Identification of Veillonella parvula and Streptococcus gordonii adhesins mediating co-aggregation and its impact on physiology and mixed biofilm structure

Abstract

ABSTRACT The dental plaque is a polymicrobial community where biofilm formation and co-aggregation, the ability to bind to other bacteria, play a major role in the construction of an organized consortium. One of its prominent members is the anaerobic diderm Veillonella parvula, considered a bridging species, which growth depends on lactate produced by oral streptococci. Understanding how V. parvula co-aggregates and the impact of aggregation has long been hampered due to the lack of appropriate genetic tools. Here we studied co-aggregation of the naturally competent strain V. parvula SKV38 with various oral bacteria and its effect on cell physiology. We show that V. parvula requires different trimeric autotransporters of the type V secretion system to adhere to oral streptococci and actinomyces. In addition, we describe a novel adhesin of Streptococcus gordonii, VisA (SGO_2004), as the protein responsible for co-aggregation with V. parvula. Finally, we show that co-aggregation does not impact cell-cell communication, which is mainly driven by environmental sensing, but plays an important role in the architecture and species distribution within the biofilm.IMPORTANCEOur research explores the mechanisms of bacterial adhesion within the dental plaque, focusing on Veillonella parvula, a key player in the oral microbiome. Dependent on lactate from streptococci, V. parvula plays a crucial bridging role in the formation of dental biofilms by co-aggregating with other bacteria. Despite its importance, the understanding of the underlying mechanisms of co-aggregation remains limited. Our study shows that V. parvula uses different trimeric autotransporters to adhere to oral Streptococci and Actinomyces. We additionally identify a novel adhesin from S. gordonii, VisA (SGO_2004) facilitating this interaction. We found that although co-aggregation does not affect cell-cell communication, it is critical for biofilm structure and species distribution. This research opens up new avenues for exploring microbial interactions in dental health and diseases.

Keywords

• Veillonella
• Streptococcus
• adhesin
• co-aggregation
• trimeric autotransporter
• dental plaque