Biological Diversity and Evolution of Type IV Secretion Systems

Abstract

The bacterial type IV secretion systems (T4SSs) are a highly functionally and structurally diverse superfamily of secretion systems found in many species of gram-negative and -positive bacteria. Collectively, the T4SSs can translocate DNA and monomeric and multimeric protein substrates to a variety of bacterial and eukaryotic cell types. Detailed phylogenomics analyses have established that the T4SSs evolved from ancient conjugation machines whose original functions were to disseminate mobile DNA elements within and between bacterial species. How members of the T4SS superfamily evolved to recognize and translocate specific substrate repertoires to prokaryotic or eukaryotic target cells is a fascinating question from evolutionary, biological, and structural perspectives. In this chapter, we will summarize recent findings that have shaped our current view of the biological diversity of the T4SSs. We focus mainly on two subtypes, designated as the types IVA (T4ASS) and IVB (T4BSS) systems that respectively are represented by the paradigmatic Agrobacterium tumefaciens VirB/VirD4 and Legionella pneumophila Dot/Icm T4SSs. We present current information about the composition and architectures of these representative systems. We also describe how these and a few related T4ASS and T4BSS members evolved as specialized nanomachines through acquisition of novel domains or subunits, a process that ultimately generated extensive genetic and structural mosaicism among this secretion superfamily. Finally, we present new phylogenomics information establishing that the T4BSSs are much more broadly distributed than initially envisioned.

Type IV Coupling Proteins as Potential Targets to Control the Dissemination of Antibiotic Resistance

“…Type IV secretion systems (T4SS) are macromolecular assemblies that can transport DNA and/or proteins (Christie, 2016). This broad superfamily, in terms of function and structure, of macromolecular complexes can be found in both Gram-negative and Gram-positive bacteria (Christie et al, 2017). Different classifications, based on different criteria, have been proposed for T4SSs (Table 1).…”

“…In any case, some T4SS, such as the one present in Agrobacterium tumefaciens, show a dual nature (Li and Christie, 2018). The second classification is based on the protein components (Christie et al, 2017;Grohmann et al, 2018). In this case, T4SS are similarly divided into two groups: type IV A (T4ASS) and type IV B (T4BSS), whose paradigmatic systems are the VirB/VirD system of A. tumefaciens and the Dot/Icm system of Legionella pneumophila, respectively.…”

The all-intracellular order Legionellales is unexpectedly diverse, globally distributed and lowly abundant

“…Despite their very broad ecological range, Legionellales have significant common characters: they replicate and multiply inside eukaryotic hosts, using a type IVB secretion system (T4BSS). This system, also known as Icm/Dot (intracellular multiplication / defect in organelle trafficking genes), is used to inject effector proteins inside the host (Nagai and Kubori 2011 ; Christie, Gomez Valero and Buchrieser 2017 ). This virulence trait is key to avoid lysosomal degradation and to replicate inside intracellular compartments (Richards et al .…”

1H, 13C, 15N resonance assignment of the C-terminal domain of the bifunctional enzyme TraI of plasmid R1

“…This transfer is important for bacteria to adapt and evolve in variable environments. Transfer of DNA also takes place between the bacterial and eukaryotic communities (Christie et al 2017 ; Ilangovan et al 2015 ).The most studied conjugation system in Gram-negative bacteria is the F family of plasmids, which includes F, R1 and pED 208. The protein investigated in this work, TraI, is encoded by the R1 plasmid.…”