Cross-feeding and interkingdom communication in dual-species biofilms of <i>Streptococcus mutans</i> and <i>Candida albicans</i>

Sztajer, Helena; Szafrański, Szymon P.; Tomasch, Jürgen; Reck, Michael; Nimtz, Manfred; Rohde, Manfred; Wagner‐Döbler, Irene

doi:10.1038/ismej.2014.73

Cited by 199 publications

(196 citation statements)

References 69 publications

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“…A total of 141 genes were regulated in the fourspecies biofilm and many of the functions can be related to the interaction with the external milieu and indicate a high phenotypic plasticity in response to the presence of other species (Frias-Lopez and Duran-Pinedo 2012; Sztajer et al, 2014). At least 52 genes were regulated only in the four-species Figure 2 (a) Heatmap of the log2 fold change (LFC) between X. retroflexus gene expression in the single-species biofilm and multispecies biofilms.…”

Section: Discussionmentioning

confidence: 99%

Distinct gene expression profile of Xanthomonas retroflexus engaged in synergistic multispecies biofilm formation

et al. 2016

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It is well known that bacteria often exist in naturally formed multispecies biofilms. Within these biofilms, interspecies interactions seem to have an important role in ecological processes. Little is known about the effects of interspecies interactions on gene expression in these multispecies biofilms. This study presents a comparative gene expression analysis of the Xanthomonas retroflexus transcriptome when grown in a single-species biofilm and in dual-and four-species consortia with Stenotrophomonas rhizophila, Microbacterium oxydans and Paenibacillus amylolyticus. The results revealed complex interdependent interaction patterns in the multispecies biofilms. Many of the regulated functions are related to interactions with the external environment and suggest a high phenotypic plasticity in response to coexistence with other species. Furthermore, the changed expression of genes involved in aromatic and branched-chain amino acid biosynthesis suggests nutrient cross feeding as a contributing factor for the observed synergistic biofilm production when these four species coexists in a biofilm.

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Section: Discussionmentioning

confidence: 99%

Distinct gene expression profile of Xanthomonas retroflexus engaged in synergistic multispecies biofilm formation

et al. 2016

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“…S. gordonii, a pioneer colonizer of dental biofilm, is arginolytic and ADS positive (33), and A. naeslundii is also detected during the early stages of dental biofilm formation (34). Furthermore, S. mutans UA159 and S. gordonii DL1 have been used in multiple laboratories in several in vitro biofilm models, and they are the strain of choice for in vivo (rodent) models of dental caries (35)(36)(37)(38)(39). Finally, these strains are well characterized (both genetically and phenotypically) and standardized, which are critical for the reproducibility of the study.…”

Section: Methodsmentioning

confidence: 99%

l -Arginine Modifies the Exopolysaccharide Matrix and Thwarts Streptococcus mutans Outgrowth within Mixed-Species Oral Biofilms

et al. 2016

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L-Arginine, a ubiquitous amino acid in human saliva, serves as a substrate for alkali production by arginolytic bacteria. Recently, exogenous L-arginine has been shown to enhance the alkalinogenic potential of oral biofilm and destabilize its microbial community, which might help control dental caries. However, L-arginine exposure may inflict additional changes in the biofilm milieu when bacteria are growing under cariogenic conditions. Here, we investigated how exogenous L-arginine modulates biofilm development using a mixed-species model containing both cariogenic (Streptococcus mutans) and arginolytic (Streptococcus gordonii) bacteria in the presence of sucrose. We observed that 1.5% (wt/vol) L-arginine (also a clinically effective concentration) exposure suppressed the outgrowth of S. mutans, favored S. gordonii dominance, and maintained Actinomyces naeslundii growth within biofilms (versus vehicle control). In parallel, topical L-arginine treatments substantially reduced the amounts of insoluble exopolysaccharides (EPS) by >3-fold, which significantly altered the three-dimensional (3D) architecture of the biofilm. Intriguingly, L-arginine repressed S. mutans genes associated with insoluble EPS (gtfB) and bacteriocin (SMU.150) production, while spxB expression (H 2 O 2 production) by S. gordonii increased sharply during biofilm development, which resulted in higher H 2 O 2 levels in arginine-treated biofilms. These modifications resulted in a markedly defective EPS matrix and areas devoid of any bacterial clusters (microcolonies) on the apatitic surface, while the in situ pH values at the biofilm-apatite interface were nearly one unit higher in arginine-treated biofilms (versus the vehicle control). Our data reveal new biological properties of L-arginine that impact biofilm matrix assembly and the dynamic microbial interactions associated with pathogenic biofilm development, indicating the multiaction potency of this promising biofilm disruptor. IMPORTANCEDental caries is one of the most prevalent and costly infectious diseases worldwide, caused by a biofilm formed on tooth surfaces. Novel strategies that compromise the ability of virulent species to assemble and maintain pathogenic biofilms could be an effective alternative to conventional antimicrobials that indiscriminately kill other oral species, including commensal bacteria. L-Arginine at 1.5% has been shown to be clinically effective in modulating cariogenic biofilms via alkali production by arginolytic bacteria. Using a mixed-species ecological model, we show new mechanisms by which L-arginine disrupts the process of biofilm matrix assembly and the dynamic microbial interactions that are associated with cariogenic biofilm development, without impacting the bacterial viability. These results may aid in the development of enhanced methods to control biofilms using L-arginine. Biofilms formed on surfaces are highly organized and structured microbial communities enmeshed in an extracellular matrix composed of polymeric substances, such as exopoly...

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“…Primers specific for the 18 S rRNA gene of C. albicans were used (18S-F GGATT-TACTGAAGACTAACTACTG, 18S-R GAACAA-CAACCGATCCCTAGT), with an annealing temperature of 59 C. The amplification protocol and genome equivalent calculations were described in detail elsewhere. 48 Briefly, the qPCR was performed using the thermocycling instructions recommended for the SYBR green PCR Master Mix (95 C for 30 s and 40 cycles of 30 s at 95 C and 30 s at 59 C). Since the organism has variable numbers of 18S rRNA gene copies per genome, 49 genome equivalents (or fungal biomass) were calculated based on standard curves obtained after amplifying 10-fold serial dilutions of fungal DNA isolated from overnight 37 C YPD broth cultures (strain SC5314).…”

Section: Dna Extraction and Candida Quantification By Qpcrmentioning

confidence: 99%

S. oralis activates the Efg1 filamentation pathway in C. albicans to promote cross-kingdom interactions and mucosal biofilms

Sobue

Bertolini

et al. 2017

Virulence

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Candida albicans and Streptococcus oralis are ubiquitous oral commensal organisms. Under hostpermissive conditions these organisms can form hypervirulent mucosal biofilms. C. albicans biofilm formation is controlled by 6 master transcriptional regulators: Bcr1, Brg1, Efg1, Tec1, Ndt80, and Rob1. The objective of this work was to test whether any of these regulators play a role in crosskingdom interactions between C. albicans and S. oralis in oral mucosal biofilms, and identify downstream target gene(s) that promote these interactions. Organotypic mucosal constructs and a mouse model of oropharyngeal infection were used to analyze mucosal biofilm growth and fungal gene expression. By screening 6 C. albicans transcription regulator reporter strains we discovered that EFG1 was strongly activated by interaction with S. oralis in late biofilm growth stages. EFG1 gene expression was increased in polymicrobial biofilms on abiotic surfaces, mucosal constructs and tongue tissues of mice infected with both organisms. EFG1 was required for robust Candidastreptococcal biofilm growth in organotypic constructs and mouse oral tissues. S. oralis stimulated C. albicans ALS1 gene expression in an EFG1-dependent manner, and Als1 was identified as a downstream effector of the Efg1 pathway which promoted C. albicans-S. oralis coaggregation interactions in mixed biofilms. We conclude that S. oralis induces an increase in EFG1 expression in C. albicans in late biofilm stages. This in turn increases expression of ALS1, which promotes coaggregation interactions and mucosal biofilm growth. Our work provides novel insights on C. albicans genes which play a role in cross-kingdom interactions with S. oralis in mucosal biofilms.

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Cross-feeding and interkingdom communication in dual-species biofilms of Streptococcus mutans and Candida albicans

Cited by 199 publications

References 69 publications

Distinct gene expression profile of Xanthomonas retroflexus engaged in synergistic multispecies biofilm formation

Distinct gene expression profile of Xanthomonas retroflexus engaged in synergistic multispecies biofilm formation

l -Arginine Modifies the Exopolysaccharide Matrix and Thwarts Streptococcus mutans Outgrowth within Mixed-Species Oral Biofilms

S. oralis activates the Efg1 filamentation pathway in C. albicans to promote cross-kingdom interactions and mucosal biofilms

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