioresour Technol 151:367–372. https://doi.org/10.1016/j.biortech.2013.10.088
Wu Z, Wang Q, Guo F et al (2014b) Responses of bacterial strains isolated from drinking water environments to N-acyl-L-homoserine lactones and their analogs during biofilm formation. Front Environ Sci Eng 8:205–214. https://doi.org/10.1007/s11783-013-0492-5
Wu H, Zhang J, Mi Z, Xie S (2015) Biofilm bacterial communities in urban drinking water distribution systems transporting waters with different purification strategies. Appl Microbiol Biotechnol 99:1947–1955. https://doi.org/10.1007/s00253-014-6095-7
Wu Y, Zhou Z, Fu H et al (2022) Metagenomic analysis of microbial community and gene function of anodic biofilm for nonylphenol removal in microbial fuel cells. J Clean Prod 374:133895. https://doi.org/10.1016/j.jclepro.2022.133895
Xiao X, Zhu WW, Liu QY et al (2016) Impairment of biofilm formation by TiO2 photocatalysis through quorum quenching. Environ Sci Technol 50:11895–11902. https://doi.org/10.1021/acs.est.6b03134
Xu X, Wang S, Li C et al (2023) Quorum sensing bacteria in microplastics epiphytic biofilms and their biological characteristics which potentially impact marine ecosystem. Ecotoxicol Environ Saf 264:115444. https://doi.org/10.1016/j.ecoenv.2023.115444
Xue Z, Seo Y (2013) Impact of chlorine disinfection on redistribution of cell clusters from biofilms. Environ Sci Technol 47:1365–1372. https://doi.org/10.1021/es304113e
Yan H, Liu C, Yu W et al (2023) The aggregate distribution of Pseudomonas aeruginosa on biochar facilitate quorum sensing and biofilm formation. Sci Total Environ 856:159034. https://doi.org/10.1016/j.scitotenv.2022.159034
Yao Y, Liu Z, Kin K et al (2022) Cross-regional scale pollution of freshwater biofilms unveiled by antibiotic resistance genes. Sci Total Environ 818:151835. https://doi.org/10.1016/j.scitotenv.2021.151835
Zammit G (2019) Phototrophic biofilm communities and adaptation to growth on ancient archaeological surfaces. Ann Microbiol 69:1047–1058. https://doi.org/10.1007/s13213-019-01471-w
Zeng DN, Fan ZY, Chi L et al (2013) Analysis of the bacterial communities associated with different drinking water treatment processes. World J Microbiol Biotechnol 29:1573–1584. https://doi.org/10.1007/s11274-013-1321-5
Zhang Y, Wu Q, Forsythe S et al (2023) The cascade regulation of small RNA and quorum sensing system: focusing on biofilm formation of foodborne pathogens in food industry. Food Biosci 52:102472. https://doi.org/10.1016/j.fbio.2023.102472
Zhao H, Zhang T, Wang H et al (2022) Occurrence of fungal spores in drinking water: a review of pathogenicity, odor, chlorine resistance and control strategies. Sci Total Environ 853:158626. https://doi.org/10.1016/j.scitotenv.2022.158626
Zhou S, An W, Zhao K et al (2023) Protection of electroactive biofilms against hypersaline shock by quorum sensing. Water Res 233:119823. https://doi.org/10.1016/j.watres.2023.119823
Zhu Y, Wang H, Li X et al (2014) Characterization of biofilm and corrosion of cast iron pipes in drinking water distribution system with UV/Cl2 disinfection. Water Res 60:174–181. https://doi.org/10.1016/j.watres.2014.04.035
Zhu Z, Shan L, Li X et al (2020) Effects of interspecific interactions on biofilm formation potential and chlorine resistance: evaluation of dual-species biofilm observed in drinking water distribution systems. J Water Process Eng 38:101564. https://doi.org/10.1016/j.jwpe.2020.101564
Zhu Q, Qian D, Yuan M et al (2023) Revealing the roles of chemical communication in restoring the formation and electroactivity of electrogenic biofilm under electrical signaling disruption. Water Res 243:120421. https://doi.org/10.1016/j.watres.2023.120421
Zuo J, Shen Y, Wang H et al (2023) Effects of metformin on Streptococcus suis LuxS/AI-2 quorum sensing system and biofilm formation. Microb Pathog 181:106183. https://doi.org/10.1016/j.micpath.2023.106183
Acknowledgements
Prof. J. Cui acknowledges Science and Technology Innovation 2030 (2023ZD04062), the Youth Innovation Program of Chinese Academy of Agricultural Sciences (Y2023QC23), Young Elite Scientists Sponsorship Program by China Association for Science and Technology (2022QNRC001), Agricultural Science and Technology Innovation Program of Chinese Academy of Agricultural Sciences and China Agriculture Research System. Prof. M.Y. Choi acknowledges the Korea Basic Science Institute (National research Facilities and Equipment Center) grant funded by the Ministry of Education. (No. 2019R1A6C1010042, 2021R1A6C103A427). The authors Prof. M.Y. Choi and Dr. J. Theerthagiri acknowledges the financial support from National Research Foundation of Korea (NRF), (2022R1A2C2010686, 2022R1A4A3033528, 2021R1I1A1A01060380, 2019H1D3A1A01071209). The author, Prof. Soorathep Kheawhom acknowledges The Program Management Unit for Human Resources & Industrial Development, Research & Innovation (B41G670026).
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PE, PP, OPK, and MYC contributed to conceptualization, critical thinking and writing original draft. XG and JC contributed to discussion and review editing. ASK and PD contributed to data collection. JT, SK, and MYC contributed review, proofread and supervision. MYC declares that he is Editor of Environmental Chemistry Letters.
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Elumalai, P., Gao, X., Cui, J. et al. Biofilm formation, occurrence, microbial communication, impact and characterization methods in natural and anthropic systems: a review. Environ Chem Lett 22, 1297–1326 (2024). https://doi.org/10.1007/s10311-024-01715-5
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DOI: https://doi.org/10.1007/s10311-024-01715-5