An Update on Bacterial Secretion Systems: their Substrate Delivery Mechanisms and their Role in Bacterial Physiology and Pathogenesis

About this Research Topic

Background

One essential biological function in prokaryotes is cargo export from the cytoplasm known as secretion. This process involves the delivery of macromolecules across the inner and/or the outer membrane of the bacterial cell and is carried out by dedicated multi-subunit protein nanomachines, referred to as secretion systems. Secretion systems are central regulators in a vast array of physiological and pathophysiological processes such as growth, pathogenesis, competition, conjugation, adhesion, horizontal gene transfer, and motility. To date, nine mechanistically distinct secretion pathways have been described, and recently, a putative tenth pathway was uncovered. These secretion pathways are classified as Type 1 to Type 10 secretion systems (T1SS-T10SS). Cargo secretion can be a single or a multi steps process and can involve a combination of secretion systems. For instance, T3SS, T4SS, and T6SS that transverse both the inner membrane (IM) and the outer membrane (OM) of gram-negative bacteria, translocate substrates in a single-step process; whereas, Sec or Tat systems usually transport cargo substrates across the IM prior to cargo secretion by T5SS and T9SS across the OM.

Secretion of substrates by bacterial secretion systems relies on coordinated gene expression and the correct assembly of multiple structural components into a functional apparatus. In some cases, like in the T4SS of the human pathogen Legionella pneumophila, at least 27 distinct proteins assemble into the secretion apparatus, which is designed to deliver hundreds of diverse protein substrates into the host cell cytosol. Typically, secretion systems include components such as:
(1) secretion ATPases that provide the energy required for transport;
(2) chaperones that mediate between the cargo and the apparatus; and
(3) structural components that form a designated translocation path between the cytosol and the periplasm and between the inner and outer membrane.
Some secretion systems like T3 and T6 systems form a proteinaceous conduit at the surface of the bacterial cell that can engage with the recipient membrane in order to deliver cargo to the neighboring cell cytosol. Substrate recognition, selection, and transport by the secretion system are highly specific and governed by specific signals that lie within the cargo, and cognate recruitment factors. Priming of the apparatus in response to various cues such as contact with nearby membranes or exposure to environmental signals affects the timing of secretion. Substrates could cross a single phospholipid membrane or even four membranes, where two belong to the bacterial donor and two to the bacterial recipient. Uncoordinated expression and assembly, as well as premature and uncontrolled activation of the secretion system, will lead to inefficient substrate transport, with serious negative consequences on bacterial cell survival. Therefore, bacteria have evolved a wide range of strategies to assure optimal secretion by tightly controlling each step in the translocation process. Recent studies employed fluorescence microscopy, Cryo-electron microscopy, and Cryo-electron tomography to image native complexes, to capture the dynamics of secretion system components, and to assist in the elucidation of the steps required for optimal secretion. Despite these advances in our understanding of bacterial secretion systems, there are still many open questions regarding gene expression, assembly, activation, substrate selection, and translocation and their role in bacterial physiology and pathogenesis that need to be addressed.

This Research Topic includes any type of manuscript published in Frontiers in Cellular and Infection Microbiology that covers all aspects of secretion systems functions, structure, assembly, cargo sorting, and delivery. Up-to-date descriptions of each transport system and their putative roles in the life cycle of common bacteria species are welcome.

Keywords: bacterial secretion systems, pathogenesis, bacterial physiology, proteins structure/function, gene expression, assembly, activation, substrate selection and translocation

Important note: All contributions to this Research Topic must be within the scope of the section and journal to which they are submitted, as defined in their mission statements. Frontiers reserves the right to guide an out-of-scope manuscript to a more suitable section or journal at any stage of peer review.

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