Dataset Information

Proteomics of Streptococcus gordonii within a model developing oral microbial community.

ABSTRACT: Streptococcus gordonii is one of several species that can initiate the formation of oral biofilms that develop into the complex multispecies microbial communities referred to as dental plaque. It is in the context of dental plaque that periodontal pathogens such as Porphyromonas gingivalis cause disease. We have previously reported a whole cell quantitative proteomics investigation of P. gingivalis in a model dental plaque community of S. gordonii, P. gingivalis, and Fusobacterium nucleatum. Here we report the adaptation of S. gordonii to the same model.1122?S. gordonii proteins were detected in S. gordonii control samples, 915 in communities with F. nucleatum, 849 with P. gingivalis, and 649 with all three organisms. Quantitative comparisons showed extensive proteome changes in association with F. nucleatum or P. gingivalis individually or both P. gingivalis and F. nucleatum together. The changes were species specific, though the P. gingivalis interaction may be dominant, indicated by large differences between the proteomes with F. nucleatum or P. gingivalis but limited changes between communities with P. gingivalis or both P. gingivalis and F. nucleatum. The results were inspected manually and an ontology analysis conducted using DAVID. Extensive changes were seen in nutrition pathways with increases in energy metabolism and changes in the resulting byproducts, while the acid and sugar repressed PTS (phosphoenolpyruvate dependent phosphotransferase system) sugar transport systems showed decreases. These results were seen across all the multispecies samples, though with different profiles according to the partner species. F. nucleatum association decreased proteins for the metabolic end products acetate and ethanol but increased lactate, the primary source of acidity from streptococcal cultures. P. gingivalis containing samples had a reduction in levels of proteins for ethanol and formate but increased proteins for both acetate and lactate production. The communities also showed increases in exopolysaccharide synthesis, amino acid biosynthesis, and oxidative stress protection and decreases in adhesion and transporter proteins.This study showed that S. gordonii demonstrates species specific responses during interactions with F. nucleatum or P. gingivalis. Extensive changes were seen in energy metabolism and byproduct production implicating nutrient transfer as an important community interaction.

SUBMITTER: Hendrickson EL

PROVIDER: S-EPMC3534352 | biostudies-literature | 2012 Sep

REPOSITORIES: biostudies-literature

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Proteomics of Streptococcus gordonii within a model developing oral microbial community.

Hendrickson Erik L EL Wang Tiansong T Dickinson Brittany C BC Whitmore Sarah E SE Wright Christopher J CJ Lamont Richard J RJ Hackett Murray M

BMC microbiology 20120918

<h4>Background</h4>Streptococcus gordonii is one of several species that can initiate the formation of oral biofilms that develop into the complex multispecies microbial communities referred to as dental plaque. It is in the context of dental plaque that periodontal pathogens such as Porphyromonas gingivalis cause disease. We have previously reported a whole cell quantitative proteomics investigation of P. gingivalis in a model dental plaque community of S. gordonii, P. gingivalis, and Fusobacte ...[more]

PMID: 22989070

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Project description:Fusobacterium nucleatum is a common oral organism that can provide adhesive and metabolic support to developing periodontal bacterial communities. It is within the context of these communities that disease occurs. We have previously reported whole cell proteomics analyses of Porphyromonas gingivalis and Streptococcus gordonii in early-stage communities with each other and with F. nucleatum, modeled using 18 h pellets. Here, we report the adaptation of F. nucleatum to the same experimental conditions as measured by differential protein expression. About 1210 F. nucleatum proteins were detected in single species F. nucleatum control samples, 1192 in communities with P. gingivalis, 1224 with S. gordonii, and 1135 with all three species. Quantitative comparisons among the proteomes revealed important changes in all mixed samples with distinct responses to P. gingivalis or S. gordonii alone and in combination. The results were inspected manually and an ontology analysis conducted using DAVID (Database for annotation, visualization, and integrated discovery). Extensive changes were detected in energy metabolism. All multispecies comparisons showed reductions in amino acid fermentation and a shift toward butanoate as a metabolic byproduct, although the two organism model community with S. gordonii showed increases in alanine, threonine, methionine, and cysteine pathways, and in the three species samples there were increases in lysine and methionine. The communities with P. gingivalis or all three organisms showed reduced glycolysis proteins, but F. nucleatum paired with S. gordonii displayed increased glycolysis/gluconeogenesis proteins. The S. gordonii containing two organism model also showed increases in the ethanolamine pathway while the three species sample showed decreases relative to the F. nucleatum single organism control. All of the nascent model communities displayed reduced translation, lipopolysaccharide, and cell wall biosynthesis, DNA replication and DNA repair.

Project description:Extracellular DNA (eDNA) is an important component of biofilm matrix that serves to maintain biofilm structural integrity, promotes genetic exchange within the biofilm, and provides protection against antimicrobial compounds. Advances in microscopy techniques have provided evidence of the cobweb- or lattice-like structures of eDNA within biofilms from a range of environmental niches. However, methods to reliably assess the abundance and architecture of eDNA remain lacking. This study aimed to address this gap by development of a novel, high-throughput image acquisition and analysis platform for assessment of eDNA networks in situ within biofilms. Utilizing Streptococcus gordonii as the model, the capacity for this imaging system to reliably detect eDNA networks and monitor changes in abundance and architecture (e.g., strand length and branch number) was verified. Evidence was provided of a synergy between glucans and eDNA matrices, while it was revealed that surface-bound nuclease SsnA could modify these eDNA structures under conditions permissive for enzymatic activity. Moreover, cross talk between the competence and hexaheptapeptide permease systems was shown to regulate eDNA release by S. gordonii. This novel imaging system can be applied across the wider field of biofilm research, with potential to significantly advance interrogation of the mechanisms by which the eDNA network architecture develops, how it can influence biofilm properties, and how it may be targeted for therapeutic benefit. IMPORTANCE Extracellular DNA (eDNA) is critical for maintaining the structural integrity of many microbial biofilms, making it an attractive target for the management of biofilms. However, our knowledge and targeting of eDNA are currently hindered by a lack of tools for the quantitative assessment of eDNA networks within biofilms. Here, we demonstrate use of a novel image acquisition and analysis platform with the capacity to reliably monitor the abundance and architecture of eDNA networks. Application of this tool to Streptococcus gordonii biofilms has provided new insights into how eDNA networks are stabilized within the biofilm and the pathways that can regulate eDNA release. This highlights how exploitation of this novel imaging system across the wider field of biofilm research has potential to significantly advance interrogation of the mechanisms by which the eDNA network architecture develops, how it can influence biofilm properties, and how it may be targeted for therapeutic benefit.

Dataset Information

Proteomics of Streptococcus gordonii within a model developing oral microbial community.

Publications

Proteomics of Streptococcus gordonii within a model developing oral microbial community.

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