149

8
CHAPTER

INTRODUCTION TO BACTERIAL
ABC PROTEINS
I. BARRY HOLLAND

In Chapter 1 in this volume, E. Dassa has
reviewed the classification of ABC proteins,
including prokaryote representatives and their
transport substrates in the many cases where
these have been identified. Previous general
reviews have also discussed the ABC proteins
in Escherichia coli (Linton and Higgins, 1998),
Bacillus subtilis (Quentin et al., 1999) and
Mycobacterium tuberculosis (Braibant et al., 2000)
and more specifically concerning bacterial
ABC exporters in E. coli (Fath and Kolter, 1993;
Young and Holland, 1999). The purpose of
this introductory chapter is therefore briefly to
highlight some of the major characteristics of
bacterial ABC systems and the breadth of their
functions.

NATURE AND
COMPOSITION OF THE
ABC TRANSPORTER
Prokaryote ABC-dependent transport systems,
whether exporters or importers, all adhere to

the usual formula of a basic four-unit structure,
two membrane components and two units of
ABC-ATPases. The membrane components and
the ABCs may be identical or non-identical and
can be fused pairwise in different combinations
as shown in Chapter 1, although unlike those
commonly found in eukaryotes no examples
of all four subunits fused together have been

ABC Proteins: From Bacteria to Man
ISBN 0-12-352551-9

identified in prokaryotes. In describing ABCdependent transport systems, it is important to
emphasize that the term ABC (ATP-binding
cassette, Hyde et al., 1990) is synonymous with
ABC-ATPase, whether present as a subdomain
or an independent polypeptide. The term ABC
transporter, on the other hand, describes the
ABC-ATPase (also called a traffic ATPase; Ames
and Lecar, 1992) plus its associated integral
membrane domains, whether fused to the ABC
or separately encoded. This core transporter or
translocation complex may be further supplemented with essential accessory or auxiliary
subunits (usually encoded separately): the
external ligand-binding protein in the case of
ABC importers, or the MFP (membrane fusion
protein) and the OMP-F (outer membrane protein/factor) or OMA (outer membrane auxiliary) integral to the inner membrane and outer
membrane, respectively. In the case of ABC
transporters, the whole complex may sometimes be referred to as the translocon, whilst for
the importers, the term permease is also used to

describe the entire complex.
Whilst ATP is the substrate for the ABCATPase, the molecule or ion being transported
by the ABC transporter is variously described
as a substrate or a transport substrate or an
allocrite. Since in our view, in the vast majority
of cases, the component being transported
remains unmodified by the process, the term
‘substrate’ is inappropriate, and we prefer allocrite, a term we coined, loosely derived from
the Greek meaning a substance transported or

Copyright 2003 Elsevier Science Ltd
All rights of reproduction in any form reserved


150

ABC PROTEINS: FROM BACTERIA TO MAN

exported (Blight and Holland, 1990; Young and
Holland, 1999).

AN ABUNDANCE OF
DIFFERENT TYPES OF
ABC PROTEINS IN
PROKARYOTES
Probably the earliest detailed studies of ABC
proteins were carried out in bacteria in the
1970s and 1980s, concerning the mechanism of
uptake of solutes such as histidine and maltose,
mediated by the ABC proteins, HisP (Ames and

Nikaido, 1978) and MalK (Bavoil et al., 1980) in
Salmonella typhimurium and E. coli, respectively.
These proteins were initially recognized as
binding ATP and subsequently as energy
generators for transport (Hobson et al., 1984;
Shuman and Silhavy, 1981), through the hydrolysis of ATP. As seen in Chapter 9, although we
still have much to learn concerning the mechanism of transport driven by, for example, HisP
and MalK, structural and genetic studies of the
importing ABCs continue to be the most
advanced.
ABC-ATPases are now recognized as one of
the major superfamilies of proteins, represented
in all three kingdoms of life and found in all
organisms so far analyzed. ABC proteins are
particularly abundant in prokaryotes, with
genes constituting from close to 1% and up to
more than 3% amongst the 19 eubacteria and
6 archaea, respectively, surveyed in Chapter 1.
The very recent sequence of the Agrobacterium
tumefaciens genome describes the highest number recorded so far, 153, excluding orphan ABCs
(with no discernible membrane domain associates). Thus, ABC transporters constitute 60% of
all transporters and about 3% of all predicted
polypeptides in the A. tumefaciens genome
(Goodner et al., 2001; Wood et al., 2001). All the
known bacterial genomes, with one exception,
Treponema pallidum (only 1.14 Mb), encode all the
three main categories of ABC protein discussed
below, the exporters, orphans and importers.
Curiously, T. pallidum and four out of the six
archaeal genomes listed in Chapter 1, apparently

do not encode any exporters.
In Chapter 1, based on cluster or phylogeny
analysis of sequences constituting the ABC
polypeptides, over 600 examples out of the more
than 2000 entries in the current databases, 33

distinct clusters were identified. These are
assigned so far to three major classes, all strongly
represented in bacteria. Class 1 contains the large
family of exporters. Class 2 is a small family of
orphans, with no known membrane protein
associates and, at least in some cases, with no
connection to membrane transport processes, for
example the bacterial UvrA protein essential for
specific DNA repair processes. Class 3 is functionally probably a more heterogeneous family,
since it probably contains both importers and
exporters. This heterogeneity may necessitate a
future separation into at least two distinct
classes.

AN ADDITIONAL CLASS
OF BACTERIAL ABCS
INVOLVED IN DNA
RECOMBINATION AND
REPAIR
Importantly, an additional important group of
ABC proteins present in both bacteria and
eukaryotes, which are not involved in transport but concerned with DNA repair or recombination, have yet to be classified as class 1, 2
or 3 and may well constitute a completely new
class. Such an example, the ABC domain of

Rad50 from Pyrococcus furiosus, involved in
homologous recombination, has recently been
crystallized and the structure determined
(Hopfner et al., 2000). The ABC domain contains the two characteristic lobes or arms found
in HisP (Hung et al., 1998). This contains all the
expected, highly conserved motifs, the Walker
A, Q-loop, Walker B and the downstream
histidine (Linton and Higgins, 1998), present
in Arm-I, the RecA-like, catalytic domain
(Geourjon et al., 2001). Similarly, Rad50 contains the signature motif in the smaller Arm-II,
sometimes referred to as the helical (Ames and
Lecar, 1992) or signaling/regulatory domain
(Holland and Blight, 1999). In reality, in the
intact Rad50 molecule, the helical or signaling
domain is interrupted by the insertion into
helix 3 of 600 residues forming a long coiled
coil region, thereby separating the Walker A
from the Walker B domain. Interestingly, as
discussed in Chapter 11, structural studies so
far indicate that functionally different types
of ABC protein display the greatest variation in


INTRODUCTION TO BACTERIAL ABC PROTEINS

structural organization in the helical domain,
frequently affecting helix 3.
The extensive coiled coil region of Rad50,
facilitating dimerization of these large molecules, restoring the close proximity of the
Walker A and B motifs for nucleotide binding,

is in fact diagnostic of a large family of bacterial
and eukaryote SMC (structural maintenance
of chromosome) proteins (Melby et al., 1998;
Soppa, 2001), many of which are involved in
condensation of DNA, including the SMC protein in B. subtilis required for chromosomal
segregation (Graumann et al., 1998). Notably,
whereas Rad50 has a relatively well-conserved
LSGG motif compared with the ‘classical’ ABC
proteins, other SMCs have a more ‘degenerate’
version of this signature motif. Finally, perhaps
the most distant relatives, but still considered
as ABC proteins (Aravind et al., 1999), are the
DNA repair enzymes such as the bacterial
MutS. These proteins contain minimal Walker
A and B motifs and have the same overall fold
for the catalytic domain as HisP (Lamers et al.,
2000), but the signature motif is significantly
diverged from that of HisP, and indeed much
of the region equivalent to the helical domain
of HisP is absent (Geourjon et al., 2001).

EXPORTERS
Class 1 ABC-ATPases (fused to a membrane
domain), and apparently some class 3 proteins
(encoded independently from the membrane
domain), constitute at least eight distinct families, all concerned with the export of a wide
range of compounds. These include extremely
large polypeptides, greater than 400 kDa in
some cases (Chapter 11), polysaccharides, a
wide variety of antibiotics, many drugs

(Chapter 12), and certain lipids (Chapter 7). A
fascinating adaptation of the modular structure
of an ABC protein is shown in the ABC component of the translocators for non-lantibiotics
secreted by Gram-positive bacteria. In these
cases the N-terminal domain of the ABC transporter carries a cytoplasmic extension to the
membrane domain (Havarstein et al., 1995),
which constitutes a cysteine protease, necessary
for processing the antibiotic peptide as it exits
from the cell (see Chapter 11). Some evidence
suggests that class 1 ABCs are also involved
in exporting fatty acids and Naϩ ions as transport substrates or allocrites. As reviewed in
Chapter 1, however, firm evidence for the identity of allocrites in many cases is still lacking.

Importantly, whilst inferences regarding potential allocrites for class 1 transporters can be
drawn from cluster analysis through guilt by
association with well-characterized transporters, this approach is not necessarily reliable.
One of the largest exporter families, DPL (see
Chapter 1), contains at least 11 subfamilies of
bacterial ABCs, which are involved in the export
of allocrites as diverse as lipids, large polypeptides, or a wide range of drugs. Of course, we
cannot rule out the possibility that some of these
transporters export in reality more than one
type of compound, as has been demonstrated
for Pgp (Johnstone et al., 2000; Raymond et al.,
1992). As a further complication, the ABC transporters in the Prt and Hly clusters in the heterogeneous DPL family require additional, specific
auxiliary membrane proteins in order to complete, if not provide, the actual translocation
pathway (Chapter 11).
Interestingly, from knowledge that is available so far, the bacterial exporters appear to fulfill a variety of important cellular functions, for
example the secretion of factors required for
dominating other bacterial species in the environment, for colonization of plant, insect or

animal hosts leading to pathogenic infection or
symbiosis, for the removal of toxic compounds
and for the biogenesis of several constituents
of the organism’s own cellular envelope. Many
of the latter are essential for respiratory functions, the integrity of the bilayer, simple surface
protection and even movement of the bacteria.
Moreover, some ABC exporters have been implicated in various developmental and differentiation programs, although their precise roles
and allocrites transported in these cases are
mostly obscure. For further information and literature sources on several of these aspects, see
other chapters in Parts I and II in this volume.

CLASS 2,
ORPHAN ABCS
The class 2 group of ABC proteins are present in
all organisms but are curious exceptions to the
rule that the ABC proteins are always involved
in transport processes across membranes. The
functions of these proteins as a group are quite
diverse and surprising, being involved in translation of polypeptides, drug and antibiotic resistance, and in DNA repair, although only the latter
two have been documented in bacteria so far
(Chapter 1). It is intriguing to know what

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ABC PROTEINS: FROM BACTERIA TO MAN

common principles might govern the action of

a highly conserved ABC domain involved in
processes as different as membrane transport,
DNA repair and protein synthesis. Interestingly,
in the bacterial UvrA protein, a tandemly duplicated ABC, there is an insertion of a DNA binding motif, a zinc finger, between the Walker A
and the signature motif in each ABC domain
(see, for example, Husain et al., 1986; Yamamoto
et al., 1996). This insertion occurs in a position
close to the equivalent of the interface between
the two lobes in the HisP structure, which presumably must affect the regulation of UvrA
function. As a further curiosity, if not a mystery,
ABCs in this group of class 2 orphans include
proteins, also with duplicated ABC domains,
from, for example, Staphylococcus aureus and
Streptomyces antibioticus (Mendez and Salas,
2001; Ross et al., 1995), responsible for resistance
(and immunity in some cases) to certain drugs
and antibiotics. The simplest explanation would
be that these ABCs do work in conjunction with
some membrane protein to export the drugs but,
despite intensive efforts, such proteins have not
yet been identified.

IMPORTERS
The class 3 ABC transporters in bacteria constitute an enormous family of import systems for
small molecules. The transport complex is composed of two molecules of an independently
encoded ABC protein(s), a hetero- or homodimer
of integral membrane proteins constituting the
translocation pathway, and an external ligandbinding protein, amongst which the most
characterized, the periplasmic binding proteins
in Gram-negative bacteria are considered in

Chapter 10. The class 3 importers have been
assigned to at least nine major families in the
phylogeny analysis in Chapter 1. The allocrites
transported cover a wide range of essential and
non-essential molecules, including several metal
ions, iron chelates, vitamin B12, mono-, di- and
oligosaccharides, polyols, polyamines, inorganic
anions such as sulfate, nitrate and phosphate,
phosphonates, peptide osmoprotectants and
ssother di- and oligopeptides. From these
examples, the import systems for histidine and
maltose will be considered in some detail in
Chapter 9, and for uptake of osmoprotectants
in Chapter 13. As already indicated, despite the
range of allocrites transported in this very large
family, the nature of the different translocators is
surprisingly uniform: an external ligand-binding

protein, free in the periplasm in Gram-negative
bacteria whilst it may be anchored to the membrane surface in Gram-positive bacteria; two
membrane proteins for transport, carrying the
EAA interaction motif; and a highly conserved
ABC protein on the cytoplasmic side of the inner
membrane. Since evidence of exchangeability
of one ABC component for another in these
otherwise very similar systems has been rarely
indicated in the literature, we must assume
that each ABC is tailormade for contact and
intramolecular signaling with its cognate membrane domains.
Recent studies of two ABC-dependent solute

uptake systems responsible for transport of
general amino acids and branched amino acids
in Rhizobium leguminosarum have revealed the
surprising finding that such systems can apparently also export these amino acids. Moreover,
the same phenomenon was demonstrated with
histidine transport in S. typhimurium (Hosie
et al., 2001). This reverse transport or bidirectional capacity of these ABC transporters raises
some complex questions concerning the solute
pathway in the two different directions. In addition, it is not yet clear whether ATPase activity
is required for the efflux process (P. Poole, personal comunication).

MEMBRANE DOMAINS
OF THE BACTERIAL
TRANSPORTERS ARE
POORLY UNDERSTOOD
Whereas great progress has been made in the
comparative, phylogenic analysis of the ABC
domains, leading to prediction of possible function in the absence of other evidence in many
cases, the cluster analysis of membrane domains
has lagged far behind. This clearly hampers
insights into the mechanistic role of these
domains as potential translocation pathways
and these are poorly understood. Nevertheless,
as discussed in Chapter 9, the early recognition
(Dassa and Hofnung, 1985) of the EAA motif,
apparently completely conserved without
exception within a cytoplasmic loop of the
membrane components of all the bacterial ABC
importers, has ultimately led to the identification of this as a specific point of contact with a
region of the helical domain of the ABC-ATPase.



INTRODUCTION TO BACTERIAL ABC PROTEINS

This is presumably also a critical point in the
intramolecular signaling pathway, coordinating
transport and energy generation.
Importantly, the EAA motif is not present in
any of the exporters, indicating that during
evolution ABC-ATPases, in bacteria at least,
have associated with more than one type of
membrane domain. Furthermore, the failure so
far to detect any kind of conserved motif in the
membrane domains of ABC exporters perhaps
emphasizes, in contrast to the importers, the
wide variation in both the mechanism and
the pathway of molecular signaling between
the membrane and ABC components of the
exporters. As indicated below and discussed in
Chapter 7, the elucidation of the structure of
the membrane domain of the E. coli MsbA
protein will now enormously stimulate this
aspect of ABC studies.

STRUCTURE AND
FUNCTION OF THE ABC
TRANSPORTERS
Notably, some of the most advanced structural
studies of ABC transporters have come from bacterial import and, more recently, bacterial export
systems. Thus, we now have high-resolution

structures for ABC importers, HisP (Hung
et al., 1998), a MalK from Thermococcus litoralis
(Diederichs et al., 2000), one ABC in the family
of branched-chain amino acid transporters and
one of unknown function (Karpowich et al.,
2001; Yuan et al., 2001). In this laboratory, we
have recently obtained the high-resolution
structure of the ABC domain of HlyB (Schmitt
et al., in preparation), a member of the large
DPL family, which includes the mammalian
TAP and Pgp (Mdr1) proteins. The implications
of all these structural advances will be considered in other chapters. As discussed in Chapter
7, a very major and exciting advance in the
field was made by the presentation of the first
structural data at 4.5 Å for the intact bacterial
exporter MsbA from E. coli (Chang and Roth,
2001). This provides the first sign of the nature
of the membrane domain, and, in particular,
that of the membrane-spanning domains.
These are finally shown to be helices, settling
some previous controversies. Most crucially, of
course, this overall structure of MsbA has profound implications for at least a global understanding of how the action of the membrane

and ABC domains may be coordinated. Chang
and Roth (see also Higgins and Linton, 2001)
on the basis of this structure have already proposed an exciting solution to a long-standing
puzzle – how close are the ABC domains in the
transporter? – that most likely they are interfaced at some point in the catalytic cycle (see
also Chapter 6), but under the influence of the
membrane domains they are well separated in

the absence of any transport substrate. Unfortunately, mechanistic studies of the nature of
the catalytic cycle of ABC proteins in bacteria,
and its relationship to the transport function,
have lagged relatively far behind those for
some of the mammalian proteins. However,
recent advances in purifying and reconstituting proteins of the maltose and histidine
uptake systems (see Chapter 9), combined with
the power of microbial genetics, promise much
for the future.
Excitingly, as this volume goes to press the
high-resolution structure of the bacterial ABC
import system for vitamin B12, BtuCD, is
reported (Locher et al., Science 296, 1091–1098),
providing many new insights into the mechanism of ABC-dependent transport.

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