Shuffling genes around in hot environments: the unique DNA transporter ofThermus thermophilus

Abstract

Natural transformation permits the transport of DNA through bacterial membranes and represents a dominant mode for the transfer of genetic information between bacteria and between microorganisms of distant evolutionary lineages and even between members of different domains. This phenomenon, known as horizontal, or lateral, gene transfer, has been a major force for genome plasticity over evolutionary history, and is largely responsible for the spread of fitness-enhancing traits, including antibiotic resistance and virulence factors. In particular, for adaptation of prokaryotes to extreme environments, lateral gene transfer seems to have played a crucial role. Here, we present a survey of the natural transformation machinery of the thermophile Thermus thermophilus HB27. A tentative model of the transformation machinery comprising of components similar to proteins of type IV pili and type II secretion systems is presented. A comparative discussion of the subunits and the structure of the DNA translocator and the underlying mechanism of transfer of free DNA in T. thermophilus highlights conserved and unique features of the DNA translocator in T. thermophilus. We hypothesize that the extraordinary broad substrate specificity and the high efficiency of the T. thermophilus DNA uptake system is of major importance for thermoadaptation and interdomain DNA transfer in hot environments.

DNA-uptake machinery of naturally competent Vibrio cholerae

“…4). The model combines data from this work with those of studies of other transformable bacteria and their Tfp and presents evidence for several important mechanisms that have not been previously addressed experimentally (6)(7)(8)(25)(26)(27)(28)(29)(30)(31). In the center of the model is a Tfp appendage with PilA as the major pilin subunit (as demonstrated in Fig.…”

Unusual N-terminal ααβαββα Fold of PilQ from Thermus thermophilus Mediates Ring Formation and Is Essential for Piliation

“…Former T. thermophilus mutant studies suggested an involvement of pilus structures in DNA uptake across the membranes because proteins essential for biogenesis of T4P, such as the inner membrane proteins PilC, PilD (prepilin peptidase), and PilF (AAA ATPase) or the pilin PilA4, are also essential for transformation (6,15). Furthermore, pilD, pilF, or pilA4 mutants exhibited an increased DNA binding compared with the wild type, which suggested an involvement of these pilus proteins in DNA uptake across the outer membrane (20).…”

“…of Molecular Biosciences, Goethe University, Frankfurt/Main, Max-von-Laue-Strasse 9, D-60438 Frankfurt, Germany. locator proteins to components of T4P and the type II protein secretion system raised the question of a functional linkage of both systems, which was unraveled by mutant studies (6,14,15). However, the question whether pili themselves are implicated in DNA uptake has not been answered to date.…”

“…DNA is bound to the secretin complex in the outer membrane, which guides the DNA translocator shaft composed of pilins through the outer membrane. The DNA transport might require dynamics of the DNA translocating shaft, which could be powered by the AAA ATPase PilF (6,(13)(14)(15). The similarities of the T. thermophilus DNA trans-* The work was supported by Deutsche Forschungsgemeinschaft Grant AV9/6-1.…”

“…Natural transformation in bacteria, which describes the uptake and incorporation of naked DNA, allows the uptake of genetic material from diverse bacterial species and even members of different domains and is perhaps the most versatile mechanism of DNA transfer (2,3). Natural transformation machineries are complex DNA translocators found in many bacteria, including bacteria thriving under extreme conditions (2,(5)(6)(7)(8).…”