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Bacterial conjugation has long served as a model system for developing a mechanistic understanding of how nucleic acids translocate across biological membranes. Early studies of the Escherichia coli F-plasmid conjugation system led to the view that conjugation is a contact-dependent process which, at least among the gram-negative bacteria, requires two cell surface structures in the donor cell that are probably joined. One structure is an extracellular filament termed the sex pilus for initiating the physical coupling of donor and recipient cells. The second is a DNA conductance channel or conjugal pore for transmission of DNA substrates across the donor cell envelope (34, 46). Classically, conjugation systems have been considered to operate on principles that are mechanistically quite different from systems dedicated to protein transport. However, recent studies have identified at least three similarities among conjugation and protein transport processes. First, sequence-based studies have identified homologies among subunits of a variety of eubacterial transport systems, including those dedicated to DNA transfer, selective protein secretion, assembly of type IV fimbriae and flagella, and extrusion of filamentous phage (44). Second, there is an accumulating body of experimental evidence supporting the notion that the conjugal transfer of DNA proceeds via recognition of sequences or motifs associated not with the DNA per se but with proteins bound to the DNA (34 and this minireview). Finally, some members of the type III protein secretion family (see below) recently identified in bacterial pathogens of plants and humans directly “inject” protein substrates into eukaryotic cells by a process requiring cell contact and, in some cases, the elaboration of extracellular filaments; in principle these structures could functionally resemble conjugative sex pili (39, 64). This minireview will focus on recent investigations of the Agrobacterium tumefaciens transport system responsible for delivery of oncogenic DNA (T-complex) across the bacterial envelope. The T-complex transporter belongs to a growing family of transporters whose subunits share extensive sequence similarities. For the present, this secretion family is referred to as a type IV secretion system, as originally proposed by Salmond (72). This classification distinguishes the type IV secretion system from other dedicated secretion pathways, including the type I secretion system exemplified by E. coli hemolysin export, the type II secretion system exemplified by Klebsiella oxytoca pullulanase export, and the type III secretion system exemplified by Yersinia pestis Yop export (for detailed information about these protein export systems, see references 30, 39, 68, and 72). However, as illustrated above, a taxonomic classification based on sequence similarities of transporter subunits is likely to prove obsolete as additional structural or functional similarities are identified among various macromolecular transport systems. By definition, members of the type IV system involved in conjugation transmit DNA to recipient cells by a contact-dependent process. Beyond requiring cell-to-cell contact, however, until very recently almost nothing was known about the biochemical reactions that govern the processing of DNA into a transfer-competent substrate or the transmission of substrate from donor to recipient cells. The first aim of this minireview is to highlight recent work demonstrating sequence and functional similarities between the T-complex transport system and related conjugation and protein export systems. The second aim is to summarize new results from structural studies that define, for the first time, early stages in the assembly of a bacterial conjugation apparatus.

Agrobacterium tumefaciens T-complex transport apparatus: a paradigm for a new family of multifunctional transporters in eubacteria