Transcriptional responses of Streptococcus gordonii and Fusobacterium nucleatum to coaggregation

Abstract

Cell‐cell interactions between genetically distinct bacteria, known as coaggregation, are important for the formation of mixed‐species biofilms such as dental plaque. Interactions lead to gene regulation in the partner organisms that may be critical for adaptation and survival in mixed‐species biofilms. Here, gene regulation responses to coaggregation between Streptococcus gordonii and Fusobacterium nucleatum were studied using dual RNA‐Seq. Initially, S. gordonii was shown to coaggregate strongly with F. nucleatum in buffer or human saliva. Using confocal laser scanning microscopy and transmission electron microscopy, cells of different species were shown to be evenly distributed throughout the coaggregate and were closely associated with one another. This distribution was confirmed by serial block face sectioning scanning electron microscopy, which provided high resolution three‐dimensional images of coaggregates. Cell‐cell sensing responses were analysed 30 minutes after inducing coaggregation in human saliva. By comparison with monocultures, 16 genes were regulated following coaggregation in F. nucleatum whereas 119 genes were regulated in S. gordonii. In both species, genes involved in amino acid and carbohydrate metabolism were strongly affected by coaggregation. In particular, one 8‐gene operon in F. nucleatum encoding sialic acid uptake and catabolism was up‐regulated 2‐ to 5‐fold following coaggregation. In S. gordonii, a gene cluster encoding functions for phosphotransferase system‐mediated uptake of lactose and galactose was down‐regulated up to 3‐fold in response to coaggregation. The genes identified in this study may play key roles in the development of mixed‐species communities and represent potential targets for approaches to control dental plaque accumulation.

Chronic Inflammation as a Link between Periodontitis and Carcinogenesis

“…F. nucleatum plays a central role in the subgingival biofilm, since it physically interacts with other microorganisms in the subgingiva [29]: P. gingivalis [30], Aggregatibacter actinomycetemcomitans [31], Prevotella spp. [32], Streptococcus gordonii [33], Candida albicans [34], and others [29, 35]. Such close interactions with several species in the biofilm are reflected in the fact that F. nucleatum acts as a bridge attaching early colonizers like Streptococcus spp.…”

Identification and localization of proteins associated with the formation of Streptococcus gordonii and Fusobacterium nucleatum biofilms

“…Bio lms are one way they coexist [31,32], and they develop thanks to multiple mechanisms associated with protein expression [33][34][35][36][37]. However, the literature on this subject is still scarce [18,37,38]. In this study, we sought to identify proteins associated with the formation of bio lms and whether these proteins are found in the membranes or in the cytoplasm of F. nucleatum and S. gordonii bio lms.…”

“…The physical attachment between the interacting species is mediated by speci c cellular adhesion proteins in their outer membranes [15]. For example, proteins of the SrtA family that anchor to the cell wall have been identi ed, such as SspA/SspB of S. gordonii, which allow interactions with other streptococci and other oral species, including Porphyromonas gingivalis, Actinomyces, and Candida [16][17][18][19]. Egland et al [20] showed that the SspA/SspB homologue of S. mutans binds to the host's saliva proteins; the host's matrix proteins, including type I collagen, bronectin, laminin, and keratin; and serum components such as brinogen.…”

Transcriptional profiling of coaggregation interactions between Streptococcus gordonii and Veillonella parvula by Dual RNA-Seq

“…Coaggregation has been suggested to play a key role in promoting interactions between different bacteria that lead to profound phenotypic changes in the partner cells that enable them to proliferate in biofilm formation. Previous studies have shown that cell-cell interactions from coaggregation or biofilm formation lead to changes in gene expression in the partner organisms that may be important for adaptation to a community lifestyle 26,28–30 . Here, S. gordonii and V. parvula were shown to form 3-dimensional coaggregate structures with cells of different species relatively evenly spread throughout.…”

“…Recently, Dual RNA-Seq has been used to study transcriptional changes in C. albicans (fungus) and S. gordonii (bacteria) following cell-cell interactions 26,27 . In addition, gene regulation in S. gordonii and Fusobacterium nucleatum has been monitored during coaggregation in human saliva 28 . In this study we performed transcriptome profiling using a Dual RNA-Seq approach to concurrently identify global changes in S. gordonii DL1 and V. parvula PK1910 gene expression following coaggregation.…”