Abstract
Multi-species bacterial and fungal communities of microbial aggregates, commonly known as biofilms, are associated with difficult-to-treat, chronic infections. These infection states are typically characterized by interactions between multiple biofilm-forming pathogens, as well as interactions of pathogens with the host microenvironment. Together, this dynamic interplay affects the progression and therapeutic outcome of the multi-species biofilm infection state, and underscores the importance of studying multi-species biofilms in the context of the complex host microenvironment. In this chapter, we review the multi-species status of important chronic infection states, including non-healing wounds, lung infections, oral and dental infections, suppurative otitis media, urinary tract infections, and medical device-associated infections. Further, we discuss the role of the host microenvironment in multi-species biofilm infections, with examples highlighting the roles of host factors in the formation, establishment, progression and outcome of these infections. This includes host niche sites, chemical and nutrient factors, immune factors, and biophysical and biomechanical cues. Next, we discuss in vitro laboratory approaches to study multi-species biofilm infections under conditions that closely recapitulate the clinical biofilm infection state. Using the case study of in vitro wound fluid models, we outline the incorporation and refinement of relevant host factors in the development of minimalist wound fluid models, and their applications to study multi-species biofilms in conditions that mimic the wound microenvironment. Finally, we suggest a “bottom-up” approach that can be used to develop in vitro milieu models for a range of infection states. While not all inclusive of the complex infection microenvironment, minimalist in vitro milieu models are a step forward from reductionist laboratory approaches, and could provide host-relevant insights into laboratory biofilm studies.
This is a preview of subscription content, log in via an institution to check access.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abdallah M, Benoliel C, Drider D et al (2014) Biofilm formation and persistence on abiotic surfaces in the context of food and medical environments. Arch Microbiol 196:453–472. https://doi.org/10.1007/S00203-014-0983-1/TABLES/1
Åberg CH, Kelk P, Johansson A (2015) Aggregatibacter actinomycetemcomitans: virulence of its leukotoxin and association with aggressive periodontitis. Virulence 6:188. https://doi.org/10.4161/21505594.2014.982428
Achterberg V, Meyer-Ingold W (2016) Hydroactive dressings and serum proteins: an in vitro study. J Wound Care 5:79–82. https://doi.org/10.12968/JOWC.1996.5.2.79
Aggarwal S, Poppele EH, Hozalski RM (2010) Development and testing of a novel microcantilever technique for measuring the cohesive strength of intact biofilms. Biotechnol Bioeng 105:924–934. https://doi.org/10.1002/BIT.22605
Akyıldız İ, Take G, Uygur K et al (2013) Bacterial biofilm formation in the middle-ear mucosa of chronic otitis media patients. Indian J Otolaryngol Head Neck Surg 65:557. https://doi.org/10.1007/S12070-012-0513-X
Alves PM, Al-Badi E, Withycombe C et al (2018) Interaction between Staphylococcus aureus and Pseudomonas aeruginosa is beneficial for colonisation and pathogenicity in a mixed biofilm. Pathog Dis 76:3. https://doi.org/10.1093/FEMSPD/FTY003
Amalaradjou MAR, Venkitanarayanan K (2013) Role of bacterial biofilms in catheter-associated urinary tract infections (CAUTI) and strategies for their control. Recent Adv Field Urin Tract Infect 10:1–32. https://doi.org/10.5772/55200
Armbruster CE, Smith SN, Yep A, Mobley HLT (2014) Increased incidence of urolithiasis and bacteremia during Proteus mirabilis and Providencia stuartii coinfection due to synergistic induction of urease activity. J Infect Dis 209:1524–1532. https://doi.org/10.1093/INFDIS/JIT663
Azevedo AS, Almeida C, Melo LF, Azevedo NF (2016) Impact of polymicrobial biofilms in catheter-associated urinary tract infections. Crit Rev Microbiol 43:423–439. https://doi.org/10.1080/1040841X.2016.1240656
Banin E, Vasil ML, Greenberg EP (2005) Iron and Pseudomonas aeruginosa biofilm formation. Proc Natl Acad Sci U S A 102:11076–11081. https://doi.org/10.1073/PNAS.0504266102
Barnes LA, Marshall CD, Leavitt T et al (2018) Mechanical forces in cutaneous wound healing: emerging therapies to minimize scar formation. Adv Wound Care 7:47–56. https://doi.org/10.1089/WOUND.2016.0709
Barraud N, Hassett DJ, Hwang SH et al (2006) Involvement of nitric oxide in biofilm dispersal of Pseudomonas aeruginosa. J Bacteriol 188:7344. https://doi.org/10.1128/JB.00779-06
Barraud N, Schleheck D, Klebensberger J et al (2009) Nitric oxide signaling in Pseudomonas aeruginosa biofilms mediates phosphodiesterase activity, decreased cyclic di-GMP levels, and enhanced dispersal. J Bacteriol 191:7333–7342. https://doi.org/10.1128/JB.00975-09/SUPPL_FILE/SUPPLEMENTAL_MATERIAL.PDF
Beebout CJ, Eberly AR, Werby SH et al (2019) Respiratory heterogeneity shapes biofilm formation and host colonization in uropathogenic Escherichia coli. mBio 10:e02400–e02418. https://doi.org/10.1128/MBIO.02400-18/SUPPL_FILE/MBIO.02400-18-SF009.TIF
Besser M, Dietrich M, Weber L et al (2020) Efficacy of antiseptics in a novel 3-dimensional human plasma biofilm model (hpBIOM). Sci Rep 101(10):1–9. https://doi.org/10.1038/s41598-020-61728-2
Bjarnsholt T, Kirketerp-Møller K, Jensen PØ et al (2008) Why chronic wounds will not heal: a novel hypothesis. Wound Repair Regen 16:2–10. https://doi.org/10.1111/J.1524-475X.2007.00283.X
Bjarnsholt T, Jensen PØ, Fiandaca MJ et al (2009) Pseudomonas aeruginosa biofilms in the respiratory tract of cystic fibrosis patients. Pediatr Pulmonol 44:547–558. https://doi.org/10.1002/PPUL.21011
Bowen WH, Koo H (2011) Biology of Streptococcus mutans-derived glucosyltransferases: role in extracellular matrix formation of cariogenic biofilms. Caries Res 45:69–86. https://doi.org/10.1159/000324598
Bowler PG, Duerden BI, Armstrong DG (2001) Wound microbiology and associated approaches to wound management. Clin Microbiol Rev 14:244–269. https://doi.org/10.1128/CMR.14.2.244-269.2001/ASSET/77FFDFF5-5FC0-491F-9435-58A827F4A4FF/ASSETS/GRAPHIC/CM0210012001.JPEG
Bowler PG, Jones SA, Walker M, Parsons D (2004) Microbicidal properties of a silver-containing Hydrofiber® dressing against a variety of burn wound pathogens. J Burn Care Rehabil 25:192–196. https://doi.org/10.1097/01.BCR.0000112331.72232.1B
Bradford C, Freeman R, Percival SL (2009) In vitro study of sustained antimicrobial activity of a new silver alginate dressing. J Am Col Certif Wound Spec 1:117. https://doi.org/10.1016/J.JCWS.2009.09.001
Bradshaw DJ, McKee AS, Marsh PD (1989) Effects of carbohydrate pulses and pH on population shifts within oral microbial communities in vitro. J Dent Res 68:1298–1302. https://doi.org/10.1177/00220345890680090101
Burkitt R, Sharp D (2017) Submicromolar quantification of pyocyanin in complex biological fluids using pad-printed carbon electrodes. Electrochem Commun 78:43–46. https://doi.org/10.1016/J.ELECOM.2017.03.021
Camus L, Briaud P, Vandenesch F, Moreau K (2021) How bacterial adaptation to cystic fibrosis environment shapes interactions between Pseudomonas aeruginosa and Staphylococcus aureus. Front Microbiol 12:411. https://doi.org/10.3389/FMICB.2021.617784/BIBTEX
Caverly LJ, LiPuma JJ (2018) Good cop, bad cop: anaerobes in cystic fibrosis airways. Eur Respir J 52:1. https://doi.org/10.1183/13993003.01146-2018
Cendra M d M, Blanco-Cabra N, Pedraz L, Torrents E (2019) Optimal environmental and culture conditions allow the in vitro coexistence of Pseudomonas aeruginosa and Staphylococcus aureus in stable biofilms. Sci Rep 91(9):1–17. https://doi.org/10.1038/s41598-019-52726-0
Cerqueira L, Oliveira JA, Nicolau A et al (2013) Biofilm formation with mixed cultures of Pseudomonas aeruginosa/Escherichia coli on silicone using artificial urine to mimic urinary catheters. Biofouling 29:829–840. https://doi.org/10.1080/08927014.2013.807913
Chew SY, Ho KL, Cheah YK et al (2019) Physiologically relevant alternative carbon sources modulate biofilm formation, cell wall architecture, and the stress and antifungal resistance of candida glabrata. Int J Mol Sci 20:3172. https://doi.org/10.3390/IJMS20133172
Chi AC, Day TA, Neville BW (2015) Oral cavity and oropharyngeal squamous cell carcinoma—an update. CA Cancer J Clin 65:401–421. https://doi.org/10.3322/CAAC.21293
Chotirmall SH, McElvaney NG (2014) Fungi in the cystic fibrosis lung: bystanders or pathogens? Int J Biochem Cell Biol 52:161–173. https://doi.org/10.1016/J.BIOCEL.2014.03.001
Chua SL, Ding Y, Liu Y et al (2016) Reactive oxygen species drive evolution of pro-biofilm variants in pathogens by modulating cyclic-di-GMP levels. Open Biol 6:160162. https://doi.org/10.1098/RSOB.160162
Cohen TS, Parker D, Prince A (2015) Pseudomonas aeruginosa host immune evasion. In: Pseudomonas, New Asp Pseudomonas Biol, vol 7, pp 3–23. https://doi.org/10.1007/978-94-017-9555-5_1
Cole SJ, Hall CL, Schniederberend M et al (2018) Host suppression of quorum sensing during catheter-associated urinary tract infections. Nat Commun 91(9):1–8. https://doi.org/10.1038/s41467-018-06882-y
Coutinho HDM, Falcão-Silva VS, Gonçalves GF (2008) Pulmonary bacterial pathogens in cystic fibrosis patients and antibiotic therapy: a tool for the health workers. Int Arch Med 1:24. https://doi.org/10.1186/1755-7682-1-24
Coutinho CP, Dos Santos SC, Madeira A et al (2011) Long-term colonization of the cystic fibrosis lung by Burkholderia cepacia complex bacteria: epidemiology, clonal variation, and genome-wide expression alterations. Front Cell Infect Microbiol 1:12. https://doi.org/10.3389/FCIMB.2011.00012/BIBTEX
Cutting KF (2013) Wound exudate: composition and functions. Br J Community Nurs 8:S4–S9. https://doi.org/10.12968/BJCN.2003.8.SUP3.11577
De Cicco F, Porta A, Sansone F et al (2014) Nanospray technology for an in situ gelling nanoparticulate powder as a wound dressing. Int J Pharm 473:30–37. https://doi.org/10.1016/J.IJPHARM.2014.06.049
De Cicco F, Russo P, Reverchon E et al (2016) Prilling and supercritical drying: a successful duo to produce core-shell polysaccharide aerogel beads for wound healing. Carbohydr Polym 147:482–489. https://doi.org/10.1016/J.CARBPOL.2016.04.031
de Vor L, Rooijakkers SHM, van Strijp JAG (2020) Staphylococci evade the innate immune response by disarming neutrophils and forming biofilms. FEBS Lett 594:2556–2569. https://doi.org/10.1002/1873-3468.13767
Delaquis PJ, Caldwell DE, Lawrence JR, AR MC (1989) Detachment of Pseudomonas fluorescens from biofilms on glass surfaces in response to nutrient stress. Microb Ecol 183(18):199–210. https://doi.org/10.1007/BF02075808
Deo PN, Deshmukh R (2019) Oral microbiome: unveiling the fundamentals. J Oral Maxillofac Pathol 23:122. https://doi.org/10.4103/JOMFP.JOMFP_304_18
Di Giulio M, Di Lodovico S, Fontana A et al (2020) Graphene oxide affects Staphylococcus aureus and Pseudomonas aeruginosa dual species biofilm in Lubbock Chronic Wound Biofilm model. Sci Rep 101(10):1–9. https://doi.org/10.1038/s41598-020-75086-6
Donlan RM (2001a) Biofilm formation: a clinically relevant microbiological process. Clin Infect Dis 33:1387–1392. https://doi.org/10.1086/322972/2/33-8-1387-TBL002.GIF
Donlan RM (2001b) Biofilms and device-associated infections. Emerg Infect Dis 7:277–281. https://doi.org/10.3201/EID0702.010226
Donlan RM, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15(2):167–193
Eix EF, Nett JE (2020) How biofilm growth affects candida-host interactions. Front Microbiol 11:1437. https://doi.org/10.3389/FMICB.2020.01437/BIBTEX
Elias S, Banin E (2012) Multi-species biofilms: living with friendly neighbors. FEMS Microbiol Rev 36:990–1004. https://doi.org/10.1111/J.1574-6976.2012.00325.X
Enyedi B, Niethammer P (2015) Mechanisms of epithelial wound detection. Trends Cell Biol 25:398–407. https://doi.org/10.1016/J.TCB.2015.02.007
Falsetta ML, Klein MI, Colonne PM et al (2014) Symbiotic relationship between Streptococcus mutans and Candida albicans synergizes virulence of plaque biofilms in vivo. Infect Immun 82:1968. https://doi.org/10.1128/IAI.00087-14
Fang FC (2004) Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat Rev Microbiol 2:820–832. https://doi.org/10.1038/NRMICRO1004
Fazli M, Bjarnsholt T, Kirketerp-Møller K et al (2009) Nonrandom distribution of Pseudomonas aeruginosa and Staphylococcus aureus in chronic wounds. J Clin Microbiol 47:4084–4089. https://doi.org/10.1128/JCM.01395-09/ASSET/7CC82769-5586-4751-AFC6-D015F51521E2/ASSETS/GRAPHIC/ZJM0120993370004.JPEG
Fernandes A, Dias M (2013) The microbiological profiles of infected prosthetic implants with an emphasis on the organisms which form biofilms. J Clin Diagn Res 7:219. https://doi.org/10.7860/JCDR/2013/4533.2732
Flynn JM, Niccum D, Dunitz JM, Hunter RC (2016) Evidence and role for bacterial mucin degradation in cystic fibrosis airway disease. PLoS Pathog 12:e1005846. https://doi.org/10.1371/JOURNAL.PPAT.1005846
Ganesh K, Sinha M, Mathew-Steiner SS et al (2015) Chronic wound biofilm model. Adv Wound Care 4:382. https://doi.org/10.1089/WOUND.2014.0587
Gaston JR, Johnson AO, Bair KL et al (2021) Polymicrobial interactions in the urinary tract: is the enemy of my enemy my friend? Infect Immun 89:e00652–e00620. https://doi.org/10.1128/IAI.00652-20/FORMAT/EPUB
Gbejuade HO, Lovering AM, Webb JC (2015) The role of microbial biofilms in prosthetic joint infections. Acta Orthop 86:147–158. https://doi.org/10.3109/17453674.2014.966290
Ghannoum MA, Jurevic RJ, Mukherjee PK et al (2010) Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog 6:1000713. https://doi.org/10.1371/JOURNAL.PPAT.1000713
Ghimire N, Pettygrove BA, Pallister KB et al (2019) Direct microscopic observation of human neutrophil-staphylococcus aureus interaction in vitro suggests a potential mechanism for initiation of biofilm infection on an implanted medical device. Infect Immun 87:e00745–e00719. https://doi.org/10.1128/IAI.00745-19/SUPPL_FILE/IAI.00745-19-SM010.AVI
Gloag ES, Fabbri S, Wozniak DJ, Stoodley P (2020) Biofilm mechanics: implications in infection and survival. Biofilms 2:100017. https://doi.org/10.1016/J.BIOFLM.2019.100017
González JF, Hahn MM, Gunn JS (2018) Chronic biofilm-based infections: skewing of the immune response. Pathog Dis 76:23. https://doi.org/10.1093/FEMSPD/FTY023
Greener B, Hughes AA, Bannister NP, Douglass J (2013) Proteases and pH in chronic wounds. J Wound Care 14:59–61. https://doi.org/10.12968/JOWC.2005.14.2.26739
Griffen AL, Beall CJ, Campbell JH et al (2012) Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. ISME J 66(6):1176–1185. https://doi.org/10.1038/ismej.2011.191
Gunn JS, Bakaletz LO, Wozniak DJ (2016) What’s on the outside matters: the role of the extracellular polymeric substance of gram-negative biofilms in evading host immunity and as a target for therapeutic intervention. J Biol Chem 291:12538–12546. https://doi.org/10.1074/JBC.R115.707547/ATTACHMENT/8136047D-93E9-416A-9693-BA5B8CC8B4DD/MMC3.PDF
Hall-Stoodley L, Hu FZ, Gieseke A et al (2006) Direct detection of bacterial biofilms on the middle-ear mucosa of children with chronic otitis media. JAMA 296:202–211. https://doi.org/10.1001/JAMA.296.2.202
Harriott MM, Noverr MC (2010) Ability of Candida albicans mutants to induce Staphylococcus aureus vancomycin resistance during polymicrobial biofilm formation. Antimicrob Agents Chemother 54:3746–3755. https://doi.org/10.1128/AAC.00573-10/ASSET/E6F8ACBF-A1D3-41BA-AB92-13FD2A0B5A58/ASSETS/GRAPHIC/ZAC9991092280006.JPEG
Harriott MM, Noverr MC (2011) Importance of Candida-bacterial multi-species biofilms in disease. Trends Microbiol 19:557–563. https://doi.org/10.1016/J.TIM.2011.07.004
Herbert BA, Novince CM, Kirkwood KL (2016) Aggregatibacter actinomycetemcomitans, a potent immunoregulator of the periodontal host defense system and alveolar bone homeostasis. Mol Oral Microbiol 31:207–227. https://doi.org/10.1111/OMI.12119
Hoiby N, Bjarnsholt T, Givskov M et al (2010) Antibiotic resistance of bacterial biofilms. Int J Antimicrob Agents 35:322–332. https://doi.org/10.1016/J.IJANTIMICAG.2009.12.011
Holá V, Ruzicka F, Horka M (2010) Microbial diversity in biofilm infections of the urinary tract with the use of sonication techniques. FEMS Immunol Med Microbiol 59:525–528. https://doi.org/10.1111/J.1574-695X.2010.00703.X
Huang R, Li M, Gregory RL (2011) Bacterial interactions in dental biofilm. Virulence 2:435. https://doi.org/10.4161/VIRU.2.5.16140
Imamura Y, Chandra J, Mukherjee PK et al (2008) Fusarium and Candida albicans biofilms on soft contact lenses: model development, influence of lens type, and susceptibility to lens care solutions. Antimicrob Agents Chemother 52:171–182. https://doi.org/10.1128/AAC.00387-07/ASSET/16ACDDB8-B36E-47FA-B010-B109DF611FA5/ASSETS/GRAPHIC/ZAC0010870270006.JPEG
Jakobsen TH, Eickhardt SR, Gheorghe AG et al (2018) Implants induce a new niche for microbiomes. APMIS 126:685–692. https://doi.org/10.1111/APM.12862
James GA, Swogger E, Wolcott R et al (2008) Biofilms in chronic wounds. Wound Repair Regen 16:37–44. https://doi.org/10.1111/j.1524-475X.2007.00321.x
Jean-Pierre F, Vyas A, Hampton TH et al (2021) One versus many: multi-species communities and the cystic fibrosis airway. mBio 12:1–7. https://doi.org/10.1128/MBIO.00006-21/ASSET/EE5D1BC5-F184-4BFC-B1E2-FDAF5474A562/ASSETS/IMAGES/MEDIUM/MBIO.00006-21-F0002.GIF
Jefferson KK (2004) What drives bacteria to produce a biofilm? FEMS Microbiol Lett 236:163–173. https://doi.org/10.1111/J.1574-6968.2004.TB09643.X
Jensen LK, Johansen ASB, Jensen HE (2017a) Porcine models of biofilm infections with focus on pathomorphology. Front Microbiol 8:1961. https://doi.org/10.3389/FMICB.2017.01961/BIBTEX
Jensen P, Kolpen M, Kragh KN, Kühl M (2017b) Microenvironmental characteristics and physiology of biofilms in chronic infections of CF patients are strongly affected by the host immune response. APMIS 125:276–288. https://doi.org/10.1111/APM.12668
Jesaitis AJ, Franklin MJ, Berglund D et al (2003) Compromised host defense on Pseudomonas aeruginosa biofilms: characterization of neutrophil and biofilm interactions. J Immunol 171:4329–4339. https://doi.org/10.4049/JIMMUNOL.171.8.4329
Johani K, Malone M, Jensen S et al (2017) Microscopy visualisation confirms multi-species biofilms are ubiquitous in diabetic foot ulcers. Int Wound J 14:1160–1169. https://doi.org/10.1111/IWJ.12777
John M, Goldsworthy H, Burton S, Lappin-Scott H (2008) Gene expression of Pseudomonas aeruginosa and MRSA within a catheter-associated urinary tract infection biofilm model. Biosci Horizons Int J Student Res 1:28–37. https://doi.org/10.1093/BIOHORIZONS/HZN008
Jones KL, Bryan TW, Jinkins PA et al (1998) Superoxide released from neutrophils causes a reduction in nitric oxide gas. Am J Phys 275:L1120–L1126. https://doi.org/10.1152/AJPLUNG.1998.275.6.L1120
Kadam S, Nadkarni S, Lele J et al (2019) Bioengineered platforms for chronic wound infection studies: how can we make them more human-relevant? Front Bioeng Biotechnol 7:418. https://doi.org/10.3389/FBIOE.2019.00418/BIBTEX
Kadam S, Madhusoodhanan V, Dhekane R et al (2021) Milieu matters: an in vitro wound milieu to recapitulate key features of, and probe new insights into, mixed-species bacterial biofilms. Biofilms 3:100047. https://doi.org/10.1016/J.BIOFLM.2021.100047
Kalan L, Grice EA (2018) Fungi in the wound microbiome. Adv Wound Care 7:247–255. https://doi.org/10.1089/WOUND.2017.0756
Kalan L, Loesche M, Hodkinson BP et al (2016) Redefining the chronic-wound microbiome: fungal communities are prevalent, dynamic, and associated with delayed healing. MBio 7:e01058–e01016. https://doi.org/10.1128/MBIO.01058-16/SUPPL_FILE/MBO004162957SF6.PDF
Kang D, Kirienko NV (2018) Interdependence between iron acquisition and biofilm formation in Pseudomonas aeruginosa. J Microbiol 56:449. https://doi.org/10.1007/S12275-018-8114-3
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
Khatoon Z, McTiernan CD, Suuronen EJ et al (2018) Bacterial biofilm formation on implantable devices and approaches to its treatment and prevention. Heliyon 4:1067. https://doi.org/10.1016/J.HELIYON.2018.E01067
Kirchner S, Fothergill JL, Wright EA et al (2012) Use of artificial sputum medium to test antibiotic efficacy against Pseudomonas aeruginosa in conditions more relevant to the cystic fibrosis lung. J Vis Exp 64:1–8. https://doi.org/10.3791/3857
Klein MI, Hwang G, Santos PHS et al (2015) Streptococcus mutans-derived extracellular matrix in cariogenic oral biofilms. Front Cell Infect Microbiol 5:10. https://doi.org/10.3389/FCIMB.2015.00010/BIBTEX
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
Krishnaswamy VR, Mintz D, Sagi I (2017) Matrix metalloproteinases: the sculptors of chronic cutaneous wounds. Biochim Biophys Acta, Mol Cell Res 1864:2220–2227. https://doi.org/10.1016/J.BBAMCR.2017.08.003
Kumar B, Cardona ST (2016) Synthetic cystic fibrosis sputum medium regulates flagellar biosynthesis through the flhF gene in Burkholderia cenocepacia. Front Cell Infect Microbiol 6:65. https://doi.org/10.3389/FCIMB.2016.00065/BIBTEX
Kumar L, Cox CR, Sarkar SK (2019) Matrix metalloprotease-1 inhibits and disrupts Enterococcus faecalis biofilms. PLoS One 14:e0210218. https://doi.org/10.1371/JOURNAL.PONE.0210218
Labovitiadi O (2011) Antimicrobial wafers as a novel technology for infection control in chronic wounds. https://rgu-repository.worktribe.com/output/248162/antimicrobial-wafers-as-a-novel-technology-for-infection-control-in-chronic-wounds
Lamont RJ, Koo H, Hajishengallis G (2018) The oral microbiota: dynamic communities and host interactions. Nat Rev Microbiol 1612(16):745–759. https://doi.org/10.1038/s41579-018-0089-x
Lee SM, Donaldson GP, Mikulski Z et al (2013) Bacterial colonization factors control specificity and stability of the gut microbiota. Nature 501:426–429. https://doi.org/10.1038/NATURE12447
Lee KWK, Periasamy S, Mukherjee M et al (2014a) Biofilm development and enhanced stress resistance of a model, mixed-species community biofilm. ISME J 84(8):894–907. https://doi.org/10.1038/ismej.2013.194
Lee RJ, Chen B, Redding KM et al (2014b) Mouse nasal epithelial innate immune responses to Pseudomonas aeruginosa quorum-sensing molecules require taste signaling components. Innate Immun 20:606–617. https://doi.org/10.1177/1753425913503386
Leid JG (2009) Bacterial biofilms resist key host defenses. Microbe 4(2):66–70
Lemos JA, Palmer SR, Zeng L et al (2019) The biology of Streptococcus mutans. Microbiol Spectr 7:7. https://doi.org/10.1128/MICROBIOLSPEC.GPP3-0051-2018
Lesouhaitier O, Clamens T, Rosay T et al (2019) Host peptidic hormones affecting bacterial biofilm formation and virulence. J Innate Immun 11:227–241. https://doi.org/10.1159/000493926
Li X, Lu N, Brady HR, Packman AI (2016) Biomineralization strongly modulates the formation of Proteus mirabilis and Pseudomonas aeruginosa dual-species biofilms. FEMS Microbiol Ecol 92:fiw189. https://doi.org/10.1093/FEMSEC/FIW189
Lightly TJ, Phung RR, Sorensen JL, Cardona ST (2017) Synthetic cystic fibrosis sputum medium diminishes Burkholderia cenocepacia antifungal activity against aspergillus fumigatus independently of phenylacetic acid production. Can J Microbiol 63:427–438. https://doi.org/10.1139/CJM-2016-0705/SUPPL_FILE/CJM-2016-0705SUPPL.ZIP
Lopez MS, Tan IS, Yan D et al (2017) Host-derived fatty acids activate type VII secretion in Staphylococcus aureus. Proc Natl Acad Sci U S A 114:11223–11228. https://doi.org/10.1073/PNAS.1700627114/-/DCSUPPLEMENTAL
Lorè NI, Cigana C, De Fino I et al (2012) Cystic fibrosis-niche adaptation of Pseudomonas aeruginosa reduces virulence in multiple infection hosts. PLoS One 7:e35648. https://doi.org/10.1371/JOURNAL.PONE.0035648
Macleod SM, Stickler DJ (2007) Species interactions in mixed-community crystalline biofilms on urinary catheters. J Med Microbiol 56:1549–1557. https://doi.org/10.1099/JMM.0.47395-0/CITE/REFWORKS
Majumder MI, Ahmed T, Hossain D, Begum SA (2014) Bacteriology and antibiotic sensitivity patterns of urinary tract infections in a tertiary hospital in Bangladesh. Mymensingh Med J 23(1):99–104. https://pubmed.ncbi.nlm.nih.gov/24584381/
Malic S, Hill KE, Hayes A et al (2009) Detection and identification of specific bacteria in wound biofilms using peptide nucleic acid fluorescent in situ hybridization (PNA FISH). Microbiology 155:2603–2611. https://doi.org/10.1099/MIC.0.028712-0/CITE/REFWORKS
Malone M, Johani K, Jensen SO et al (2017) Effect of cadexomer iodine on the microbial load and diversity of chronic non-healing diabetic foot ulcers complicated by biofilm in vivo. J Antimicrob Chemother 72:2093–2101. https://doi.org/10.1093/JAC/DKX099
Manuela B, Milad K, Anna-Lena S et al (2017) Acute and chronic wound fluid inversely influence wound healing in an in-vitro 3D wound model. J Tissue Repair Regen 1:1–11. https://doi.org/10.14302/ISSN.2640-6403.JTRR-17-1818
Marsh PD, Devine DA (2011) How is the development of dental biofilms influenced by the host? J Clin Periodontol 38:28–35. https://doi.org/10.1111/J.1600-051X.2010.01673.X
Mathee K, Ciofu O, Sternberg C et al (1999) Mucoid conversion of Pseudomonas aeruginosa by hydrogen peroxide: a mechanism for virulence activation in the cystic fibrosis lung. Microbiology 145(Pt 6):1349–1357. https://doi.org/10.1099/13500872-145-6-1349
Mauch RM, Østrup Jensen P, Moser C et al (2017) Mechanisms of humoral immune response against Pseudomonas aeruginosa biofilm infection in cystic fibrosis. J Cyst Fibros 17:143–152. https://doi.org/10.1016/j.jcf.2017.08.012
McDermid AS, McKee AS, Marsh PD (1988) Effect of environmental pH on enzyme activity and growth of Bacteroides gingivalis W50. Infect Immun 56:1096. https://doi.org/10.1128/iai.56.5.1096-1100.1988
Mettraux GR, Gusberti FA, Graf H (1984) Oxygen tension (pO2) in untreated human periodontal pockets. J Periodontol 55:516–521. https://doi.org/10.1902/JOP.1984.55.9.516
Milne SD, Connolly P (2014) The influence of different dressings on the pH of the wound environment. J Wound Care 23:53–57. https://doi.org/10.12968/JOWC.2014.23.2.53
Mndlovu H, du Toit LC, Kumar P et al (2019) Development of a fluid-absorptive alginate-chitosan bioplatform for potential application as a wound dressing. Carbohydr Polym 222:114988. https://doi.org/10.1016/J.CARBPOL.2019.114988
Monaco JAL, Lawrence WT (2003) Acute wound healing: an overview. Clin Plast Surg 30:1–12. https://doi.org/10.1016/S0094-1298(02)00070-6
Montelongo-Jauregui D, Srinivasan A, Ramasubramanian AK, Lopez-Ribot JL (2016) An in vitro model for oral mixed biofilms of Candida albicans and Streptococcus gordonii in synthetic saliva. Front Microbiol 7:686. https://doi.org/10.3389/FMICB.2016.00686
Mortensen BL, Skaar EP (2012) Host–microbe interactions that shape the pathogenesis of Acinetobacter baumannii infection. Cell Microbiol 14:1336–1344. https://doi.org/10.1111/J.1462-5822.2012.01817.X
Moser C, Pedersen HT, Lerche CJ et al (2017) Biofilms and host response – helpful or harmful. APMIS 125:320–338. https://doi.org/10.1111/APM.12674
Narayanan G, Ormond BR, Gupta BS, Tonelli AE (2015) Efficient wound odor removal by β-cyclodextrin functionalized poly (ε-caprolactone) nanofibers. J Appl Polym Sci 132:45. https://doi.org/10.1002/APP.42782
Neelakantan P, Romero M, Vera J et al (2017) Biofilms in endodontics—current status and future directions. Int J Mol Sci 18:1748. https://doi.org/10.3390/IJMS18081748
Neve RL, Carrillo BD, Phelan VV (2021) Impact of artificial sputum medium formulation on pseudomonas aeruginosa secondary metabolite production. J Bacteriol 203:e00250. https://doi.org/10.1128/JB.00250-21/SUPPL_FILE/JB.00250-21-S0006.XLSX
Nguyen M, Sharma A, Wu W et al (2016) The fermentation product 2,3-butanediol alters P. aeruginosa clearance, cytokine response and the lung microbiome. ISME J 10:2978. https://doi.org/10.1038/ISMEJ.2016.76
O’Brien S, Fothergill JL (2017) The role of multispecies social interactions in shaping Pseudomonas aeruginosa pathogenicity in the cystic fibrosis lung. FEMS Microbiol Lett 364:128. https://doi.org/10.1093/FEMSLE/FNX128
O’Toole G, Kaplan HB, Kolter R (2000) Biofilm formation as microbial development. Annu Rev Microbiol 54:49–79. https://doi.org/10.1146/ANNUREV.MICRO.54.1.49
Oliveira F, Rohde H, Vilanova M, Cerca N (2021) The emerging role of iron acquisition in biofilm-associated infections. Trends Microbiol 29:772–775. https://doi.org/10.1016/J.TIM.2021.02.009
Omar A, Wright JB, Schultz G et al (2017) Microbial biofilms and chronic wounds. Microorganisms 5:95–99. https://doi.org/10.3390/MICROORGANISMS5010009
Ormerod LD, Ruoff KL, Meisler DM et al (1991) Infectious crystalline keratopathy. Role of nutritionally variant streptococci and other bacterial factors. Ophthalmology 98:159–169. https://doi.org/10.1016/S0161-6420(91)32321-2
Parreira P, Martins MCL (2021) The biophysics of bacterial infections: adhesion events in the light of force spectroscopy. Cell Surf 7:100048. https://doi.org/10.1016/J.TCSW.2021.100048
Peters BM, Ovchinnikova ES, Krom BP et al (2012) Staphylococcus aureus adherence to Candida albicans hyphae is mediated by the hyphal adhesin Als3p. Microbiology 158:2975. https://doi.org/10.1099/MIC.0.062109-0
Pettygrove BA, Kratofil RM, Alhede M et al (2021) Delayed neutrophil recruitment allows nascent Staphylococcus aureus biofilm formation and immune evasion. Biomaterials 275:120775. https://doi.org/10.1016/J.BIOMATERIALS.2021.120775
Poore TS, Hong G, Zemanick ET (2021) Fungal infection and inflammation in cystic fibrosis. Pathogens 10:618. https://doi.org/10.3390/PATHOGENS10050618
Qin Y, He Y, She Q et al (2019) Heterogeneity in respiratory electron transfer and adaptive iron utilization in a bacterial biofilm. Nat Commun 101(10):1–12. https://doi.org/10.1038/s41467-019-11681-0
Raad II, Hanna HA (2002) Intravascular catheter-related infections: new horizons and recent advances. Arch Intern Med 162:871–878. https://doi.org/10.1001/ARCHINTE.162.8.871
Raafat AI, El-Sawy NM, Badawy NA et al (2018) Radiation fabrication of xanthan-based wound dressing hydrogels embedded ZnO nanoparticles: in vitro evaluation. Int J Biol Macromol 118:1892–1902. https://doi.org/10.1016/J.IJBIOMAC.2018.07.031
Rajeev G, Xifre-Perez E, Prieto Simon B et al (2018) A label-free optical biosensor based on nanoporous anodic alumina for tumour necrosis factor-alpha detection in chronic wounds. Sensors Actuators B Chem 257:116–123. https://doi.org/10.1016/J.SNB.2017.10.156
Ramstedt M, Burmølle M (2022) Can multi-species biofilms defeat antimicrobial surfaces on medical devices? Curr Opin Biomed Eng 22:100370. https://doi.org/10.1016/J.COBME.2022.100370
Rao Y, Shang W, Yang Y et al (2020) Fighting mixed-species microbial biofilms with cold atmospheric plasma. Front Microbiol 11:1000. https://doi.org/10.3389/FMICB.2020.01000/BIBTEX
Riquelme SA, Ahn D, Prince A (2018) Pseudomonas aeruginosa and Klebsiella pneumoniae adaptation to innate immune clearance mechanisms in the lung. J Innate Immun 10:442–454. https://doi.org/10.1159/000487515
Rodesney CA, Roman B, Dhamani N et al (2017) Mechanosensing of shear by Pseudomonas aeruginosa leads to increased levels of the cyclic-di-GMP signal initiating biofilm development. Proc Natl Acad Sci U S A 114:5906–5911. https://doi.org/10.1073/PNAS.1703255114/SUPPL_FILE/PNAS.201703255SI.PDF
Roilides E, Simitsopoulou M, Katragkou A, Walsh TJ (2015) How biofilms evade host defenses. Microbiol Spectr 3:3. https://doi.org/10.1128/MICROBIOLSPEC.MB-0012-2014
Sabir N, Ikram A, Zaman G et al (2017) Bacterial biofilm-based catheter-associated urinary tract infections: causative pathogens and antibiotic resistance. Am J Infect Control 45:1101–1105. https://doi.org/10.1016/J.AJIC.2017.05.009
Said J, Dodoo CC, Walker M et al (2014) An in vitro test of the efficacy of silver-containing wound dressings against Staphylococcus aureus and Pseudomonas aeruginosa in simulated wound fluid. Int J Pharm 462:123–128. https://doi.org/10.1016/J.IJPHARM.2013.12.037
Sajjan U, Thanassoulis G, Cherapanov V et al (2001) Enhanced susceptibility to pulmonary infection with Burkholderia cepacia in Cftr(−/−) mice. Infect Immun 69:5138–5150. https://doi.org/10.1128/IAI.69.8.5138-5150.2001
Salgar-Chaparro SJ, Lepkova K, Pojtanabuntoeng T et al (2020) Nutrient level determines biofilm characteristics and subsequent impact on microbial corrosion and biocide effectiveness. Appl Environ Microbiol 86:e02885. https://doi.org/10.1128/AEM.02885-19/SUPPL_FILE/AEM.02885-19-S0001.PDF
Samaranayake L, Matsubara VH (2017) Normal oral flora and the oral ecosystem. Dent Clin 61:199–215. https://doi.org/10.1016/J.CDEN.2016.11.002
Sarigul N, Korkmaz F, Kurultak İ (2019) A new artificial urine protocol to better imitate human urine. Sci Rep 91(9):1–11. https://doi.org/10.1038/s41598-019-56693-4
Segata N, Haake SK, Mannon P et al (2012) Composition of the adult digestive tract bacterial microbiome based on seven mouth surfaces, tonsils, throat and stool samples. Genome Biol 13:1–18. https://doi.org/10.1186/GB-2012-13-6-R42/FIGURES/6, https://genomebiology.biomedcentral.com/articles/10.1186/gb-2012-13-6-r42
Serra R, Grande R, Buffone G et al (2016) Extracellular matrix assessment of infected chronic venous leg ulcers: role of metalloproteinases and inflammatory cytokines. Int Wound J 13:53. https://doi.org/10.1111/IWJ.12225
Settem RP, El-Hassan AT, Honma K et al (2012) Fusobacterium nucleatum and tannerella forsythia induce synergistic alveolar bone loss in a mouse periodontitis model. Infect Immun 80:2436–2443. https://doi.org/10.1128/IAI.06276-11/ASSET/93EC17B7-2973-4BC4-91FA-D2CF6DF0C372/ASSETS/GRAPHIC/ZII9990997180007.JPEG
Shanmugasundaram N, Sundaraseelan J, Uma S et al (2006) Design and delivery of silver sulfadiazine from alginate microspheres-impregnated collagen scaffold. J Biomed Mater Res B Appl Biomater 77B:378–388. https://doi.org/10.1002/JBM.B.30405
Sharp D (2013) Printed composite electrodes for in-situ wound pH monitoring. Biosens Bioelectron 50:399–405. https://doi.org/10.1016/J.BIOS.2013.06.042
Shepherd J, Douglas I, Rimmer S et al (2009) Development of three-dimensional tissue-engineered models of bacterial infected human skin wounds. Tissue Eng Part C Methods 15:475–484. https://doi.org/10.1089/TEN.TEC.2008.0614
Silva MD, Sillankorva S (2019) Otitis media pathogens – a life entrapped in biofilm communities. Crit Rev Microbiol 45:595–612. https://doi.org/10.1080/1040841X.2019.1660616
Simoska O, Duay J, Stevenson KJ (2020) Electrochemical detection of multianalyte biomarkers in wound healing efficacy. ACS Sens 5:3547–3557. https://doi.org/10.1021/ACSSENSORS.0C01697/SUPPL_FILE/SE0C01697_SI_001.PDF
Singer AJ, Dagum AB (2009) Current management of acute cutaneous wounds. N Engl J Med 359:1037–1046. https://doi.org/10.1056/NEJMRA0707253
Siqueira JF, Rôças IN (2021) Present status and future directions: microbiology of endodontic infections. Int Endod J 55:512–530. https://doi.org/10.1111/IEJ.13677
Sissons CH, Cutress TW, Hoffman MP, Wakefield JSJ (1991) A multi-station dental plaque microcosm (artificial mouth) for the study of plaque growth, metabolism, pH, and mineralization. J Dent Res 70:1409–1416. https://doi.org/10.1177/00220345910700110301
Sissons CH, Cutress TW, Faulds G, Wong L (1992) pH responses to sucrose and the formation of pH gradients in thick “artificial mouth” microcosm plaques. Arch Oral Biol 37:913–922. https://doi.org/10.1016/0003-9969(92)90062-D
Sissons CH, Wong L, Cutress TW (1995) Patterns and rates of growth of microcosm dental plaque biofilms. Oral Microbiol Immunol 10:160–167. https://doi.org/10.1111/J.1399-302X.1995.TB00137.X
Stecher B (2015) The roles of inflammation, nutrient availability and the commensal microbiota in enteric pathogen infection. Microbiol Spectr 3:297–320. https://doi.org/10.1128/MICROBIOLSPEC.MBP-0008-2014
Stewart PS, Philip Stewart CS (2014) Biophysics of biofilm infection. Pathog Dis 70:212–218. https://doi.org/10.1111/2049-632X.12118
Sun Y, Dowd SE, Smith E et al (2008) In vitro multispecies Lubbock chronic wound biofilm model. Wound Repair Regen 16:805–813. https://doi.org/10.1111/J.1524-475X.2008.00434.X
Suryaletha K, John J, Radhakrishnan MP et al (2018) Metataxonomic approach to decipher the polymicrobial burden in diabetic foot ulcer and its biofilm mode of infection. Int Wound J 15:473–481. https://doi.org/10.1111/IWJ.12888
Thaarup IC, Bjarnsholt T (2020) Current in vitro biofilm-infected chronic wound models for developing new treatment possibilities. Adv Wound Care 10:91–102. https://doi.org/10.1089/WOUND.2020.1176
Thomen P, Robert J, Monmeyran A et al (2017) Bacterial biofilm under flow: first a physical struggle to stay, then a matter of breathing. PLoS One 12:e0175197. https://doi.org/10.1371/JOURNAL.PONE.0175197
Thornton RB, Rigby PJ, Wiertsema SP et al (2011) Multi-species bacterial biofilm and intracellular infection in otitis media. BMC Pediatr 11:1–10. https://doi.org/10.1186/1471-2431-11-94
Tilley D, Kerrigan SW (2013) Platelet-bacterial interactions in the pathogenesis of infective endocarditis—part I: the streptococcus. In: Recent advances in infective endocarditis. InTech. https://doi.org/10.5772/55912
Trautner BW, Darouiche RO (2004) Role of biofilm in catheter-associated urinary tract infection. Am J Infect Control 32:177. https://doi.org/10.1016/J.AJIC.2003.08.005
Trøstrup H, Thomsen K, Calum H et al (2016) Animal models of chronic wound care: the application of biofilms in clinical research. Chronic Wound Care Manag Res 3:123–132. https://doi.org/10.2147/CWCMR.S84361
Turner KH, Wessel AK, Palmer GC et al (2015) Essential genome of Pseudomonas aeruginosa in cystic fibrosis sputum. Proc Natl Acad Sci U S A 112:4110–4115. https://doi.org/10.1073/PNAS.1419677112/SUPPL_FILE/PNAS.1419677112.SD10.XLSX
Tytgat HLP, Nobrega FL, van der Oost J, de Vos WM (2019) Bowel biofilms: tipping points between a healthy and compromised gut? Trends Microbiol 27:17–25. https://doi.org/10.1016/J.TIM.2018.08.009
Vasconcelos A, Pêgo AP, Henriques L et al (2010) Protein matrices for improved wound healing: elastase inhibition by a synthetic peptide model. Biomacromolecules 11:2213–2220. https://doi.org/10.1021/BM100537B
Venkataraman A, Rosenbaum MA, Werner JJ et al (2014) Metabolite transfer with the fermentation product 2,3-butanediol enhances virulence by Pseudomonas aeruginosa. ISME J 8:1210. https://doi.org/10.1038/ISMEJ.2013.232
Watters C, Fleming D, Bishop D, Rumbaugh KP (2016) Host responses to biofilm. Prog Mol Biol Transl Sci 142:193–239. https://doi.org/10.1016/BS.PMBTS.2016.05.007
Wijesinghe G, Dilhari A, Gayani B et al (2019) Influence of laboratory culture media on in vitro growth, adhesion, and biofilm formation of Pseudomonas aeruginosa and Staphylococcus aureus. Med Princ Pract 28:28–35. https://doi.org/10.1159/000494757
Wolcott RD, Hanson JD, Rees EJ et al (2016) Analysis of the chronic wound microbiota of 2,963 patients by 16S rDNA pyrosequencing. Wound Repair Regen 24:163–174. https://doi.org/10.1111/WRR.12370
Wong L, Sissions CH (2001) A comparison of human dental plaque microcosm biofilms grown in an undefined medium and a chemically defined artificial saliva. Arch Oral Biol 46:477–486. https://doi.org/10.1016/S0003-9969(01)00016-4
Wysocki A (1996) Wound fluids and the pathogenesis of chronic wounds. J WOCN 23:283–290. https://doi.org/10.1016/S1071-5754(96)90047-9
Yan J, Bassler BL (2019) Surviving as a community: antibiotic tolerance and persistence in bacterial biofilms. Cell Host Microbe 26:15–21. https://doi.org/10.1016/J.CHOM.2019.06.002
Yu Y, Singh H, Tsitrin T et al (2021) Urethral catheter biofilms reveal plasticity in bacterial composition and metabolism and withstand host immune defenses in hypoxic environment. Front Med 8:788. https://doi.org/10.3389/FMED.2021.667462/BIBTEX
Zaat S, Broekhuizen C, Riool M (2010) Host tissue as a niche for biomaterial-associated infection. Future Microbiol 5:1149–1151. https://doi.org/10.2217/FMB.10.89
Zhao R, Liang H, Clarke E et al (2016) Inflammation in chronic wounds. Int J Mol Sci 17:2085. https://doi.org/10.3390/IJMS17122085
Conflict of Interest
None.
Author Contributions
Anoushka Gholap: Writing the original draft, Preparation of figures. Snehal Murumkar: Writing the original draft, Preparation of figures. Meetali Barhate: Writing the original draft, Preparation of figures. Radhika Dhekane: Writing the original draft. Nijamuddin Shaikh: Writing the original draft. Deepti Bandaru: Writing the original draft. Rutuja Ugale: Writing the original draft. Utkarsha Tikhole: Writing the original draft. Snehal Kadam: Writing the original draft. Vandana Madhusoodhanan: Writing the original draft. Karishma S Kaushik: Conceptualization, Project administration, Supervision, Writing the original draft, Finalizing draft, Editing draft.
Funding
Karishma S Kaushik’s academic appointment is funded by the Ramalingaswami Re-entry Fellowship (BT/HRD/35/02/2006). Snehal Kadam and Nijamuddin Shaikh were supported for a select duration of this work on the Ramalingaswami Re-entry Fellowship (to KSK). Radhika Dhekane is funded by the Innovative Young Biotechnologist Award (BT/12/IYBA/2019/05 to KSK). Deepti Bandaru is a paid consultant with Centre for Health, Research and Education, Southampton, United Kingdom.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2023 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Dhekane, R. et al. (2023). 3M’s of Multi-Species Biofilms: Microbial Pathogens, Microenvironments, and Minimalist Laboratory Approaches to Study Multi-Species Biofilms Under Microenvironmental Conditions. In: Kaushik, K.S., Darch, S.E. (eds) Multispecies Biofilms. Springer Series on Biofilms, vol 12. Springer, Cham. https://doi.org/10.1007/978-3-031-15349-5_1
Download citation
DOI: https://doi.org/10.1007/978-3-031-15349-5_1
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-031-15348-8
Online ISBN: 978-3-031-15349-5
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)