Molecular trafficking between bacteria determines the shape of gut microbial community

Abstract

Complex inter-bacterial interactions largely influence the structure and function of the gut microbial community. Though several host-associated phenomena have often been shown to be involved in the stability, structure, and function of the gut microbial community, the implication of contact-dependent and contact-independent inter-bacterial interactions has been overlooked. Such interactions are tightly governed at multiple layers through several extracellular organelles, including contact-dependent inhibition (CDI), nanotubes, type VI secretion system (T6SS), and membrane vesicles (MVs). Recent advancements in molecular techniques have revealed that such extracellular organelles function beyond exhibiting competitive behavior and are also involved in manifesting cooperative behaviors. Cooperation between bacteria occurs through the sharing of several beneficial molecules including nucleic acids, proteins, metabolites, and nutrients among the members of the community, while competition occurs by means of multiple toxins. Intrinsic coordination between contact-dependent and contact-independent mechanisms collectively provides a fitness advantage and increased colonization resistance to the gut microbiota, where molecular trafficking plays a key role. This review is intended to provide a comprehensive view of the salient features of the different bacterial interactions and to highlight how microbiota deploy multifaceted organelles, for exerting both cooperative and competitive behaviors. We discuss the current knowledge of bacterial molecular trafficking and its impact on shaping the gut microbial community.

Keywords: Microbiota; contact-dependent interaction; nanotubes; quorum sensing; social behavior.

Figure 1.

Different set of contact-dependent mechanisms of enteric bacteria. (a) Schematic diagram represents how bacteria interact with cooperatives in a contact-dependent manner, where CDI, T6SS and nanotubes provide fitness advantage to bacteria by facilitating cooperative behaviors. Each mechanism plays an imperative role in bacterial survival. (b) Inhibitor cells kill target cells by translocating toxins through CDI, T6SS, nanotubes and T7SS.^, CDI and T6SS mediate interaction between gram-negative bacteria, whereas T7SS mediates interaction between gram-positive bacteria

Figure 2.

Schematic illustration of how enteric bacteria cooperate with neighboring cells in a contact-independent manner. (a) Streptomycin treatment selectively eliminates Firmicutes population in the gut. QS signal AI-2 restores the balance between Bacteroidetes and Firmicutes after antibiotic induced dysbiosis. (b) Microbiota secretes polysaccharide-digestive enzymes in the milieu or through membrane vesicles, which digest the polysaccharides into monosaccharides that can be accessible to other members. (c) Bacteria secrete numerous molecules as a public goods to share with their community members.^,108

Figure 3.

Diagrammatic representation of how microbiota competes with pathogens in a contact-independent manner. (a) Microbiota secretes toxic molecules that affect the growth of the competitors. (b) Colonization of V. cholera in the intestine causes inflammation. (c) Blautia obeum produces AI-2 like molecule that suppresses the QS mechanism of V. cholera. Similarly, (d) B. subtilis restricts the colonization of S. aureus through the production of fengycin that competitively binds with QS receptor AgrC of S. aureus. (e) B. subtilis defective to produce fengycin is not able to restrict colonization of S. aureus.