Publications by authors named "Mette Burmølle"

67 Publications

Community-wide changes reflecting bacterial interspecific interactions in multispecies biofilms.

Crit Rev Microbiol 2021 May 2;47(3):338-358. Epub 2021 Mar 2.

State Key Laboratory of Food Science and Technology, Jiangnan University, Wuxi, China.

Existence of most bacterial species, in natural, industrial, and clinical settings in the form of surface-adhered communities or biofilms has been well acknowledged for decades. Research predominantly focusses on single-species biofilms as these are relatively easy to study. However, microbiologists are now interested in studying multispecies biofilms and revealing interspecific interactions in these communities because of the existence of a plethora of different bacterial species together in almost all natural settings. Multispecies biofilms-led emergent properties are triggered by bacterial social interactions which have huge implication for research and practical knowledge useful for the control and manipulation of these microbial communities. Here, we discuss some important bacterial interactions that take place in multispecies biofilm communities and provide insights into community-wide changes that indicate bacterial interactions and elucidate underlying mechanisms.
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http://dx.doi.org/10.1080/1040841X.2021.1887079DOI Listing
May 2021

Antibiotic susceptibility of cystic fibrosis lung microbiome members in a multispecies biofilm.

Biofilm 2020 Dec 13;2:100031. Epub 2020 Jun 13.

Laboratory of Pharmaceutical Microbiology, Ghent University, Belgium.

The lungs of cystic fibrosis (CF) patients are often chronically colonized by multiple microbial species that can form biofilms, including the major CF pathogen . Herewith, lower microbial diversity in CF airways is typically associated with worse health outcomes. In an attempt to treat CF lung infections patients are frequently exposed to antibiotics, which may affect microbial diversity. This study aimed at understanding if common antibiotics that target influence microbial diversity. To this end, a microaerophilic multispecies biofilm model of frequently co-isolated members of the CF lung microbiome (, , , , , and ) was exposed to antipseudomonal antibiotics. We found that antibiotics that affected several dominant species (i.e. ceftazidime, tobramycin) resulted in higher species evenness compared to colistin, which is only active against . Furthermore, susceptibility of individual species in the multispecies biofilm following antibiotic treatment was compared to that of the respective single-species biofilms, showing no differences. Adding three anaerobic species (, , and ) to the multispecies biofilm did not influence antibiotic susceptibility. In conclusion, our study demonstrates antibiotic-dependent effects on microbial community diversity of multispecies biofilms comprised of CF microbiome members.
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http://dx.doi.org/10.1016/j.bioflm.2020.100031DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7798459PMC
December 2020

Persistence and progression of staphylococcal infection in the presence of public goods.

NPJ Biofilms Microbiomes 2020 11 27;6(1):55. Epub 2020 Nov 27.

Section of Microbiology, Department of Biology, Faculty of Science, University of Copenhagen, 2100, Copenhagen, Denmark.

Staphylococcus aureus is a prominent etiological agent of suppurative abscesses. In principle, abscess formation and purulent exudate are classical physiological features of healing and tissue repair. However, S. aureus deploys two coagulases that can usurp this classical host response and form distinct abscess lesions. Here, we establish that during coinfection with coagulase producers and non-producers, coagulases are shared public goods that contribute to staphylococcal persistence, abscess formation, and disease progression. Coagulase-negative mutants that do not produce the public goods themselves are able to exploit those cooperatively secreted by producers and thereby thrive during coinfection at the expense of others. This study shows the importance of social interactions among pathogens concerning clinical outcomes.
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http://dx.doi.org/10.1038/s41522-020-00168-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7699630PMC
November 2020

Do environmental pharmaceuticals affect the composition of bacterial communities in a freshwater stream? A case study of the Knivsta river in the south of Sweden.

Sci Total Environ 2021 Apr 16;763:142991. Epub 2020 Oct 16.

Department of Chemistry, Umeå Center for Microbial Research, Umeå University, 901 87 Umeå, Sweden. Electronic address:

Pharmaceutical substances present at low concentrations in the environment may cause effects on biological systems such as microbial consortia living on solid riverbed substrates. These consortia are an important part of the river ecosystem as they form part of the food chain. This case study aims to contribute to an increased understanding of how low levels of pharmaceuticals in freshwater streams may influence sessile bacterial consortia. An important point source for pharmaceutical release into the environment is treated household sewage water. In order to investigate what types of effects may occur, we collected water samples as well as riverbed substrates from a small stream in the south of Sweden, Knivstaån, upstream and downstream from a sewage treatment plant (STP). Data from these samples formed the base of this case study where we investigated both the presence of pharmaceuticals in the water and bacterial composition on riverbed substrates. In the water downstream from the STP, 19 different pharmaceuticals were detected at levels below 800 ng/dm. The microbial composition was obtained from sequencing 16S rRNA genes directly from substrates as well as from cultivated isolates. The cultivated strains showed reduced species variability compared with the data obtained directly from the substrates. No systematic differences were observed following the sampling season. However, differences could be seen between samples upstream and downstream from the STP effluent. We further observed large similarities in bacterial composition on natural stones compared to sterile stones introduced into the river approximately two months prior to sampling, giving indications for future sampling methodology of biofilms.
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http://dx.doi.org/10.1016/j.scitotenv.2020.142991DOI Listing
April 2021

Do Mixed-Species Biofilms Dominate in Chronic Infections?-Need for Visualization of Bacterial Organization.

Front Cell Infect Microbiol 2020 5;10:396. Epub 2020 Aug 5.

Department of Immunology and Microbiology, Faculty of Health and Medical Sciences, Costerton Biofilm Center, University of Copenhagen, Copenhagen, Denmark.

Chronic infections present a serious economic burden to health-care systems. The severity and prevalence of chronic infections are continuously increasing due to an aging population and an elevated number of lifestyle related diseases such as diabetes. Treatment of chronic infections has proven difficult, mainly due to the presence of biofilms that render bacteria more tolerant toward antimicrobials and the host immune response. Chronic infections have been described to harbor several different bacterial species and it has been hypothesized that microscale interactions and mixed-species consortia are present as described for most natural occurring biofilms i.e., aquatic systems and industrial settings, but also for some commensal human biofilms i.e., the mouth microbiota. However, the presence of mixed-species biofilms in chronic infections is most often an assumption based on culture-based methods and/or by means of molecular approaches, such as PCR and sequencing performed from homogenized bulk tissue samples. These methods disregard the spatial organization of the bacterial community and thus valuable information on biofilm aggregate composition, spatial organization, and possible interactions between different species is lost. Hitherto, only few studies have made visual presentations of mixed-species biofilms in chronic infections, which is pivotal for the description of bacterial composition, spatial distribution, and interspecies interaction on the microscale. In order for bacteria to interact (synergism, commensalism, mutualism, competition, etc.) they need to be in close proximity to each other on the scale where they can affect e.g., solute concentrations. We argue that visual proof of mixed species biofilms in chronic infections is scarce compared to what is seen in e.g., environmental biofilms and call for a debate on the importance of mixed-species biofilm in chronic infections.
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http://dx.doi.org/10.3389/fcimb.2020.00396DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7419433PMC
August 2020

The T-shirt microbiome is distinct between individuals and shaped by washing and fabric type.

Environ Res 2020 06 30;185:109449. Epub 2020 Mar 30.

Section of Microbiology, Department of Biology, University of Copenhagen, Denmark. Electronic address:

Activity of the microbial population in clothing causes unpleasant odor and textile deterioration. However, little is known about how the textile microbial community is shaped. In this study, we developed a method for extracting DNA from small amounts of detergent-washed clothing, and applied it to both worn and unworn, washed and unwashed cotton and polyester samples of the axillary region of T-shirts from 10 male subjects. The combined application of 16S rRNA gene amplicon sequencing and quantitative PCR allowed us to estimate the absolute abundances of bacteria in the samples. We found that the T-shirt microbiome was highly individual, both in composition, diversity and microbial biomass. Fabric type was influential where Acinetobacter was more abundant in cotton. Intriguingly, unworn cotton T-shirts had a native microbiome dominated by Acinetobacter, whereas unworn polyester had no detectable bacterial microbiome. The native textile microbiome did not seem to have any effect on the microbial composition emerging from wearing the garment. Surprisingly, washing in mild detergent had only minor effects on the composition and biomass of the microbial community, and only few Amplicon Sequence Variants (ASV)s were found to decrease in abundance after washing. Individual variations between test subjects shaped the microbial community more than the type of fabric or wash with detergent. The individuality of T-shirt microbiomes and specificity of the washing procedure suggests that personalized laundry regimes could be applied to increase efficient removal of undesired bacteria.
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http://dx.doi.org/10.1016/j.envres.2020.109449DOI Listing
June 2020

High cell densities favor lysogeny: induction of an H20 prophage is repressed by quorum sensing and enhances biofilm formation in Vibrio anguillarum.

ISME J 2020 07 9;14(7):1731-1742. Epub 2020 Apr 9.

Department of Biology, University of Copenhagen, Copenhagen, Denmark.

Temperate ϕH20-like phages are repeatedly identified at geographically distinct areas as free phage particles or as prophages of the fish pathogen Vibrio anguillarum. We studied mutants of a lysogenic isolate of V. anguillarum locked in the quorum-sensing regulatory modes of low (ΔvanT) and high (ΔvanO) cell densities by in-frame deletion of key regulators of the quorum-sensing pathway. Remarkably, we find that induction of the H20-like prophage is controlled by the quorum-sensing state of the host, with an eightfold increase in phage particles per cell in high-cell-density cultures of the quorum-sensing-deficient ΔvanT mutant. Comparative studies with prophage-free strains show that biofilm formation is promoted at low cell density and that the H20-like prophage stimulates this behavior. In contrast, the high-cell-density state is associated with reduced prophage induction, increased proteolytic activity, and repression of biofilm. The proteolytic activity may dually function to disperse the biofilm and as a quorum-sensing-mediated antiphage strategy. We demonstrate an intertwined regulation of phage-host interactions and biofilm formation, which is orchestrated by host quorum-sensing signaling, suggesting that increased lysogeny at high cell density is not solely a strategy for phages to piggy-back the successful bacterial hosts but is also a host strategy evolved to take control of the lysis-lysogeny switch to promote host fitness.
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http://dx.doi.org/10.1038/s41396-020-0641-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7305317PMC
July 2020

Community-intrinsic properties enhance keratin degradation from bacterial consortia.

PLoS One 2020 31;15(1):e0228108. Epub 2020 Jan 31.

Section for Microbiology, Department of Biology, University of Copenhagen, Copenhagen, Denmark.

Although organic matter may accumulate sometimes (e.g. lignocellulose in peat bog), most natural biodegradation processes are completed until full mineralization. Such transformations are often achieved by the concerted action of communities of interacting microbes, involving different species each performing specific tasks. These interactions can give rise to novel "community-intrinsic" properties, through e.g. activation of so-called "silent genetic pathways" or synergistic interplay between microbial activities and functions. Here we studied the microbial community-based degradation of keratin, a recalcitrant biological material, by four soil isolates, which have previously been shown to display synergistic interactions during biofilm formation; Stenotrophomonas rhizophila, Xanthomonas retroflexus, Microbacterium oxydans and Paenibacillus amylolyticus. We observed enhanced keratin weight loss in cultures with X. retroflexus, both in dual and four-species co-cultures, as compared to expected keratin degradation by X. retroflexus alone. Additional community intrinsic properties included accelerated keratin degradation rates and increased biofilm formation on keratin particles. Comparison of secretome profiles of X. retroflexus mono-cultures to co-cultures revealed that certain proteases (e.g. serine protease S08) were significantly more abundant in mono-cultures, whereas co-cultures had an increased abundance of proteins related to maintaining the redox environment, e.g. glutathione peroxidase. Hence, one of the mechanisms related to the community intrinsic properties, leading to enhanced degradation from co-cultures, might be related to a switch from sulfitolytic to proteolytic functions between mono- and co-cultures, respectively.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0228108PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6994199PMC
May 2020

Interspecies interactions reduce selection for a biofilm-optimized variant in a four-species biofilm model.

Environ Microbiol Rep 2019 12 14;11(6):835-839. Epub 2019 Nov 14.

Section of Microbiology, Department of Biology, University of Copenhagen, Copenhagen, Denmark.

Multispecies biofilms are structured and spatially defined communities, where interspecies interactions impact assembly and functionality. Here, we compared the spatial organization and growth of bacterial cells in differently composed biofilm communities over time to determine links between interspecies interactions and selection for biofilm phenotypes of individual species. An established model community consisting of Stenotrophomonas rhizophila, Xanthomonas retroflexus, Microbacterium oxydans and Paenibacillus amylolyticus was used. It was found that interspecies interactions led to varying levels of selection for a new colony phenotype of X. retroflexus, depending on the presence/absence of other species. When M. oxydans was absent, X. retroflexus was not able to establish in the top layers of the biofilm, which led to selection for a hyper-matrix forming phenotype of X. retroflexus that successfully established in the biofilm top layers. No such phenotypic X. retroflexus variants were identified in the presence of M. oxydans. These findings indicate that interspecies interactions may lead to favourable localization of individual species in a multispecies biofilm and thereby reduce selection for competitive phenotypes.
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http://dx.doi.org/10.1111/1758-2229.12803DOI Listing
December 2019

Unravelling interspecies interactions across heterogeneities in complex biofilm communities.

Environ Microbiol 2020 01 10;22(1):5-16. Epub 2019 Nov 10.

Section of Microbiology, Department of Biology, University of Copenhagen, Copenhagen, Denmark.

The importance of microbial biofilms has been well-recognized for several decades, and focus is now shifting towards investigating multispecies biofilm communities rather than mono- or dual-species biofilms. Therefore, the demand for techniques that provide a sufficient amount of information at adequate resolution is increasing. One major challenge for multispecies studies is that diversity and spatial organization often lead to a high degree of spatial and chemical heterogeneity. Many current approaches do not account for such heterogeneity and therefore only provide average information (-omics techniques in particular), which could obscure important information about the community. Here, we bring attention to the issues of heterogeneity when analysing synthetic multi-species biofilms, in vitro, and the importance of multi-scale approaches. We provide an overview of current and newer approaches that can be applied to biofilm communities, in order to elucidate interactions at the appropriate scale.
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http://dx.doi.org/10.1111/1462-2920.14834DOI Listing
January 2020

Interspecies interactions reduce selection for a biofilm optimized variant in a four-species biofilm model.

Environ Microbiol 2019 Sep 12. Epub 2019 Sep 12.

Section of Microbiology, Department of Biology, University of Copenhagen, Denmark.

Multispecies biofilms are structured and spatially defined communities, where interspecies interactions impact assembly and functionality. Here we compared the spatial organization and growth of bacterial cells in differently composed biofilm communities over time to determine links between interspecies interactions and selection for biofilm phenotypes of individual species. An established model community consisting of Stenotrophomonas rhizophila, Xanthomonas retroflexus, Microbacterium oxydans and Paenibacillus amylolyticus was used. It was found that interspecies interactions led to varying levels of selection for a new colony phenotype of X. retroflexus, depending on the presence/absence of other species. When M. oxydans was absent, X. retroflexus was not able to establish in the top layers of the biofilm, which led to selection for a hyper-matrix forming phenotype of X. retroflexus that successfully established in the biofilm top layers. No such phenotypic X. retroflexus variants were identified in the presence of M. oxydans. These findings indicate that interspecies interactions may lead to favourable localization of individual species in a multispecies biofilm and thereby reduce selection for competitive phenotypes. This article is protected by copyright. All rights reserved.
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http://dx.doi.org/10.1111/1462-2920.14802DOI Listing
September 2019

Priority of Early Colonizers but No Effect on Cohabitants in a Synergistic Biofilm Community.

Front Microbiol 2019 23;10:1949. Epub 2019 Aug 23.

Section of Microbiology, Department of Biology, University of Copenhagen, Copenhagen, Denmark.

The arrival order of different species to a habitat can strongly impact community assembly and succession dynamics, thus influencing functionality. In this study, we asked how prior colonization of one community member would influence the assembly of a synergistic multispecies biofilm community grown . We expected that the prior arrival would confer an advantage, in particular for good biofilm formers. Yet, we did not know if the cohabitants would be impaired or benefit from the pre-colonization of one member, depending on its ability to form biofilm. We used a consortium consisting of four soil bacteria; and . This consortium has been shown to act synergistically when grown together, thus increasing biofilm production. The results showed that the two good biofilm formers gained a fitness advantage (increase in abundance) when allowed prior colonization on an abiotic surface before the arrival of their cohabitants. Interestingly, the significantly higher number of the pre-colonized biofilm formers did not affect the resulting composition in the subsequent biofilm after 24 h.
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http://dx.doi.org/10.3389/fmicb.2019.01949DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6716445PMC
August 2019

Deciphering links between bacterial interactions and spatial organization in multispecies biofilms.

ISME J 2019 12 27;13(12):3054-3066. Epub 2019 Aug 27.

School of Food and Pharmaceutical engineering, Nanjing Normal University, Nanjing, China.

Environmental microbes frequently live in multispecies biofilms where mutualistic relationships and co-evolution may occur, defining spatial organization for member species and overall community functions. In this context, intrinsic properties emerging from microbial interactions, such as efficient organization optimizing growth and activities in multispecies biofilms, may become the object of fitness selection. However, little is known on the nature of underlying interspecies interactions during establishment of a predictable spatial organization within multispecies biofilms. We present a comparative metatranscriptomic analysis of bacterial strains residing in triple-species and four-species biofilms, aiming at deciphering molecular mechanisms underpinning bacterial interactions responsible of the remarkably enhanced biomass production and associated typical spatial organization they display. Metatranscriptomic profiles concurred with changes in micro-site occupation in response to the addition/removal of a single species, being driven by both cooperation, competition, and facilitation processes. We conclude that the enhanced biomass production of the four-species biofilm is an intrinsic community property emerging from finely tuned space optimization achieved through concerted antagonistic and mutualistic interactions, where each species occupies a defined micro-site favoring its own growth. Our results further illustrate how molecular mechanisms can be better interpreted when supported by visual imaging of actual microscopic spatial organization, and we propose phenotypic adaptation selected by social interactions as molecular mechanisms stabilizing microbial communities.
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http://dx.doi.org/10.1038/s41396-019-0494-9DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6864094PMC
December 2019

Mixed-species biofilms in the food industry: Current knowledge and novel control strategies.

Crit Rev Food Sci Nutr 2020 1;60(13):2277-2293. Epub 2019 Jul 1.

College of Biosystems Engineering and Food Science, Zhejiang University, Hangzhou, China.

Attachment of microorganisms to food contact surfaces and the subsequent formation of biofilms may cause equipment damage, food spoilage and even diseases. Mixed-species biofilms are ubiquitous in the food industry and they generally exhibit higher resistance to disinfectants and antimicrobials compared to single-species biofilms. The physiology and metabolic activity of microorganisms in mixed-species biofilms are however rather complicated to study, and despite targeted research efforts, the potential role of mixed-species biofilms in food industry is still rather unexplored. In this review, we summarize recent studies in the context of bacterial social interactions in mixed-species biofilms, resistance to disinfectants, detection methods, and potential novel strategies to control the formation of mixed-species biofilms for enhanced food safety and food quality.
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http://dx.doi.org/10.1080/10408398.2019.1632790DOI Listing
September 2020

Insights into Psychrotrophic Bacteria in Raw Milk: A Review.

J Food Prot 2019 Jul;82(7):1148-1159

1 College of Biosystems Engineering and Food Science, Zhejiang University, Hangzhou 310058, People's Republic of China.

Highlights: Levels of psychrotrophic bacteria in raw milk are affected by to habitats and farm hygiene. Biofilms formed by psychrotrophic bacteria are persistent sources of contamination. Heat-stable enzymes produced by psychrotrophic bacteria compromise product quality. Various strategies are available for controlling dairy spoilage caused by psychrotrophic bacteria.
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http://dx.doi.org/10.4315/0362-028X.JFP-19-032DOI Listing
July 2019

Big Impact of the Tiny: Bacteriophage-Bacteria Interactions in Biofilms.

Trends Microbiol 2019 09 22;27(9):739-752. Epub 2019 May 22.

Section of Microbiology, Department of Biology, University of Copenhagen, Denmark. Electronic address:

Bacteriophages (phages) have been shaping bacterial ecology and evolution for millions of years, for example, by selecting for defence strategies. Evidence supports that bacterial biofilm formation is one such strategy and that biofilm-mediated protection against phage infection depends on maturation and composition of the extracellular matrix. Interestingly, studies have revealed that phages can induce and strengthen biofilms. Here we review interactions between bacteria and phages in biofilms, discuss the underlying mechanisms, the potential of phage therapy for biofilm control, and emphasize the importance of considering biofilms in future phage research. This is especially relevant as biofilms are associated with increased tolerance towards antibiotics and are implicated in the majority of chronic infections.
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http://dx.doi.org/10.1016/j.tim.2019.04.006DOI Listing
September 2019

Fluidic resistance control enables high-throughput establishment of mixed-species biofilms.

Biotechniques 2019 05;66(5):235-239

Section of Microbiology, Universitetsparken 15, Department of Biology, Faculty of Science, University of Copenhagen, 2100 Copenhagen, Denmark.

Bacteria often live in communities of mixed species embedded in a self-produced extracellular matrix of polysaccharides, proteins and DNA, termed biofilms. The BioFlux microfluidic flow system is useful for studying biofilm formation in different media under flow. However, analyzing the architecture and maturation of biofilms under flow requires a proper seeding, which can prove difficult when working with bacteria of different sizes, motile bacteria or aiming for a high number of replicates. Here we developed an efficient protocol that exploits viscosity tuning and seeding indicator dyes to improve seeding and allow for high-throughput examination and visualization of consistent mono- and mixed-species biofilm developments under flow.
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http://dx.doi.org/10.2144/btn-2018-0150DOI Listing
May 2019

Evaluating Efficacy of Antimicrobial and Antifouling Materials for Urinary Tract Medical Devices: Challenges and Recommendations.

Macromol Biosci 2019 05 18;19(5):e1800384. Epub 2019 Mar 18.

University of Groningen, University Medical Center Groningen, Department of Biomedical Engineering, Antonius Deusinglaan 1, 9713 AV, Groningen, The Netherlands.

In Europe, the mean incidence of urinary tract infections in intensive care units is 1.1 per 1000 patient-days. Of these cases, catheter-associated urinary tract infections (CAUTI) account for 98%. In total, CAUTI in hospitals is estimated to give additional health-care costs of £1-2.5 billion in the United Kingdom alone. This is in sharp contrast to the low cost of urinary catheters and emphasizes the need for innovative products that reduce the incidence rate of CAUTI. Ureteral stents and other urinary-tract devices suffer similar problems. Antimicrobial strategies are being developed, however, the evaluation of their efficacy is very challenging. This review aims to provide considerations and recommendations covering all relevant aspects of antimicrobial material testing, including surface characterization, biocompatibility, cytotoxicity, in vitro and in vivo tests, microbial strain selection, and hydrodynamic conditions, all in the perspective of complying to the complex pathology of device-associated urinary tract infection. The recommendations should be on the basis of standard assays to be developed which would enable comparisons of results obtained in different research labs both in industry and in academia, as well as provide industry and academia with tools to assess the antimicrobial properties for urinary tract devices in a reliable way.
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http://dx.doi.org/10.1002/mabi.201800384DOI Listing
May 2019

coagulases are exploitable yet stable public goods in clinically relevant conditions.

Proc Natl Acad Sci U S A 2018 12 21;115(50):E11771-E11779. Epub 2018 Nov 21.

Section of Microbiology, Department of Biology, Faculty of Science, University of Copenhagen, 2100 Copenhagen, Denmark;

Coagulation is an innate defense mechanism intended to limit blood loss and trap invading pathogens during infection. However, has the ability to hijack the coagulation cascade and generate clots via secretion of coagulases. Although many have this characteristic, some do not. The population dynamics regarding this defining trait have yet to be explored. We report here that coagulases are public goods that confer protection against antimicrobials and immune factors within a local population or community, thus promoting growth and virulence. By utilizing variants of a methicillin-resistant we infer that the secretion of coagulases is a cooperative trait, which is subject to exploitation by invading mutants that do not produce the public goods themselves. However, overexploitation, "tragedy of the commons," does not occur at clinically relevant conditions. Our micrographs indicate this is due to spatial segregation and population viscosity. These findings emphasize the critical role of coagulases in a social evolution context and provide a possible explanation as to why the secretion of these public goods is maintained in mixed communities.
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http://dx.doi.org/10.1073/pnas.1804850115DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6294911PMC
December 2018

Insights into Bacterial Milk Spoilage with Particular Emphasis on the Roles of Heat-Stable Enzymes, Biofilms, and Quorum Sensing.

J Food Prot 2018 10;81(10):1651-1660

1 College of Biosystems Engineering and Food Science, Zhejiang University, Hangzhou 310058, People's Republic of China; and.

Milk spoilage caused by psychrotrophic bacteria and their heat-stable enzymes is a serious challenge for the dairy industry. In many studies, spoilage has been explored based on the simplistic view of undesirable enzymes produced by planktonic cells. Recently, biofilms and quorum sensing (QS) have been suggested as important factors in the deterioration of milk, which opens new avenues for investigation of the processes and challenges. Production and heat stability of enzymes are enhanced in biofilms, mainly because of inherent differences in physiological states and protective shielding by extracellular polymeric substances. QS plays a key role in modulating expression of hydrolytic enzymes and biofilm formation. To date, few studies have been conducted to investigate the complex interplays of enzyme production, biofilm formation, and QS. This review provides novel insights into milk spoilage with particular emphasis on the roles of biofilms and QS and summarizes potential effective strategies for controlling the spoilage of milk.
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http://dx.doi.org/10.4315/0362-028X.JFP-18-094DOI Listing
October 2018

Community Synergy between Bacterial Soil Isolates Can Be Facilitated by pH Stabilization of the Environment.

Appl Environ Microbiol 2018 11 17;84(21). Epub 2018 Oct 17.

Section for Microbiology, University of Copenhagen, Copenhagen, Denmark

The composition and development of naturally occurring microbial communities are defined by a complex interplay between the community and the surrounding environment and by interactions between community members. Intriguingly, these interactions can in some cases cause synergies, where the community is able to outperform its single-species constituents. However, the underlying mechanisms driving community interactions are often unknown and difficult to identify due to high community complexity. Here, we show how opposite pH drift induced by specific community members leads to pH stabilization of the microenvironment, acting as a positive interspecies interaction, driving community synergy in a model consortium of four coisolated soil bacteria, , , , and We use microsensor pH measurements to show how individual species change the local pH microenvironment and how cocultivation leads to a stabilized pH regime over time. Specifically, acid production from and alkali production primarily from led to an overall pH stabilization of the local environment over time, which in turn resulted in enhanced community growth. This specific type of interspecies interaction was found to be highly dependent on medium type and concentration; however, similar pH drift from the individual species could be observed across medium variants. Understanding interspecies interactions in bacterial communities is important for unraveling species dynamics in naturally occurring communities. These dynamics are fundamental for identifying evolutionary drivers and for the development of efficient biotechnological industry applications. Recently, pH interplay among community members has been identified as a factor affecting community development, and pH stabilization has been demonstrated to result in enhanced community growth. The use of model communities in which the effect of changing pH level can be attributed to specific species contributes to the investigation of community developmental drivers. This contributes to assessment of the extent of emergent behavior and members' contributions to community development. Here, we show that pH stabilization of the microenvironment in a synthetic coisolated model community results in synergistic growth. This observation adds to the growing diversity of community interactions leading to enhanced community growth and hints toward pH as a strong driver for community development in diverse environments.
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http://dx.doi.org/10.1128/AEM.01450-18DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6193382PMC
November 2018

Enhanced bacterial mutualism through an evolved biofilm phenotype.

ISME J 2018 11 5;12(11):2608-2618. Epub 2018 Jul 5.

Department of Biology, University of Copenhagen, 2100, Copenhagen Ø, Denmark.

Microbial communities primarily consist of multiple species that affect one another's fitness both directly and indirectly. This study showed that the cocultivation of Paenibacillus amylolyticus and Xanthomonas retroflexus exhibited facultative mutualistic interactions in a static environment, during the course of which a new adapted phenotypic variant of X. retroflexus appeared. Although the emergence of this variant was not directly linked to the presence of P. amylolyticus, its establishment in the coculture enhanced the productivity of both species due to mutations that stimulated biofilm formation. The mutations were detected in genes encoding a diguanylate cyclase predicted to synthesise cyclic-di-GMP. Examinations of the biofilm formed in cocultures of P. amylolyticus and the new variant of X. retroflexus revealed a distinct spatial organisation: P. amylolyticus only resided in biofilms in association with X. retroflexus and occupied the outer layers. The X. retroflexus variant therefore facilitated increased P. amylolyticus growth as it produced more biofilm biomass. The increase in X. retroflexus biomass was thus not at the expense of P. amylolyticus, demonstrating that interspecies interactions can shape diversification in a mutualistic coculture and reinforce these interactions, ultimately resulting in enhanced communal performance.
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http://dx.doi.org/10.1038/s41396-018-0165-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6194118PMC
November 2018

Micro-scale intermixing: a requisite for stable and synergistic co-establishment in a four-species biofilm.

ISME J 2018 08 18;12(8):1940-1951. Epub 2018 Apr 18.

Section of Microbiology, Department of Biology, University of Copenhagen, Copenhagen, Denmark.

Microorganisms frequently coexist in complex multispecies communities, where they distribute non-randomly, reflective of the social interactions that occur. It is therefore important to understand how social interactions and local spatial organization influences multispecies biofilm succession. Here the localization of species pairs was analyzed in three dimensions in a reproducible four-species biofilm model, to study the impact of spatial positioning of individual species on the temporal development of the community. We found, that as the biofilms developed, species pairs exhibited distinct intermixing patterns unique to the four-member biofilms. Higher biomass and more intermixing were found in four-species biofilms compared to biofilms with fewer species. Intriguingly, in local regions within the four member biofilms where Microbacterium oxydans was scant, both biomass and intermixing of all species were lowered, compared to regions where M. oxydans was present at typical densities. Our data suggest that Xanthomonas retroflexus and M. oxydans, both low abundant biofilm-members, intermixed continuously during the development of the four-species biofilm, hereby facilitating their own establishment. In turn, this seems to have promoted distinct spatial organization of Stenotrophomonas rhizophila and Paenibacillus amylolyticus enabling enhanced growth of all four species. Here local intermixing of bacteria advanced the temporal development of a multi-species biofilm.
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http://dx.doi.org/10.1038/s41396-018-0112-2DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6052071PMC
August 2018

Disease-induced assemblage of a plant-beneficial bacterial consortium.

ISME J 2018 06 8;12(6):1496-1507. Epub 2018 Mar 8.

Plant-Microbe Interactions, Institute of Environmental Biology, Utrecht University, Padualaan 8, 3584 CH, Utrecht, The Netherlands.

Disease suppressive soils typically develop after a disease outbreak due to the subsequent assembly of protective microbiota in the rhizosphere. The role of the plant immune system in the assemblage of a protective rhizosphere microbiome is largely unknown. In this study, we demonstrate that Arabidopsis thaliana specifically promotes three bacterial species in the rhizosphere upon foliar defense activation by the downy mildew pathogen Hyaloperonospora arabidopsidis. The promoted bacteria were isolated and found to interact synergistically in biofilm formation in vitro. Although separately these bacteria did not affect the plant significantly, together they induced systemic resistance against downy mildew and promoted growth of the plant. Moreover, we show that the soil-mediated legacy of a primary population of downy mildew infected plants confers enhanced protection against this pathogen in a second population of plants growing in the same soil. Together our results indicate that plants can adjust their root microbiome upon pathogen infection and specifically recruit a group of disease resistance-inducing and growth-promoting beneficial microbes, therewith potentially maximizing the chance of survival of their offspring that will grow in the same soil.
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http://dx.doi.org/10.1038/s41396-018-0093-1DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5956071PMC
June 2018

Synergistic Interactions in Microbial Biofilms Facilitate the Establishment of Opportunistic Pathogenic Fungi in Household Dishwashers.

Front Microbiol 2018 30;9:21. Epub 2018 Jan 30.

Department of Biology, Biotechnical Faculty, University of Ljubljana, Ljubljana, Slovenia.

Biofilms formed on rubber seals in dishwashers harbor diverse microbiota. In this study, we focussed on the microbial composition of bacteria and fungi, isolated from a defined area of one square centimeter of rubber from four domestic dishwashers and assessed their abilities to multispecies biofilm formation. A total of 80 isolates (64 bacterial and 16 fungal) were analyzed. Multiple combinations of bacterial isolates from each dishwasher were screened for synergistic interactions. 32 out of 140 tested (23%) four-species bacterial combinations displayed consistent synergism leading to an overall increase in biomass, in all experimental trails. Bacterial isolates from two of the four dishwashers generated a high number of synergistically interacting four-species consortia. Network based correlation analyses also showed higher co-occurrence patterns observed between bacterial members in the same two dishwasher samples, indicating cooperative effects. Furthermore, two synergistic four-species bacterial consortia were tested for their abilities to incorporate an opportunistic fungal pathogen, and their establishment as biofilms on sterile ethylene propylene diene monomer M-class (EPDM) rubber and polypropylene (PP) surfaces. When the bacterial consortia included , the overall cell numbers of both bacteria and fungi increased and a substantial increase in biofilm biomass was observed. These results indicate a novel phenomenon of cross kingdom synergy in biofilm formation and these observations could have potential implications for human health.
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http://dx.doi.org/10.3389/fmicb.2018.00021DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5797641PMC
January 2018

Synergistic Interactions within a Multispecies Biofilm Enhance Individual Species Protection against Grazing by a Pelagic Protozoan.

Front Microbiol 2017 9;8:2649. Epub 2018 Jan 9.

Section for Microbiology, Department of Biology, University of Copenhagen, Copenhagen, Denmark.

Biofilm formation has been shown to confer protection against grazing, but little information is available on the effect of grazing on biofilm formation and protection in multispecies consortia. With most biofilms in nature being composed of multiple bacterial species, the interactions and dynamics of a multispecies bacterial biofilm subject to grazing by a pelagic protozoan predator were investigated. To this end, a mono and multispecies biofilms of four bacterial soil isolates, namely and , were constructed and subjected to grazing by the ciliate . In monocultures, grazing strongly reduced planktonic cell numbers in and and also . At the same time, cell numbers in the underlying biofilms increased in and , but not in . This may be due to the fact that while grazing enhanced biofilm formation in the former two species, no biofilm was formed by in monoculture, either with or without grazing. In four-species biofilms, biofilm formation was higher than in the best monoculture, a strong biodiversity effect that was even more pronounced in the presence of grazing. While cell numbers of , and in the planktonic fraction were greatly reduced in the presence of grazers, cell numbers of all three species strongly increased in the biofilm. Our results show that synergistic interactions between the four-species were important to induce biofilm formation, and suggest that bacterial members that produce more biofilm when exposed to the grazer not only protect themselves but also supported other members which are sensitive to grazing, thereby providing a "shared grazing protection" within the four-species biofilm model. Hence, complex interactions shape the dynamics of the biofilm and enhance overall community fitness under stressful conditions such as grazing. These emerging inter- and intra-species interactions could play a vital role in biofilm dynamics in natural environments like soil or aquatic systems.
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http://dx.doi.org/10.3389/fmicb.2017.02649DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5767253PMC
January 2018

Microbial Diversity and Putative Opportunistic Pathogens in Dishwasher Biofilm Communities.

Appl Environ Microbiol 2018 03 14;84(5). Epub 2018 Feb 14.

Molecular Microbial Ecology Group, Section of Microbiology, Department of Biology, University of Copenhagen, Copenhagen, Denmark

Extreme habitats are not only limited to natural environments, but also exist in manmade systems, for instance, household appliances such as dishwashers. Limiting factors, such as high temperatures, high and low pHs, high NaCl concentrations, presence of detergents, and shear force from water during washing cycles, define microbial survival in this extreme system. Fungal and bacterial diversity in biofilms isolated from rubber seals of 24 different household dishwashers was investigated using next-generation sequencing. Bacterial genera such as , , and , known to include opportunistic pathogens, were represented in most samples. The most frequently encountered fungal genera in these samples belonged to , , and , also known to include opportunistic pathogenic representatives. This study showed how specific conditions of the dishwashers impact the abundance of microbial groups and investigated the interkingdom and intrakingdom interactions that shape these biofilms. The age, usage frequency, and hardness of incoming tap water of dishwashers had significant impact on bacterial and fungal community compositions. Representatives of spp. were found at the highest prevalence (100%) in all dishwashers and are assumed to be one of the first colonizers in recently purchased dishwashers. Pairwise correlations in tested microbiomes showed that certain bacterial groups cooccur, as did the fungal groups. In mixed bacterial-fungal biofilms, early adhesion, contact, and interactions were vital in the process of biofilm formation, where mixed complexes of bacteria and fungi could provide a preliminary biogenic structure for the establishment of these biofilms. Worldwide demand for household appliances, such as dishwashers and washing machines, is increasing, as is the number of immunocompromised individuals. The harsh conditions in household dishwashers should prevent the growth of most microorganisms. However, our research shows that persisting polyextremotolerant groups of microorganisms in household appliances are well established under these unfavorable conditions and supported by the biofilm mode of growth. The significance of our research is in identifying the microbial composition of biofilms formed on dishwasher rubber seals, how diverse abiotic conditions affect microbiota, and which key microbial members were represented in early colonization and contamination of dishwashers, as these appliances can present a source of domestic cross-contamination that leads to broader medical impacts.
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http://dx.doi.org/10.1128/AEM.02755-17DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5812945PMC
March 2018

Bacterial social interactions and the emergence of community-intrinsic properties.

Curr Opin Microbiol 2018 04 1;42:104-109. Epub 2017 Dec 1.

Section of Microbiology, Department of Biology, University of Copenhagen, Denmark. Electronic address:

Bacterial communities are dominated and shaped by social interactions, which facilitate the emergence of properties observed only in the community setting. Such community-intrinsic properties impact not only the phenotypes of cells in a community, but also community composition and function, and are thus likely to affect a potential host. Studying community-intrinsic properties is, therefore, important for furthering our understanding of clinical, applied and environmental microbiology. Here, we provide recent examples of research investigating community-intrinsic properties, focusing mainly on community composition and interactions in multispecies biofilms. We hereby wish to emphasize the importance of studying social interactions in settings where community-intrinsic properties are likely to emerge.
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http://dx.doi.org/10.1016/j.mib.2017.11.018DOI Listing
April 2018

A meta-proteomics approach to study the interspecies interactions affecting microbial biofilm development in a model community.

Sci Rep 2017 11 28;7(1):16483. Epub 2017 Nov 28.

Section of Microbiology, Department of Biology, University of Copenhagen, Copenhagen, Denmark.

Microbial biofilms are omnipresent in nature and relevant to a broad spectrum of industries ranging from bioremediation and food production to biomedical applications. To date little is understood about how multi-species biofilm communities develop and function on a molecular level, due to the complexity of these biological systems. Here we apply a meta-proteomics approach to investigate the mechanisms influencing biofilm formation in a model consortium of four bacterial soil isolates; Stenotrophomonas rhizophila, Xanthomonas retroflexus, Microbacterium oxydans and Paenibacillus amylolyticus. Protein abundances in community and single species biofilms were compared to describe occurring inter-species interactions and the resulting changes in active metabolic pathways. To obtain full taxonomic resolution between closely related species and empower correct protein quantification, we developed a novel pipeline for generating reduced reference proteomes for spectral database searches. Meta-proteomics profiling indicated that community development is dependent on cooperative interactions between community members facilitating cross-feeding on specific amino acids. Opposite regulation patterns of fermentation and nitrogen pathways in Paenibacillus amylolyticus and Xanthomonas retroflexus may, however, indicate that competition for limited resources also affects community development. Overall our results demonstrate the multitude of pathways involved in biofilm formation in mixed communities.
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http://dx.doi.org/10.1038/s41598-017-16633-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5705676PMC
November 2017

Antagonism correlates with metabolic similarity in diverse bacteria.

Proc Natl Acad Sci U S A 2017 10 18;114(40):10684-10688. Epub 2017 Sep 18.

Department of Biology, University of Copenhagen, 2100 Copenhagen Ø, Denmark

In the , Charles R. Darwin [Darwin C (1859) ] proposed that the struggle for existence must be most intense among closely related species by means of their functional similarity. It has been hypothesized that this similarity, which results in resource competition, is the driver of the evolution of antagonism among bacteria. Consequently, antagonism should mostly be prevalent among phylogenetically and metabolically similar species. We tested the hypothesis by screening for antagonism among all possible pairwise interactions between 67 bacterial species from 8 different environments: 2,211 pairs of species and 4,422 interactions. We found a clear association between antagonism and phylogenetic distance, antagonism being most likely among closely related species. We determined two metabolic distances between our strains: one by scoring their growth on various natural carbon sources and the other by creating metabolic networks of predicted genomes. For both metabolic distances, we found that the probability of antagonism increased the more metabolically similar the strains were. Moreover, our results were not compounded by whether the antagonism was between sympatric or allopatric strains. Intriguingly, for each interaction the antagonizing strain was more likely to have a wider metabolic niche than the antagonized strain: that is, larger metabolic networks and growth on more carbon sources. This indicates an association between an antagonistic and a generalist strategy.
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http://dx.doi.org/10.1073/pnas.1706016114DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5635879PMC
October 2017