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Decoding the impact of interspecies interactions on biofilm matrix components

ABSTRACT: Multispecies biofilms consist of complex communities where extracellular polymeric substances (EPS) are vital in their structure, adaptability, and function. However, characterizing the components of EPS, particularly glycans and proteins, remains a challenge due to the diverse species and their interactions within the matrix. This study examined how interactions between different species affect EPS components' production and spatial organization. We utilized a consortium of four bacterial soil isolates that have previously demonstrated various intrinsic properties in biofilm communities: Microbacterium oxydans, Paenibacillus amylolyticus, Stenotrophomonas rhizophila, and Xanthomonas retroflexus. We used fluorescence lectin-binding analysis (FLBA) to identify specific glycan components and meta-proteomics to characterize matrix proteins in mono- and multispecies biofilms. Our results revealed diverse glycan structures and compositions, including fucose and different amino sugar-containing polymers, with substantial differences between monospecies and multispecies biofilms. In isolation, M. oxydans produced galactose/N-Acetylgalactosamine network-like structures and influenced the matrix composition in multispecies biofilms. Proteomic analysis revealed flagellin proteins in Xanthomonas and Paenibacillus, particularly in multispecies biofilms. Additionally, surface-layer proteins and a unique peroxidase were found in P. amylolyticus multispecies biofilms, indicating enhanced oxidative stress resistance and structural stability under these conditions. This study highlights the crucial role of interspecies interactions in shaping biofilm matrices and the production of glycans and proteins. These findings deepen our understanding of biofilm complexity and may lead to new approaches for controlling biofilms in various environments.

INSTRUMENT(S): Q Exactive HF

ORGANISM(S): Xanthomonas Retroflexus Paenibacillus Amylolyticus Microbacterium Oxydans Stenotrophomonas Rhizophila

SUBMITTER: Cristina Amador

LAB HEAD: Cristina Amador

PROVIDER: PXD057669 | Pride | 2025-03-31

REPOSITORIES: Pride

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			Action	DRS
	20210217_KMJ_MWN_Cristina_200min_1ug_15cm_01.raw	Raw
	20210217_KMJ_MWN_Cristina_200min_1ug_15cm_02.raw	Raw
	20210217_KMJ_MWN_Cristina_200min_1ug_15cm_03.raw	Raw
	20210217_KMJ_MWN_Cristina_200min_1ug_15cm_04.raw	Raw
	20210217_KMJ_MWN_Cristina_200min_1ug_15cm_05.raw	Raw

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Project description:Polymicrobial biofilms are of large medical importance, but little is known about their physiology and the underlying interspecies interactions. Here we studied two human pathogens, the opportunistic fungus Candida albicans and the caries promoting bacterium Streptococcus mutans. Both species formed biofilms in monoculture, with C. albicans growing mainly in the virulence-associated hyphae form, and S. mutans forming a thick layer of extracellular polymeric substances (EPS). Biofilm growth was enhanced in dual-species biofilms, which reached twice the biomass of monospecies biofilms and higher cell numbers of both S. mutans and C. albicans. EPS production by S. mutans was strongly suppressed in dual-species biofilms. Virulence traits of S. mutans, e.g. genetic competence, biofilm formation and bacteriocin synthesis are controlled by quorum sensing through activation of the alternative sigma factor SigX. SigX is induced by the pheromones CSP (competence stimulating factor) or XIP (sigX inducing peptide). Strong induction of sigX was observed in dual species biofilms indicated by fluorescence of a reporter strain for the sigX promoter, S. mutans PcomX-gfp, as well as by qRT-PCR of comX. The peak of sigX expression occurred after 10 h of biofilm growth. Conditioned media from mixed biofilms but not from C. albicans or S. mutans cultivated alone activated sigX in the reporter strain. Deletion mutants for the comC and comS genes encoding the precursors of CSP and XIP, respectively, were constructed. Conditioned media from mixed biofilms with S. mutans DcomS were unable to induce sigX in the reporter strain, while deletion of comC had no effect. These data show that synthesis of XIP was induced in S. mutans by coculture with C. albicans. Transcriptome analysis of S. mutans in single and mixed biofilms confirmed strong induction of comS, sigX, and the downstream late competence genes in dual-species biofilms. Among the late competence genes, fratricins were discovered for the first time. The comCDE operon and bacteriocin related genes were also induced, but much weaker. Genes related to oxidative stress, chaperones and glycosyltransferase genes required for EPS synthesis from sucrose were down-regulated, while glycogen synthesis genes were up-regulated, indicating that S. mutans was protected from oxidative stress and provided with excess sugar for storage polymer synthesis in mixed biofilms. The data show that in dual-species biofilms, C. albicans improves growth of S. mutans, suppresses its EPS formation and induces the complete quorum sensing signalling system, thus fundamentally changing the virulence properties of the caries pathogen, including its potential interactions with other members of the polymicrobial dental plaque community. Dual-species biofilms of S. mutans and C. albicans and single-species biofilms of S. mutans were cultivated in 24-well microtitre plates in YNBB medium. Transcriptional profiles of S. mutans in single- and dual-species biofilms were analysed at early (6 h) and late (10 h) logarithmic phase of the biofilm growth, as well as after 24 h when biofilms entered stationary phase. Transcriptional profiles of S. mutans grown in the dual-species biofilms were compared to profiles obtained for single-species biofilm from the same time point. Three biological and one to two technical replicas were used in the microarray study. RNA samples were labeled with Cy3 or Cy5 using the ULS fluorescent labeling kit (Kreatech, Germany). Seven hundred nanograms of Cy3 or Cy5 labeled RNA after fragmentation were hybridized to the microarray at 65M-BM-0C for 17 h using the Agilent hybridization chamber according to the manufacturer's instructions. The arrays were scanned using the Agilent DNA microarray scanner and the raw data were extracted using Agilent Feature Extraction software (v. 10.7).

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Decoding the impact of interspecies interactions on biofilm matrix components

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