Protein transport in Archaea: Sec and twin arginine translocation pathways
Introduction
Interactions between the cytoplasm and the extracytoplasmic environment are essential for cellular life. For example, cells must communicate signals across the membrane, take up nutrients and secrete toxins. Moreover, extracytoplasmic proteins, such as polymer-degrading enzymes, or subunits of extracytoplasmic cellular structures, such as flagella and pili, need to be secreted. Thus, all organisms must have the ability to translocate proteins both into and across the hydrophobic membranes that provide the semipermeable barrier to the cytoplasm.
Most proteins traverse the membrane in an unfolded conformation by way of pathways such as the type II, type III or the universally conserved Sec pathway [1, 2, 3]. In addition, many prokaryotes and plant chloroplasts are able to secrete folded proteins across the cytoplasmic and thylakoid membranes, respectively, by way of the twin arginine translocation (Tat) pathway [4, 5].
Most of what is known about protein translocation has been revealed from analyses of the bacterial and eukaryotic translocation pathways. However, more recent studies have also provided information about transport into and across archaeal cytoplasmic membranes. In this review, following brief general overviews, we summarize these data and discuss how these studies have revealed novel aspects of Sec and Tat translocation in all domains of life.
Section snippets
Signal peptides and signal peptidases
The targeting of membrane proteins to the Sec pore involves cytoplasmic recognition of a hydrophobic transmembrane segment (TM) of the protein [6]. Sec substrates that are translocated across the hydrophobic membrane possess amino-terminal signal peptides that resemble a TM, but they also contain a short positively charged amino-terminus and often a signal peptidase recognition site (Figure 1) [7]. Upon cleavage, the substrate is either released from the membrane or anchored to the lipid
Sec-mediated protein translocation
Many Sec substrates are recognized by the signal recognition particle (SRP) by virtue of their TMs or a highly hydrophobic amino-terminal signal peptide as they emerge from translating ribosomes [6, 19]. Subsequent recognition of the SRP–ribosome nascent chain complex by the membrane-associated SRP receptor targets the ribosome nascent chain to the Sec pore where the substrate is translocated co-translationally in a SecA-dependent or -independent manner [6]. SRP-independent substrates are
Translocation and assembly of extracellular protein structures
Bacteria have evolved distinct mechanisms to secrete and to assemble subunits of various extracytoplasmic structures. For example, bacterial flagella subunits are translocated in a Sec-independent manner by way of a specialized type III secretion apparatus, which is located at the base of the flagellum [31]. Newly synthesized flagellins, which lack amino-terminal signal peptides, are transported through the hollow flagellum structure and are incorporated at the distal tip under the filament
Twin arginine translocation
Many of the prokaryotic Tat substrates that were initially identified possessed redox cofactors, which led to the conclusion that the Tat pathway was a specialized export machinery required mainly for secretion of this subset of proteins [4, 8]. However, surprisingly, recent analysis of numerous archaeal and, subsequently, bacterial genomes revealed that the Tat pathway is a general translocation pathway required for secretion of a wide range of substrates [42, 43]. The selective pressure that
Conclusions
Complete genome sequences of ∼25 archaea, representing organisms from all major subgroupings and the extreme environments that they inhabit, are currently available. Increasing interest in the study of these remarkable organisms has also led to significant improvements in the genetic manipulation of several different species, including methanogens, extreme halophiles and hyperthermophiles [46]. Advances in biochemical and genetic approaches should allow complementation of structural work with
Update
The reference cited in the main body of text as K Dilks et al., unpublished, has now been accepted for publication [52].
References and recommended reading
Papers of particular interest, published within the annual period of review, have been highlighted as:
• of special interest
•• of outstanding interest
Acknowledgements
We thank Amy Decatur and members of the Pohlschröder laboratory for critical reading of the manuscript. Support was provided to MP by a grant from the National Science Foundation (reference no. MCB-0239215) and the Department of Energy (reference no. DE-FG02-01ER15169), and to KFJ by a grant from the Natural Sciences and Engineering Research Council of Canada.
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