Community-wide changes reflecting bacterial interspecific interactions in multispecies biofilms

References

• Amanatidou E, Matthews AC, Kuhlicke U, Neu TR, McEvoy JP, Raymond B. 2019. Biofilms facilitate cheating and social exploitation of β-lactam resistance in Escherichia coli. NPJ Biofilms Microbiomes. 5(1):36.
   PubMedGoogle Scholar
• Andersson S, Kuttuva Rajarao G, Land CJ, Dalhammar G. 2008. Biofilm formation and interactions of bacterial strains found in wastewater treatment systems. FEMS Microbiol Lett. 283(1):83–90.
   PubMed Web of Science ®Google Scholar
• B George A, Korolev KS. 2018. Chirality provides a direct fitness advantage and facilitates intermixing in cellular aggregates. PLoS Comput Biol. 14(12):e1006645.
   PubMed Web of Science ®Google Scholar
• Bao K, Bostanci N, Selevsek N, Thurnheer T, Belibasakis GN. 2015. Quantitative proteomics reveal distinct protein regulations caused by Aggregatibacter actinomycetemcomitans within subgingival biofilms. PLoS ONE. 10(3):e0119222.
   PubMed Web of Science ®Google Scholar
• Bao K, Bostanci N, Thurnheer T, Belibasakis GN. 2017. Proteomic shifts in multi-species oral biofilms caused by Anaeroglobus geminatus. Sci Rep. 7(1):4409.
   PubMedGoogle Scholar
• Bar-On YM, Phillips R, Milo R. 2018. The biomass distribution on Earth. Proc Natl Acad Sci USA. 115(25):6506–6511.
   PubMed Web of Science ®Google Scholar
• Billings N, Millan M, Caldara M, Rusconi R, Tarasova Y, Stocker R, Ribbeck K. 2013. The extracellular matrix component Psl provides fast-acting antibiotic defense in Pseudomonas aeruginosa biofilms. PLoS Pathog. 9(8):e1003526
   PubMed Web of Science ®Google Scholar
• Boyle KE, Heilmann S, van Ditmarsch D, Xavier JB. 2013. Exploiting social evolution in biofilms. Curr Opin Microbiol. 16(2):207–212.
   PubMed Web of Science ®Google Scholar
• Breugelmans P, Barken KB, Tolker-Nielsen T, Hofkens J, Dejonghe W, Springael D. 2008. Architecture and spatial organization in a triple-species bacterial biofilm synergistically degrading the phenylurea herbicide linuron. FEMS Microbiol Ecol. 64(2):271–282.
   PubMed Web of Science ®Google Scholar
• Burmolle M, et al. 2006. Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Applied Environ Microbiol. 72(6):3916–3923.
   PubMed Web of Science ®Google Scholar
• Burmølle M, Kjøller A, and Sørensen SJ. 2011. Biofilms in soil. In: J. Gliński, J. Horabik, and J. Lipiec, editors. Encyclopedia of agrophysics, Dordrecht: Springer. p. 70–75.
   Google Scholar
• Burmølle M, Ren D, Bjarnsholt T, Sørensen SJ. 2014. Interactions in multispecies biofilms: do they actually matter? Trends Microbiol. 22(2):84–91.
   PubMed Web of Science ®Google Scholar
• Burmølle M, Webb JS, Rao D, Hansen LH, Sørensen SJ, Kjelleberg S. 2006. Enhanced biofilm formation and increased resistance to antimicrobial agents and bacterial invasion are caused by synergistic interactions in multispecies biofilms. Appl Environ Microbiol. 72(6):3916–3923.
   PubMed Web of Science ®Google Scholar
• Carvalho D. 2018. C.C.C.R. Marine biofilms: a successful microbial strategy with economic implications. Front Mar Sci. 5:126.
   Web of Science ®Google Scholar
• Cheng Y, Yam JKH, Cai Z, Ding Y, Zhang L-H, Deng Y, Yang L. 2019. Population dynamics and transcriptomic responses of Pseudomonas aeruginosa in a complex laboratory microbial community. NPJ Biofilms Microbiomes. 5(1):1.
   PubMedGoogle Scholar
• Chorianopoulos NG, Giaouris ED, Skandamis PN, Haroutounian SA, Nychas G-JE. 2008. Disinfectant test against monoculture and mixed-culture biofilms composed of technological, spoilage and pathogenic bacteria: bactericidal effect of essential oil and hydrosol of Satureja thymbra and comparison with standard acid-base sanitizers. J Appl Microbiol. 104(6):1586–1596.
   PubMed Web of Science ®Google Scholar
• Chung YW, Gwak H-J, Moon S, Rho M, Ryu J-H. 2020. Functional dynamics of bacterial species in the mouse gut microbiome revealed by metagenomic and metatranscriptomic analyses. PLoS ONE. 15(1):e0227886.
   PubMed Web of Science ®Google Scholar
• Cruciata M, Gaglio R, Scatassa ML, Sala G, Cardamone C, Palmeri M, Moschetti G, La Mantia T, Settanni L. 2017. Formation and characterization of early bacterial biofilms on different wood typologies applied in dairy production. Appl Environ Microbiol. 84(4):e02107–17.
   Web of Science ®Google Scholar
• de Vos WM. 2015. Microbial biofilms and the human intestinal microbiome. Npj Biofilms Microbiomes. 1(1):3.
   Google Scholar
• Deng Y-J, Wang SY. 2016. Synergistic growth in bacteria depends on substrate complexity. J Microbiol. 54(1):23–30.
   PubMed Web of Science ®Google Scholar
• Didienne R, Defargues C, Callon C, Meylheuc T, Hulin S, Montel M-C. 2012. Characteristics of microbial biofilm on wooden vats ('gerles') in PDO Salers cheese. Int J Food Microbiol. 156(2):91–101.
   PubMed Web of Science ®Google Scholar
• Dieltjens L, Appermans K, Lissens M, Lories B, Kim W, Van der Eycken EV, Foster KR, Steenackers HP. 2020. Inhibiting bacterial cooperation is an evolutionarily robust anti-biofilm strategy. Nat Commun. 11(1):107.
   PubMed Web of Science ®Google Scholar
• Donlan RM. 2002. Biofilms: microbial life on surfaces. Emerg Infect Dis. 8(9):881–890.
   PubMed Web of Science ®Google Scholar
• Edlund A, Yang Y, Yooseph S, He X, Shi W, McLean JS. 2018. Uncovering complex microbiome activities via metatranscriptomics during 24 hours of oral biofilm assembly and maturation. Microbiome. 6(1):217.
   PubMedGoogle Scholar
• Egland PG, Dû LD, Kolenbrander PE. 2001. Identification of independent Streptococcus gordonii SspA and SspB functions in coaggregation with Actinomyces naeslundii. Infect Immun. 69(12):7512–7516.
   PubMed Web of Science ®Google Scholar
• Elias S, Banin E. 2012. Multi-species biofilms: living with friendly neighbors. FEMS Microbiol Rev. 36(5):990–1004.
   PubMed Web of Science ®Google Scholar
• Estrela S, Brown SP. 2013. Metabolic and demographic feedbacks shape the emergent spatial structure and function of microbial communities. PLoS Comput Biol. 9(12):e1003398.
   PubMed Web of Science ®Google Scholar
• Evans CR, Kempes CP, Price-Whelan A, Dietrich LEP. 2020. Metabolic heterogeneity and cross-feeding in bacterial multicellular systems. Trends Microbiol. 28(9):732–743.
   PubMed Web of Science ®Google Scholar
• Fan Y, Huang X, Chen J, Han B. 2020. Formation of a mixed-species biofilm is a survival strategy for unculturable lactic acid bacteria and Saccharomyces cerevisiae in Daqu, a Chinese traditional fermentation starter. Front Microbiol. 11:138(
   PubMed Web of Science ®Google Scholar
• Fiegna F, Yu Y-TN, Kadam SV, Velicer GJ. 2006. Evolution of an obligate social cheater to a superior cooperator. Nature. 441(7091):310–314.
   PubMed Web of Science ®Google Scholar
• Flemming H-C, Wingender J, Szewzyk U, Steinberg P, Rice SA, Kjelleberg S. 2016. Biofilms: an emergent form of bacterial life. Nat Rev Microbiol. 14(9):563–575.
   PubMed Web of Science ®Google Scholar
• Flemming H-C, Wuertz S. 2019. Bacteria and archaea on Earth and their abundance in biofilms. Nat Rev Microbiol. 17(4):247–260.
   PubMed Web of Science ®Google Scholar
• Foster JS, Kolenbrander PE. 2004. Development of a multispecies oral bacterial community in a saliva-conditioned flow cell. Appl Environ Microbiol. 70(7):4340–4348.
   PubMed Web of Science ®Google Scholar
• Frias-Lopez J, Duran-Pinedo A. 2012. Effect of periodontal pathogens on the metatranscriptome of a healthy multispecies biofilm model. J Bacteriol. 194(8):2082–2095.
   PubMed Web of Science ®Google Scholar
• Guillonneau R, et al. 2018. Multispecies biofilm development of marine bacteria implies complex relationships through competition and synergy and modification of matrix components. Front Microbiol. 9:1960.
   PubMed Web of Science ®Google Scholar
• Hansen LBS, Ren D, Burmølle M, Sørensen SJ. 2017. Distinct gene expression profile of Xanthomonas retroflexus engaged in synergistic multispecies biofilm formation. Isme J. 11(1):300–303.
   PubMed Web of Science ®Google Scholar
• Hartmann R, Singh PK, Pearce P, Mok R, Song B, Díaz-Pascual F, Dunkel J, Drescher K. 2019. Emergence of three-dimensional order and structure in growing biofilms. Nat Phys. 15(3):251–256.
   PubMed Web of Science ®Google Scholar
• Hendrickson EL, Wang T, Dickinson BC, Whitmore SE, Wright CJ, Lamont RJ, Hackett M. 2012. Proteomics of Streptococcus gordonii within a model developing oral microbial community. BMC Microbiol. 12(1):211
   PubMedGoogle Scholar
• Henson MA, Phalak P. 2017. Byproduct cross feeding and community stability in an in silico biofilm model of the gut microbiome. Processes. 5(4):13.
   Google Scholar
• Herschend J, Damholt ZBV, Marquard AM, Svensson B, Sørensen SJ, Hägglund P, Burmølle M. 2017. A meta-proteomics approach to study the interspecies interactions affecting microbial biofilm development in a model community. Sci Rep. 7(1):16483.
   PubMedGoogle Scholar
• Hibbing ME, Fuqua C, Parsek MR, Peterson SB. 2010. Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol. 8(1):15–25.
   PubMed Web of Science ®Google Scholar
• Irie Y, Roberts AEL, Kragh KN, Gordon VD, Hutchison J, Allen RJ, Melaugh G, Bjarnsholt T, West SA, Diggle SP, et al. 2017. The Pseudomonas aeruginosa PSL polysaccharide is a social but noncheatable trait in biofilms. mBio. 8(3):e00374–e00317.
   PubMed Web of Science ®Google Scholar
• Jayathilake PG, Jana S, Rushton S, Swailes D, Bridgens B, Curtis T, Chen J. 2017. Extracellular polymeric substance production and aggregated bacteria colonization influence the competition of microbes in biofilms. Front Microbiol. 8:1865.
   PubMed Web of Science ®Google Scholar
• Kaplan A, Kaplan CW, He X, McHardy I, Shi W, Lux R. 2014. Characterization of aid1, a novel gene involved in Fusobacterium nucleatum interspecies interactions. Microb Ecol. 68(2):379–387.
   PubMed Web of Science ®Google Scholar
• Karygianni L, Ren Z, Koo H, Thurnheer T. 2020. Biofilm matrixome: Extracellular components in structured microbial communities. Trends Microbiol. 28(8):668–681.
   PubMed Web of Science ®Google Scholar
• Kelvin Lee KW, Hoong Yam JK, Mukherjee M, Periasamy S, Steinberg PD, Kjelleberg S, Rice SA. 2016. Interspecific diversity reduces and functionally substitutes for intraspecific variation in biofilm communities. Isme J. 10(4):846–857.
   PubMed Web of Science ®Google Scholar
• Keshvardoust P, Huron VAA, Clemson M, Constancias F, Barraud N, Rice SA. 2019. Biofilm formation inhibition and dispersal of multi-species communities containing ammonia-oxidising bacteria. NPJ Biofilms Microbiomes. 5(1):22.
   PubMedGoogle Scholar
• Khatoon Z, McTiernan CD, Suuronen EJ, Mah T-F, Alarcon EI. 2018. Bacterial biofilm formation on implantable devices and approaches to its treatment and prevention. Heliyon. 4(12):e01067.
   PubMed Web of Science ®Google Scholar
• Klein MI, Xiao J, Lu B, Delahunty CM, Yates JR, Koo H. 2012. Streptococcus mutans protein synthesis during mixed-species biofilm development by high-throughput quantitative proteomics. PLoS ONE. 7(9):e45795.
   PubMed Web of Science ®Google Scholar
• Kleiner M, Dong X, Hinzke T, Wippler J, Thorson E, Mayer B, Strous M. 2018. Metaproteomics method to determine carbon sources and assimilation pathways of species in microbial communities. Proc Natl Acad Sci USA. 115(24):E5576–E5584.
   PubMed Web of Science ®Google Scholar
• Kleiner M, Thorson E, Sharp CE, Dong X, Liu D, Li C, Strous M. 2017. Assessing species biomass contributions in microbial communities via metaproteomics. Nat Commun. 8(1):1558
   PubMed Web of Science ®Google Scholar
• Kolenbrander PE, Andersen RN, Blehert DS, Egland PG, Foster JS, Palmer RJ. 2002. Communication among oral bacteria. Microbiol Mol Biol Rev. 66(3):486–505, table of contents. +.
   PubMed Web of Science ®Google Scholar
• Kolenbrander PE, Palmer RJ, Periasamy S, Jakubovics NS. 2010. Oral multispecies biofilm development and the key role of cell-cell distance. Nat Rev Microbiol. 8(7):471–480.
   PubMed Web of Science ®Google Scholar
• Kolenbrander PE. 2000. Oral microbial communities: biofilms, interactions, and genetic systems. Annu Rev Microbiol. 54:413–437.
   PubMed Web of Science ®Google Scholar
• Kreft JU. 2004. Biofilms promote altruism. Microbiology (Reading)). 150(Pt 8):2751–2760.
   PubMedGoogle Scholar
• Kuboniwa M, Tribble GD, James CE, Kilic AO, Tao L, Herzberg MC, Shizukuishi S, Lamont RJ. 2006. Streptococcus gordonii utilizes several distinct gene functions to recruit Porphyromonas gingivalis into a mixed community. Mol Microbiol. 60(1):121–139.
   PubMed Web of Science ®Google Scholar
• Kuchina A. 2020. Microbial single-cell RNA sequencing by split-pool barcoding. Science. 371: eaba5257.
   PubMedGoogle Scholar
• Laganenka L, Sourjik V. 2017. Autoinducer 2-dependent Escherichia coli biofilm formation is enhanced in a dual-species coculture. Appl Environ Microbiol. 84(5):e02638–17.
   Web of Science ®Google Scholar
• Lamont RJ, El-Sabaeny A, Park Y, Cook GS, Costerton JW, Demuth DR. 2002. Role of the Streptococcus gordonii SspB protein in the development of Porphyromonas gingivalis biofilms on streptococcal substrates. Microbiology (Reading)). 148(Pt 6):1627–1636.
   PubMedGoogle Scholar
• Lapointe C, Deschênes L, Ells TC, Bisaillon Y, Savard T. 2019. Interactions between spoilage bacteria in tri-species biofilms developed under simulated meat processing conditions. Food Microbiol. 82:515–522.
   PubMed Web of Science ®Google Scholar
• Lee KWK, Periasamy S, Mukherjee M, Xie C, Kjelleberg S, Rice SA. 2014. Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm. Isme J. 8(4):894–907.
   PubMed Web of Science ®Google Scholar
• Leriche V, Briandet R, Carpentier B. 2003. Ecology of mixed biofilms subjected daily to a chlorinated alkaline solution: spatial distribution of bacterial species suggests a protective effect of one species to another. Environ Microbiol. 5(1):64–71.
   PubMed Web of Science ®Google Scholar
• Lima BP, Shi W, Lux R. 2017. Identification and characterization of a novel Fusobacterium nucleatum adhesin involved in physical interaction and biofilm formation with Streptococcus gordonii. MicrobiologyOpen. 6(3):e00444.
   Web of Science ®Google Scholar
• Liu NT, Bauchan GR, Francoeur CB, Shelton DR, Lo YM, Nou X. 2016. Ralstonia insidiosa serves as bridges in biofilm formation by foodborne pathogens Listeria monocytogenes, Salmonella enterica, and Enterohemorrhagic Escherichia coli. Food Control. 65:14–20.
   Web of Science ®Google Scholar
• Liu W, Jacquiod S, Brejnrod A, Russel J, Burmølle M, Sørensen SJ. 2019. Deciphering links between bacterial interactions and spatial organization in multispecies biofilms. Isme J. 13(12):3054–3066.
   PubMed Web of Science ®Google Scholar
• Liu W, Russel J, Røder HL, Madsen JS, Burmølle M, Sørensen SJ. 2017. Low-abundant species facilitates specific spatial organization that promotes multispecies biofilm formation. Environ Microbiol. 19(7):2893–2905.
   PubMed Web of Science ®Google Scholar
• Lories B, Roberfroid S, Dieltjens L, De Coster D, Foster KR, Steenackers HP. 2020. Biofilm bacteria use stress responses to detect and respond to competitors. Curr Biol. 30(7):1231–1244.e4.
   PubMed Web of Science ®Google Scholar
• Luppens SBI, Kara D, Bandounas L, Jonker MJ, Wittink FRA, Bruning O, Breit TM, Ten Cate JM, Crielaard W. 2008. Effect of Veillonella parvula on the antimicrobial resistance and gene expression of Streptococcus mutans grown in a dual-species biofilm. Oral Microbiol Immunol. 23(3):183–189.
   PubMedGoogle Scholar
• Madsen JS, Burmølle M, Hansen LH, Sørensen SJ. 2012. The interconnection between biofilm formation and horizontal gene transfer. FEMS Immunol Med Microbiol. 65(2):183–195.
   PubMedGoogle Scholar
• Malic S, Hill KE, Playle R, Thomas DW, Williams DW. 2011. In vitro interaction of chronic wound bacteria in biofilms. J Wound Care. 20(12):569–577.
   PubMed Web of Science ®Google Scholar
• Mulet X, Moyá B, Juan C, Macià MD, Pérez JL, Blázquez J, Oliver A. 2011. Antagonistic interactions of Pseudomonas aeruginosa antibiotic resistance mechanisms in planktonic but not biofilm growth. Antimicrob Agents Chemother. 55(10):4560–4568.
   PubMed Web of Science ®Google Scholar
• Nadell CD, Bassler BL. 2011. A fitness trade-off between local competition and dispersal in Vibrio cholerae biofilms. Proc Natl Acad Sci USA. 108(34):14181–14185.
   PubMed Web of Science ®Google Scholar
• Nadell CD, Foster KR, Xavier JB. 2010. Emergence of spatial structure in cell groups and the evolution of cooperation. PLoS Comput Biol. 6(3):e1000716.
   PubMed Web of Science ®Google Scholar
• Nadell CD, Xavier JB, Foster KR. 2009. The sociobiology of biofilms. FEMS Microbiol Rev. 33(1):206–224.
   PubMed Web of Science ®Google Scholar
• Narisawa N, Haruta S, Arai H, Ishii M, Igarashi Y. 2008. Coexistence of antibiotic-producing and antibiotic-sensitive bacteria in biofilms is mediated by resistant bacteria. Appl Environ Microbiol. 74(12):3887–3894.
   PubMed Web of Science ®Google Scholar
• Nozhevnikova AN, Botchkova EA, Plakunov VK. 2015. Multi-species biofilms in ecology, medicine, and biotechnology. Microbiol. 84(6):731–750.
   Web of Science ®Google Scholar
• Oliveira NM, Oliveria NM, Martinez-Garcia E, Xavier J, Durham WM, Kolter R, Kim W, Foster KR. 2015. Biofilm formation as a response to ecological competition. PLoS Biol. 13(7):e1002191.
   PubMed Web of Science ®Google Scholar
• Orazi G, O’Toole GA. 2019. It takes a village": mechanisms underlying antimicrobial recalcitrance of polymicrobial biofilms. J Bacteriol. 202(1):e00530–e00519.
   PubMed Web of Science ®Google Scholar
• Oxaran V, Dittmann KK, Lee SHI, Chaul LT, Fernandes de Oliveira CA, Corassin CH, Alves VF, De Martinis ECP, Gram L. 2018. Behavior of foodborne pathogens Listeria monocytogenes and Staphylococcus aureus in mixed-species biofilms exposed to biocides. Appl Environ Microbiol. 84(24):e02038–e02018.
   PubMed Web of Science ®Google Scholar
• Özkaya Ö, Xavier KB, Dionisio F, Balbontín R. 2017. Maintenance of microbial cooperation mediated by public goods in single- and multiple-trait scenarios. J Bacteriol. 199(22):e00297–e00217.
   Web of Science ®Google Scholar
• Parijs I, Steenackers HP. 2018. Competitive inter-species interactions underlie the increased antimicrobial tolerance in multispecies brewery biofilms. ISME J. 12(8):2061–2075.
   PubMed Web of Science ®Google Scholar
• Park J, Shokeen B, Haake SK, Lux R. 2016. Characterization of Fusobacterium nucleatum ATCC 23726 adhesins involved in strain-specific attachment to Porphyromonas gingivalis. Int J Oral Sci. 8(3):138–144.
   Web of Science ®Google Scholar
• Penesyan A, Nagy SS, Kjelleberg S, Gillings MR, Paulsen IT. 2019. Rapid microevolution of biofilm cells in response to antibiotics. NPJ Biofilms Microbiomes. 5(1):34
   PubMedGoogle Scholar
• Periasamy S, Chalmers NI, Du-Thumm L, Kolenbrander PE. 2009. Fusobacterium nucleatum ATCC 10953 requires Actinomyces naeslundii ATCC 43146 for growth on saliva in a three-species community that includes Streptococcus oralis 34. Appl Environ Microbiol. 75(10):3250–3257.
   PubMed Web of Science ®Google Scholar
• Periasamy S, et al. 2015. Pseudomonas aeruginosa PAO1 exopolysaccharides are important for mixed species biofilm community development and stress tolerance. Front Microbiol. 6:851–851.
   PubMed Web of Science ®Google Scholar
• Periasamy S, Kolenbrander PE. 2010. Central role of the early colonizer Veillonella sp. in establishing multispecies biofilm communities with initial, middle, and late colonizers of enamel. J Bacteriol. 192(12):2965–2972.
   PubMed Web of Science ®Google Scholar
• Piccardi P, Vessman B, Mitri S. 2019. Toxicity drives facilitation between 4 bacterial species. Proc Natl Acad Sci U S A. 116(32):15979–15984.
   PubMed Web of Science ®Google Scholar
• Popat R, Crusz SA, Messina M, Williams P, West SA, Diggle SP. 2012. Quorum-sensing and cheating in bacterial biofilms. Proc Biol Sci. 279(1748):4765–4771.
   PubMed Web of Science ®Google Scholar
• Raghupathi PK, et al. 2018. Synergistic interactions within a multispecies biofilm enhance individual species protection against grazing by a pelagic protozoan. Front Microbiol. 8:2649.
   PubMed Web of Science ®Google Scholar
• Rainey PB, Rainey K. 2003. Evolution of cooperation and conflict in experimental bacterial populations. Nature. 425(6953):72–74.
   PubMed Web of Science ®Google Scholar
• Rao D, Webb JS, Kjelleberg S. 2005. Competitive interactions in mixed-species biofilms containing the marine bacterium Pseudoalteromonas tunicata. Appl Environ Microbiol. 71(4):1729–1736.
   PubMed Web of Science ®Google Scholar
• Rath H, et al. 2017. Biofilm formation by the oral pioneer colonizer Streptococcus gordonii: an experimental and numerical study. FEMS Microbiol Eco. 93(3). DOI:10.1093/femsec/fix010.
   PubMed Web of Science ®Google Scholar
• Redanz S, Standar K, Podbielski A, Kreikemeyer B. 2011. A five-species transcriptome array for oral mixed-biofilm studies. Plos One. 6(12):e27827.
   PubMed Web of Science ®Google Scholar
• Ren D, Madsen JS, Sørensen SJ, Burmølle M. 2015. High prevalence of biofilm synergy among bacterial soil isolates in cocultures indicates bacterial interspecific cooperation. Isme J. 9(1):81–89.
   PubMed Web of Science ®Google Scholar
• Ren Y, Wang C, Chen Z, Allan E, van der Mei HC, Busscher HJ. 2018. Emergent heterogeneous microenvironments in biofilms: substratum surface heterogeneity and bacterial adhesion force-sensing. FEMS Microbiol Rev. 42(3):259–272.
   PubMed Web of Science ®Google Scholar
• Røder HL, Hansen LH, Sørensen SJ, Burmølle M. 2013. The impact of the conjugative IncP-1 plasmid pKJK5 on multispecies biofilm formation is dependent on the plasmid host. FEMS Microbiol Lett. 344(2):186–192.
   PubMed Web of Science ®Google Scholar
• Røder HL, Herschend J, Russel J, Andersen MF, Madsen JS, Sørensen SJ, Burmølle M. 2018. Enhanced bacterial mutualism through an evolved biofilm phenotype. Isme J. 12(11):2608–2618.
   PubMed Web of Science ®Google Scholar
• Røder HL, Olsen NMC, Whiteley M, Burmølle M. 2020. Unravelling interspecies interactions across heterogeneities in complex biofilm communities. Environ Microbiol. 22(1):5–16.
   PubMed Web of Science ®Google Scholar
• Røder HL, Raghupathi PK, Herschend J, Brejnrod A, Knøchel S, Sørensen SJ, Burmølle M. 2015. Interspecies interactions result in enhanced biofilm formation by co-cultures of bacteria isolated from a food processing environment. Food Microbiol. 51:18–24.
   PubMed Web of Science ®Google Scholar
• Romero-Lastra P, Sánchez MC, Llama-Palacios A, Figuero E, Herrera D, Sanz M. 2019. Gene expression of Porphyromonas gingivalis ATCC 33277 when growing in an in vitro multispecies biofilm. Plos One. 14(8):e0221234.
   PubMed Web of Science ®Google Scholar
• Rossi E, Cimdins A, Lüthje P, Brauner A, Sjöling Å, Landini P, Römling U. 2018. "It's a gut feeling" - Escherichia coli biofilm formation in the gastrointestinal tract environment. Crit Rev Microbiol. 44(1):1–30.
   PubMed Web of Science ®Google Scholar
• Russel J, Røder HL, Madsen JS, Burmølle M, Sørensen SJ. 2017. Antagonism correlates with metabolic similarity in diverse bacteria. Proc Natl Acad Sci USA. 114(40):10684–10688.
   PubMed Web of Science ®Google Scholar
• Sadiq FA, Yan B, Zhao J, Zhang H, Chen W. 2020. Untargeted metabolomics reveals metabolic state of bifidobacterium bifidum in the biofilm and Planktonic States. LWT. 118:108772.
   Web of Science ®Google Scholar
• Sadiq FA, Flint S, Li YJun, Ou K, Yuan L, He GQ. 2017. Phenotypic and genetic heterogeneity within biofilms with particular emphasis on persistence and antimicrobial tolerance. Future Microbiol. 12:1087–1107.
   PubMed Web of Science ®Google Scholar
• Sadiq FA, Flint S, Yuan L, Li Y, Liu TJie, He G. 2017. Propensity for biofilm formation by aerobic mesophilic and thermophilic spore forming bacteria isolated from Chinese milk powders. Int J Food Microbiol. 262:89–98.
   PubMed Web of Science ®Google Scholar
• Salgar-Chaparro SJ, Lepkova K, Pojtanabuntoeng T, Darwin A, Machuca LL. 2020. Nutrient level determines biofilm characteristics and subsequent impact on microbial corrosion and biocide effectiveness. Appl Environ Microbiol. 86(7):e02885–19.
   PubMed Web of Science ®Google Scholar
• Schink B. 1997. Energetics of syntrophic cooperation in methanogenic degradation. Microbiol Mol Biol Rev. 61(2):262–280.
   PubMed Web of Science ®Google Scholar
• Schluter J, Nadell CD, Bassler BL, Foster KR. 2015. Adhesion as a weapon in microbial competition. Isme J. 9(1):139–149.
   PubMed Web of Science ®Google Scholar
• Schwering M, Song J, Louie M, Turner RJ, Ceri H. 2013. Multi-species biofilms defined from drinking water microorganisms provide increased protection against chlorine disinfection. Biofouling. 29(8):917–928.
   PubMed Web of Science ®Google Scholar
• Smith WPJ, Davit Y, Osborne JM, Kim W, Foster KR, Pitt-Francis JM. 2017. Cell morphology drives spatial patterning in microbial communities. Proc Natl Acad Sci U S A. 114(3):E280–E286.
   PubMed Web of Science ®Google Scholar
• Tavernier S, Crabbé A, Hacioglu M, Stuer L, Henry S, Rigole P, Dhondt I, Coenye T. 2017. Community composition determines activity of antibiotics against multispecies biofilms. Antimicrob Agents Chemother. 61(9):e00302–e00317.
   PubMed Web of Science ®Google Scholar
• Tavernier S, Sass A, De Bruyne M, Baeke F, De Rycke R, Crabbé A, Vandecandelaere I, Van Nieuwerburgh F, Coenye T. 2018. Decreased susceptibility of Streptococcus anginosus to vancomycin in a multispecies biofilm is due to increased thickness of the cell wall. J Antimicrob Chemother. 73(9):2323–2330.
   PubMed Web of Science ®Google Scholar
• Thompson AF, English EL, Nock AM, Willsey GG, Eckstrom K, Cairns B, Bavelock M, Tighe SW, Foote A, Shulman H, et al. 2020. Characterizing species interactions that contribute to biofilm formation in a multispecies model of a potable water bacterial community. Microbiology (Reading)). 166(1):34–43.,
   PubMed Web of Science ®Google Scholar
• Tsuneda S, Park S, Hayashi H, Jung J, Hirata A. 2001. Enhancement of nitrifying biofilm formation using selected EPS produced by heterotrophic bacteria. Water Sci Technol. 43(6):197–204.
   PubMed Web of Science ®Google Scholar
• Vandecandelaere I, Van Nieuwerburgh F, Deforce D, Coenye T. 2017. Metabolic activity, urease production, antibiotic resistance and virulence in dual species biofilms of Staphylococcus epidermidis and Staphylococcus aureus. PLOS One. 12(3):e0172700
   PubMed Web of Science ®Google Scholar
• Varposhti M, Entezari F, Feizabadi MM. 2014. Synergistic interactions in mixed-species biofilms of pathogenic bacteria from the respiratory tract. Rev Soc Bras Med Trop. 47(5):649–652.
   PubMed Web of Science ®Google Scholar
• Wang L, Xie X, Qi M, Weir MD, Reynolds MA, Li C, Zhou C, Xu HHK. 2019. Effects of single species versus multispecies periodontal biofilms on the antibacterial efficacy of a novel bioactive Class-V nanocomposite. Dent Mater. 35(6):847–861.
   PubMed Web of Science ®Google Scholar
• Wang R, Kalchayanand N, Schmidt JW, Harhay DM. 2013. Mixed biofilm formation by shiga toxin-producing Escherichia coli and Salmonella enterica serovar Typhimurium enhanced bacterial resistance to sanitization due to extracellular polymeric substances. J Food Prot. 76(9):1513–1522.
   PubMed Web of Science ®Google Scholar
• West SA, Griffin AS, Gardner A, Diggle SP. 2006. Social evolution theory for microorganisms. Nat Rev Microbiol. 4(8):597–607.
   PubMed Web of Science ®Google Scholar
• Wexler AG, Bao Y, Whitney JC, Bobay L-M, Xavier JB, Schofield WB, Barry NA, Russell AB, Tran BQ, Goo YA, et al. 2016. Human symbionts inject and neutralize antibacterial toxins to persist in the gut. Proc Natl Acad Sci USA. 113(13):3639–3644.,
   PubMed Web of Science ®Google Scholar
• Wiedenbeck J, Cohan FM. 2011. Origins of bacterial diversity through horizontal genetic transfer and adaptation to new ecological niches. FEMS Microbiol Rev. 35(5):957–976.
   PubMed Web of Science ®Google Scholar
• Xavier JB, Foster KR. 2007. Cooperation and conflict in microbial biofilms. Proc Natl Acad Sci USA. 104(3):876–881.
   PubMed Web of Science ®Google Scholar
• Yannarell SM, Grandchamp GM, Chen S-Y, Daniels KE, Shank EA. 2019. A dual-species biofilm with emergent mechanical and protective properties. J Bacteriol. 201(18). DOI:10.1128/JB.00670-18.
   PubMed Web of Science ®Google Scholar
• Zhou Y, et al. 2019., Short-time antibacterial effects of dimethylaminododecyl methacrylate on oral multispecies biofilm in vitro. BioMed Res Inter. 2019:6393470.
   PubMed Web of Science ®Google Scholar
• Zottola EA, Sasahara KC. 1994. Microbial biofilms in the food processing industry—Should they be a concern? Int J Food Microbiol. 23(2):125–148.
   PubMed Web of Science ®Google Scholar
• Zupančič J, Raghupathi PK, Houf K, Burmølle M, Sørensen SJ, Gunde-Cimerman N. 2018. Synergistic interactions in microbial biofilms facilitate the establishment of opportunistic pathogenic fungi in household dishwashers. Front Microbiol. 9:21.
   PubMed Web of Science ®Google Scholar