Ins and Outs of Glucose Transport Systems in Eubacteria

REVIEW ARTICLE
Ins and outs of glucose transport systems in eubacteria

Knut Jahreis1, Elisangela F. Pimentel-Schmitt2, Reinhold Bruckner
3
& Fritz Titgemeyer2
1
Department of Biology and Chemistry, University of Osnabruck,
Osnabruck,
Germany; 2Department of Microbiology, Friedrich-Alexander-University
Erlangen-Nurnberg,
Erlangen, Germany; and 3Department of Microbiology, University Kaiserslautern, Kaiserslautern, Germany
Correspondence: Fritz Titgemeyer, Abstract

Department of Oecotrophology,
Fachhochschule Munster,
Corrensstr. 25,
Glucose is the classical carbon source that is used to investigate the transport,
48149 Munster,
Germany. Tel.: 149 9131 metabolism, and regulation of nutrients in bacteria. Many physiological phenom-
482482; fax: 149 251 8365402; e-mail: ena like nutrient limitation, stress responses, production of antibiotics, and
fritz.titgemeyer@gmail.com differentiation are inextricably linked to nutrition. Over the years glucose trans-
port systems have been characterized at the molecular level in more than 20
Downloaded from http://femsre.oxfordjournals.org/ by guest on April 2, 2016

Received 24 August 2007; revised 22 April bacterial species. This review aims to provide an overview of glucose uptake
2008; accepted 21 May 2008. systems found in the eubacterial kingdom. In addition, it will highlight the diverse
First published online 18 July 2008.
and sophisticated regulatory features of glucose transport systems.
DOI:10.1111/j.1574-6976.2008.00125.x
Editor: Keith Chater
Keywords
carbon regulation; sugar transport;
phosphotransferase system; Mlc.
level in more than 20 different bacterial species (Fig. 1 and

Introduction Table 1). Their mode of action, their regulation, and their
Microorganisms have the capacity to utilize a variety of impact on the cellular physiology show fascinating features.
nutrients and adapt to continuously changing environmen- This review aims to survey and compare the currently
tal conditions. In general, the presence of a rapidly metabo- recognized glucose transport systems that have been char-
lizable carbon source leads to its immediate utilization and acterized in eubacteria. The nutrient is taken up by carrier
is accompanied by a number of regulatory events that systems of the PTS, by proton or cation gradient-driven
hamper the use of other carbon sources of less energetic transporters, through ATP-dependent ATP-binding cassette
value (reviewed in Bruckner & Titgemeyer, 2002). This was (ABC) permeases, and even via diffusion by specific facil-
first investigated in detail by Monod (1942), who described itator proteins. The activity of the glucose transport systems
the phenomenon of diauxic growth, showing that the often determines the rate of the metabolic flux and thus has
bacterium Escherichia coli primarily chooses glucose when a direct impact on the speed of growth (Bruckner &
exposed to a nutrient mixture of glucose and sorbitol. Since Titgemeyer, 2002; Bettenbrock et al., 2006). Besides this,
then, glucose has been the classic preferred carbon source GLTs can act as sensory systems for carbon regulation and
that has been studied for decades in order to reveal the chemotaxis, and have been associated with morphogenesis
molecular mechanisms of carbon transport and regulation. (Lux et al., 1995; Bruckner & Titgemeyer, 2002; Rigali et al.,
The first glucose transporter (GLT) was described in 1966 2006). Their importance is further underlined as they can
when a glucose-specific phosphoenolpyruvate-dependent also serve as entry systems for phages or bacteriocins (Erni,
phosphotransferase system (PTS) in E. coli was identified 2006; Diep et al., 2007). Recent findings have illustrated that
(Kundig et al., 1966). The corresponding DNA sequences of the regulation of glucose transport can be quite sophisticated,
the permease subunits were reported in 1984 and 1986 showing that one single glucose permease gene is regulated
(Nelson et al., 1984; Erni & Zanolari, 1986). Today, we have at multiple levels, involving several transcription factors,
sequence information of hundreds of glucose transport auxiliary regulatory proteins, small regulatory RNAs and
systems, disclosed through genome sequencing. About 30 protein phosphorylation (Bohm & Boos, 2004; Vanderpool
of these are characterized experimentally at the molecular & Gottesman, 2004; Becker et al., 2006).
FEMS Microbiol Rev 32 (2008) 891907

c 2008 Federation of European Microbiological Societies
Published by Blackwell Publishing Ltd. All rights reserved
892 K. Jahreis et al.
Lactobacillus casei
Lactobacillus curvatus
Bacillus subitilis Streptococcus mutans PTS
Bifidobacterium longum Streptococcus bovis
Corynebacterium glutamicum Streptococcus thermophilus
Mycobacterium smegmatis Streptococcus salivarius
Vibrio parahaemolyticus Lactococcus lactis
Enterococcus faecalis
e Glucose
Streptomyces coelicolor cos
Bifidobacterium longum Glu Es
Mycobacterium smegmatis
ch
er
IICMan
Glucose
IIDMan
Bacillus subtilis ich
IIBC
ia
C Glc
Cyanobacterium synechocystis sp co
Brucella abortus li
A
FS
an
Glc
IIB
IIABMan
an
Glucose
IIC M
M
IID M
H+
ag
IIAGlc
BA N
G
Glucose lc
P IIABMan
IIC
Glucose
Zymomonas mobilis GL
H+
F GalP
Glucose
MglB
Glucose-6-P
A
HPr-P Mgl
ATP MglC

Glucose GlkA Fructose-6-P
GlcU
? Glucose
Fructose-1,6-bis-P
Bacillus subtilis
Staphylococcus xylosus EI-P
Staphylococcus carnosus
lc
PEP
G
IIA
IIC
BM
lS
c alX
Gl
Sg
se
u co Ma
n IIA
Gl
IIC
+ II A an
Na
B
Malk
Na
M
1
IIB
g
Vibrio parahaemolyticus
Malk1
IIC
Xanthomonas oryzae
MalF
Ma
IID
MalG
Glucose
n
GlcG
GlcF
Ma
n
SGLT Vibrio furnissii

MalE
GlcE
Glucose
Thermus thermophilus
ABC
Fig. 1. Glucose transport systems of the bacterial kingdom. A cell is presented in which all 21 molecular characterized glucose uptake systems are
displayed. The five transport systems of Escherichia coli are shown separately on the right side. The transporter families are coloured as follows: ABC,
red; MFS, light blue; PTS, yellow; SGLT, dark blue; GlcU, green. For further explanation, see text. MFS, major facilitator super family.
In our overview, we will highlight that (1) bacteria can different permeases for glucose, including the major uptake
have up to five different glucose transport systems, that (2) system IICBGlc of the PTS type (Lengeler, 1993; Postma
related species use predominantly the same permease type, et al., 1993) (Fig. 1). The PTS, which is the major uptake
although their lifestyle is totally different, and that (3) the system for carbohydrates in enteric bacteria, consists of two
distinct regulatory features are sometimes unrelated and general, cytoplasmic proteins, Enzyme I (EI) and the
diverse, indicating that they have evolved separately to phosphocarrier protein HPr, and a number of carbohy-
respond optimally to the habitat conditions of each bacterial drate-specific transporters. These so-called Enzymes II
species. (IIABC) are composed of multidomain proteins present as
a single or as several individual polypeptides. While two
domains: IIA and IIB: are hydrophilic and involved in
Gram-negative bacteria phosphoryl group transfer, the IIC and IID (when it is
present) domains are membrane-bound and active in sugar
Escherichia coli and other enteric bacteria permeation across the membrane. The PTS-specific phos-
The molecular knowledge of glucose uptake and regulation phorylation chain begins with the autophosphorylation of
stems from investigations in E. coli. This bacterium has five EI at a histidine residue to histidines of HPr and then IIA,

c 2008 Federation of European Microbiological Societies FEMS Microbiol Rev 32 (2008) 891907
Ins and outs of glucose transport systems in eubacteria 893
Table 1. Bacterial glucose transport systems

Protein family
PTS MFS ABC SGLT GlcU References

Gram-negative bacteria
Brucella abortus 1 Essenberg et al. (1997)
Escherichia coli 3 1 1 Kundig et al. (1966), Lengeler (1993),
Postma et al. (1993), Ferenci (1996),
Saier et al. (1973), Postma (1977), Erni et al. (1987)
Synechocystis 1 Zhang et al. (1989)
Thermus thermophilus 2 Chevance et al. (2006)
Vibrio furnissii 3 Bouma & Roseman (1996a, b)
Vibrio parahaemolyticus 1 1 Kubota et al. (1979), Sarker et al. (1994)
Xanthomonas oryzae 1 Tsuge et al. (2001)
Zymomonas mobilis 1 Weisser et al. (1995), Parker et al. (1995)
Low-GC Gram-positive bacteria
Bacillus subtilis 1 1 1 Paulsen et al. (1998), Sutrina et al. (1990),
Fiegler et al. (1999), Abranches et al. (2003)
Enterococcus faecalis 1 Muraoka et al. (1991)

Lactobacillus casei 1 Veyrat et al. (1994)
Lactobacilus curvatus 1 Veyrat et al. (1996)
Lactococcus lactis 1 Thompson & Chassy (1983)
Staphylococcus carnosus 2 Christiansen & Hengstenberg (1999)
Staphylococcus xylosus 1 1 Fiegler et al. (1999)
Streptococcus bovis 1 Asanuma et al. (2004)
Streptococcus mutans 1 Abranches et al. (2003)
Streptococcus salivarius 1 Lortie et al. (2000)
Streptococcus thermophilus 1 Cochu et al. (2003)
High-GC Gram-positive bacteria
Bifidobacterium longum 1 1 Parche et al. (2006, 2007)
Corynebacterium glutamicum 1 Moon et al. (2005)
Mycobacterium smegmatis 1 1 Titgemeyer et al. (2007)
Streptomyces coelicolor 2 van Wezel et al. (2005)
MFS, major facilitator super family.
which finally phosphorylates a histidyl or a cysteyl residue of The mannose-specific PTS can transport glucose very
IIB, the IIB domain. The carbohydrate is transported efficiently with an apparent Km of 15 mM (Stock et al.,
through IIC or IICD, in the case of mannose-class PTSs, 1982) and is characterized by a broad substrate specificity
into the cell by concomitant phosphorylation from the IIB for mannose, glucose, and other derivatives of glucose
domain. altered at the C-2 carbon residue (Robillard & Broos,
Escherichia coli K-12 utilizes three different PTS-trans- 1999). Enzyme IINag exhibits only a marginal glucose trans-
porters for the uptake of glucose. The regular glucose-PTS port capacity. The capability of glucose uptake and phos-
consists of two subunits: the IIAGlc (also called IIACrr, phorylation by IINag, however, can be dramatically enhanced
encoded by the crr gene) and the IICBGlc (encoded by the by a single mutation, the substitution of phenylalanine 437
ptsG gene) (Erni & Zanolari, 1986). The Km for glucose by serine (K. Jahreis, unpublished results).
transport was reported to be in the range of 520 mM All the enteric bacteria sequenced thus far carry a ptsG
depending on the tested strain in the different labora- gene. The deduced protein sequences usually exhibit more
tories (Adler & Epstein, 1974; Lengeler et al., 1981; Stock than 90% identical amino acid residues. The IICBGlc from
et al., 1982; Lux et al., 1999). Moreover, wild-type IICBGlc E. coli K-12 and Salmonella enterica serovar Typhimurium
has a good affinity for a- and -methylglucosides, 1-thio- (reviewed in Erni, 2001), together with the mannitol-
glucose, 5-thio-glucose, and a low affinity for 2-deoxyglucose specific IICBAMtl (reviewed in Robillard & Broos, 1999)
and mannose (Erni, 2001). In addition, glucose can also and the b-glucoside-specific IIBCABgl (Yagur-Kroll &
be internalized by the mannose-PTS IIMan (IIABMan Amster-Choder, 2005), are by far the best-characterized
-IICMan-IIDMan) (Gutknecht et al., 1999) and the N-acetyl- PTS transporters. The hydrophilic IIB-domain of the GLT
glucosamine-PTS IINag (IICBANag) (Postma et al., 1993). carries the phosphorylation site Cys421, whereas the

c2008 Federation of European Microbiological Societies
IIC-domain contains the sugar-binding site. Complementa- bined, retain complete transport and phosphotransfer activity
tion between IIB and IIC domains on different subunits in a (Buhr et al., 1994).
IICBGlc dimer is possible (Lanz & Erni, 1998). Although the The IIAGlc forms a b-sandwich with six antiparallel
sites of IICB phosphorylation are known and easily recog- strands on either side. The two important residues His90,
nized from the amino acid motifs, residues that directly which is transiently phosphorylated, and His75, which seems
participate in sugar binding have not been clearly identified to stabilize the negative charge of PHis90, face each other at
thus far. Seventeen different mutations in PtsG have been the centre of the active site (Dorschug et al., 1984). The
described that cause a so-called relaxed conformation, binding surface for its interaction partner HPr on the IIAGlc
which leads to transport and phosphorylation of several is concave and located in a shallow depression, while that on
other carbohydrates (e.g. ribitol, arabinitol, ribose, xylose, HPr is convex and located on a protrusion. The central
fructose, and mannitol, respectively) (Erni, 2001). These region of each binding surface is hydrophilic and sur-
amino acid substitutions are scattered all over the IIC- rounded by polar and charged residues. The latter are
domain, except for the second and third predicted trans- entirely positive in the case of HPr and mostly negative in
membrane helix. The conformational changes caused by the case of IIAGlc (Wang et al., 2000). The binding surface of
these mutations, however, are still not clear. It has been the other interaction partner IIBGlc, resembles the one from
proposed that each monomer has a sugar-binding site of its HPr, a convex protrusion. The phosphoryl donor and
own with, logically, two sites in the dimer. These are acceptor residues, His90 of IIAGlc and Cys421 of IIBGlc are in

distinguished by their different affinities for the substrate, close proximity and buried within the centre of the interface
being simultaneously accessible from the cytoplasmic face (Cai et al., 2003).
and from the outside (Garcia-Alles et al., 2002). Further-
more, complementation analysis revealed that the IICBGlc
Regulatory considerations
subunits co-operate insofar as phosphoryl group transfer
from one IIB domain to the other is possible (Lanz & Erni, A number of studies in the last few years have revealed that
1998). the regulation of ptsG expression in E. coli K-12 is very
complex and involves several transcription factors, auxiliary
proteins, a small regulatory RNA, and diverse sigma factors
Structural considerations
(Fig. 2). Glucose uptake derepresses ptsG expression by
Whereas information on the structure of the integral inactivation of the glucose repressor Mlc (mnemonic for
membrane IIC domain is limited and controversially dis- makes large colonies) (Hosono et al., 1995; Plumbridge,
cussed, the structures of the IIBGlc-domain and the IIAGlc 2002; Bohm & Boos, 2004). The current model predicts that
protein have been solved (Worthylake et al., 1991; Eberstadt dephosphorylated IICBGlc, generated during glucose trans-
et al., 1996; Gemmecker et al., 1997). For the IIC-domain, port, binds Mlc and sequesters the repressor away from its
two detailed secondary structure models exist (Buhr & Erni, DNA-binding sites (Lee et al., 2000; Tanaka et al., 2000; Nam
1993; Lengeler et al., 1994). Both predict a topology of eight et al., 2001). Mlc is also involved in the glucose-dependent
transmembrane helices with the carboxy- and the amino- regulation of the ptsHIcrr operon that encodes EI, HPr, and
terminal ends oriented to the cytosol. However, the models IIAGlc, in regulation of the malT gene for the transcriptional
differ completely in the regions and orientations of the last activator of the maltose regulon: and in regulation of the
three transmembrane segments. All data available present genes for IIMan, manXYZ. Mlc is, therefore, considered
cannot distinguish between the two models. a pleiotropic-acting transcription factor responsible for
The IIBGlc-domain is a split a/b sandwich that consists of the induction of genes in the presence of glucose. Recently,
a four-stranded antiparallel b-sheet and three helices packed our group identified a novel regulatory factor called MtfA
against one side of the sheet. The active Cys421-residue is (mnemonic for Mlc-titration factor A) (Becker et al., 2006).
in the loop between strands b1 and b2. The IIB-domain This cytoplasmic, auxiliary protein binds to and inactivates
is connected to the IIC-domain by a flexible linker, which Mlc. In this way, it has a severe impact on ptsG regulation
contains a highly conserved KTPGRED motif that is and probably also on other Mlc-regulated genes. Interest-
present in all PTS permeases specific for glucose or ingly, MtfA orthologues exist in many Proteobacteria.
N-acetyglucosamine. Mutations or a deletion of this region The second major regulator of ptsG transcription is a
in PtsG were shown to be more deleterious to transport and global regulator, the cAMP-receptor protein (CRP) (also
phosphorylation activity than its absence in split or circu- known as CAP for catabolite activator protein). Mlc and
larly permuted forms of the protein (reviewed in Erni, cAMPCRP work antagonistically, because cAMP levels are
2001). The function of this sequence, however, is not clear. low during growth on glucose. Hence, their action results in
The two domains can be split within their connecting linker precise control of ptsG expression under various growth
peptide, expressed as separate proteins and, when recom- conditions. This can be explained, because IICBGlc is not

Escherichia coli
glc + glc
(Specific repression by Mlc) (Fine tuning regulation by global regulators)
Glc
IIC IIC
IIB P IIB
Glc-P Mlc SgrT
MtfA MtfA
Fig. 2. Regulation of the major glucose
Mlc Mlc
transport system IICBGlc (encoded by ptsG) in
Escherichia coli. In the absence of glucose, ptsG P Fis
cAMP ArcA
expression is repressed by Mlc. In the presence of +
CAP
glucose, Mlc is sequestered to the GLT IICBGlc or
to the auxiliary protein MtfA. Expression of ptsG +
+
depends on the global-acting transcription Mlc Mlc
factors CAP, ArcA, and Fis and on several sigma ptsG
ptsG OP ptsG OP ptsG
factors. The stability of the ptsG-mRNA is

regulated by the small regulatory RNA SgrS.
The small protein SgrT that is encoded in the 5 0
RNAseE
end of sgrS is somehow involved in the
downregulation of IICBGlc activity. SgrS
only involved in glucose transport but further has a major cent IIGlc peptide, mediates the Hfq/SgrS-dependent degra-
influence on the phosphorylation levels of all other PTS dation presumably by reducing second rounds of translation
proteins, especially on the phosphorylation state of IIAGlc, a (Kawamoto et al., 2005; Vanderpool & Gottesman, 2005).
central element in global carbon regulation (Bruckner & Last year, a novel regulatory feature was reported for the sgrS
Titgemeyer, 2002). In this context, it was not surprising that locus, which seems to have a dual function (Wadler &
more transcription factors were identified (Fig. 2). Among Vanderpool, 2007): the 5 0 end of sgrS, upstream of the
them are ArcA, a major transcription factor for the switch nucleotides involved in base pairing with the ptsG mRNA
between aerobic and anaerobic growth in E. coli (Jeong et al., (Fig. 2), contains a 43-aa ORF called sgrT. This small SgrT
2004), the two alternative sigma factors s32 for heat shock polypeptide apparently inhibits glucose transport activity
response (Shin et al., 2001) and sS for the expression of during glucose-phosphate stress by directly inactivating
genes in the stationary growth phase (Seeto et al., 2004), and PtsG transport activity, which would be the first example
the small globally acting DNA-binding protein Fis (Shin for such a regulatory mechanism within the PTS.
et al., 2003). All these different regulatory effects might emphasize the
In addition to these regulation mechanisms at the tran- important function of the glucosePTS in the global regula-
scriptional level, ptsG expression is posttranscriptionally tion of carbohydrate uptake in enteric bacteria. Especially
regulated by the modulation of its mRNA stability in the role of the IIAGlc has been known for a long time.
response to the glycolytic flux in the cells (Kimata et al., Unphosphorylated IIAGlc, which is generated during the
2001; Morita et al., 2003). As revealed by the Gottesman uptake of glucose or other PTS carbohydrates, is an allos-
group, accumulation of glucose-6-phosphate or fructose-6- teric inhibitor of the lactose permease LacY, the glycerol
phosphate activates the transcriptional activator SgrR, kinase GlpK, the MalK subunit of the maltose transport
which in turn leads to the synthesis of the small regulatory complex, and raffinose permease (Bruckner & Titgemeyer,
RNA SgrS (Vanderpool & Gottesman, 2004). SgrS is com- 2002). Inhibition by IIAGlc always prevents uptake and
plementary to the 5 0 end of the ptsG-mRNA and is capable formation of metabolites, which are inducers for other
of forming Hfq-dependent RNARNA hybrids, which are carbohydrate uptake systems. Thus, this mechanism has
degraded in an RNAse E/degradosome-dependent manner. been defined as inducer exclusion (reviewed in Bruckner
The degradosome contains polynucleotide phosphorylase & Titgemeyer, 2002; Deutscher et al., 2006). As long as
(PNPase), RhlB helicase, and a glycolytic enzyme, enolase, glucose or other PTS substrates are available, the transcrip-
that appears to be crucial for the degradation in re- tion of operons for alternative catabolite pathways is re-
sponse to metabolic stress (Morita et al., 2004). It was pressed. In contrast, the concentration of phospho-IIAGlc
further shown that ptsG-mRNA localization to the inner starts to increase after the PTS substrates are consumed
membrane, coupled with the membrane insertion of nas- (Bettenbrock et al., 2007). Phosphorylated IIAGlc directly or

indirectly activates the enzyme adenylate cyclase and cAMP impact on glucose metabolism. Replacement of the glucose-
concentrations increase (Park et al., 2006). Thus, genes and PTS by the galactose permease in genetically engineered
operons whose transcription depends on the activation by strains reduced acetate accumulation and improved biopro-
the cAMPCAP complex are transcribed, provided the cess formation probably by increasing the glycolytic flux to
specific inducer is also present. This type of regulation is fermentation products (Hernandez-Montalvo et al., 2003;
known as carbon-catabolite repression. De Anda et al., 2006).
Last but not least, using the PEP-dependent phospho-
transferase EI, the PTS is capable of sensing the physiological
state of the cell by measuring the intracellular PEP to
Vibrio species
pyruvate ratio. Any change of this ratio, even caused by the Vibrionaceae are closely related to the above-described
transport of non-PTS substrates like glucose-6-phosphate enteric bacteria. For the facultatively anaerobic, pathogenic
(Hogema et al., 1998), directly influences the autopho- species of Vibrio furnissii, three different PTS-dependent
sphorylation activity of EI and in turn the phosphorylation permeases have been described, which complement an
state of HPr and IIAGlc, the general regulatory output E. coli mutant deficient in glucose transport (Bouma &
protein of the PTS (Bruckner & Titgemeyer, 2002). Roseman, 1996a, b). The first permease, designated as MalX,
exhibits 38% identical residues with the IICBGlc from E. coli
and 37% with the IICBAGlc from B. subtilis. However, the

Glucose flux considerations
highest similarity was observed to MalX from E. coli (67%
Different approaches have been adopted using the glucose- identity), a PTS permease of unknown substrate specificity
PTS to develop a computer model of bacterial growth under (Postma et al., 1993). The second permease was termed
various conditions. A comprehensive model on glucose/ NagE, because it shows with 47% identical residues the
lactose diauxic growth behaviour was presented for example highest similarity to the N-terminal, hydrophobic domain
by Kremling et al. (2001) and has been extended recently IIC of the N-acetyl-glucosamine-PTS IICBANag (gene nagE)
(Bettenbrock et al., 2006). This model perfectly reproduces from E. coli. Both MalX and NagE lack the IIA domain
biomass yield, glucose and lactose consumption, the prefer- and require an additional IIAGlc factor for transport and
ential use of glucose, and the induction of the lac operon phosphorylation. For NagE, it was demonstrated that both
over time. This is a first step on the way to a complex N-acetylglucosamine and glucose were transported and
computer model of the whole bacterial metabolism, which phosphorylated. The third glucose-transporting system was
takes both metabolic fluxes and their regulation into described as a mannose/glucose-specific PTS (Bouma &
account. Roseman, 1996b). The corresponding genes were similar to
the manXYZ (IIC, IID, IIABMan) genes of E. coli with the
difference that in V. furnissii, the IIA and IIB proteins are
Alternatives
encoded by two individual genes: manZ and manW. By
Besides PTS-dependent glucose transport systems, enteric heterologous expression in E. coli, it was shown that these
bacteria can also internalize glucose by two different galac- four proteins are sufficient for the phosphoryl transfer and
tose-induced uptake systems: the galactose permease GalP transport of mannose and glucose in vivo and in vitro.
and the methyl-galactoside permease MglBAC (Ferenci, Unlike the E. coli mannose-PTS, V. furnissii IIMan is not
1996). Escherichia coli or Salmonella strains lacking both EI capable of transporting N-acetylglucosamine or fructose.
and HPr regain the ability to utilize glucose by constitutive However, it should be noted that the manXYZW genes of
expression of one of the two galactose systems (Saier et al., V. furnissii have the highest similarity to an N-acetylgalacto-
1973). It was also found that under glucose limitation in a samine PTS (aga gene locus) of E. coli (Brinkkotter et al.,
chemostat, the mgl system is induced by endogenous 2000). In addition, both gene loci comprise a gene for an
galactose synthesis (Death & Ferenci, 1994). Especially the N-acetylgalactosamine deacetylase. Hence, the identified
ATP-driven ABC transporter MglBAC exhibits a very high IIMan of V. furnissii may transport N-acetylgalactosamine as
affinity for glucose with a Km of about 10 mM, whereas the the main substrate. A V. furnissii equivalent of E. coli IICBGlc
proton-symporter GalP has a Km for glucose in the 100 mM has not yet been found.
range (Lengeler, 1993). GalP has been characterized further In the Gram-negative, halophilic marine, pathogenic
with a Km for galactose of 45 mM and a rather broad bacterium Vibrio parahaemolyticus glucose is taken up by
specificity for galactose, glucose, mannose, fucose, 2-deoxy- two systems: a PTS and a sodium-coupled permease (Kubota
galactose, and 2-deoxyglucose (Postma, 1977). In contrast to et al., 1979; Sarker et al., 1997, 1994). Based on biochemical
PTSs, growth on glucose transported via MglBAC or GalP data, the V. parahaemolyticus glucosePTS seems to be
permeases requires subsequent phosphorylation by glucoki- similar to the glucose-PTS of enteric bacteria, while the
nase. Interestingly, such a setting can already have a drastic other GLT (SglS) is a member of the sodium/glucose

transporter family (SGLT) that is typically found in mamma- mediates the uptake of fructose and xylose (Weisser et al.,
lian cells (Wood & Trayhurn, 2003). The energy necessary for 1995). Subsequent phosphorylation of glucose in Z. mobilis
the transport is generated by the electrochemical potential of is catalysed by the glucokinase GlkA. Heterologous comple-
Na1 across the cell membrane, which is established by the mentation using appropriate E. coli mutants demonstrated
respiration-driven Na1 pump and the Na1/H1 antiporter that the expression of glkA of Z. mobilis restores the
(Tsuchiya & Shinoda, 1985; Kuroda et al., 1994). SglS glucokinase phenotype (Snoep et al., 1994). The introduc-
mediates not only the uptake of glucose but also the uptake tion of glf into glucose transport-negative, glucokinase-
of galactose, fucose, salt, and water (Sarker et al., 1997). The positive E. coli derivatives led to the restoration of growth
Km for glucose and galactose were determined as 30 and on glucose. Transport kinetics of heterologous expression of
14 mM, respectively, with a calculated Vmax of 97 and glf in such E. coli mutants with [14C]substrates demon-
85 nmol min1 mg1 protein. strated that Glf has a Km of 2.5 0.3 mM and a Vmax of
92 5 nmol min1 mg1 protein for glucose. Moreover, the
Xanthomonas oryzae pv. oryzae presence or absence of GlkA did not change the apparent Km
of Glf for glucose, whereas the Vmax for glucose transport
In addition to the symporter system of V. parahaemolyticus, went up by 80% in the presence of glucokinase (Parker
other members of the SGLT family transporter were identi- et al., 1995). Interestingly, the apparent Km for glucose of
fied in X. oryzae pv. oryzae, a plant-pathogenic bacterium Glf in recombinant E. coli strains is significantly lower than

(Tsuge et al., 2001), which belongs to the Gammaproteobac- measurements of the Km for glucose performed with
teria. This GLT shares 50% amino acid identity to the Na1/ wild-type Z. mobilis (Struch et al., 1991). An explanation
H1 glucose permease of V. parahaemolyticus and also has an for this difference is not known. Nevertheless, because
additional affinity for galactose. However, the rates of Z. mobilis resides in the glucose-rich juice of Agave amer-
[14C]glucose transported by GLT did not decrease in the icana, the presence of the low-affinity facilitator Glf is very
presence or absence of NaCl, or when replaced by KCl. It has appropriate.
been suggested that GLT does not need Na1 to couple
glucose transport. Because the transport buffer did not
Cyanobacterium Synechocystis sp.
contain additional cations, it was suggested that GLT is a
H1-coupled GLT rather than a Na1/glucose symporter. In photoautotrophic cyanobacterium Synechocystis sp., the
respiratory process to metabolize sugars is utilized besides
their natural photosynthetic process to generate energy
Brucella abortus
(Joset-Espardellier et al., 1978). By recovery of the glucose
The facultative intracellular pathogen B. abortus belongs to transport capacity of a transport-deficient Synechocystis
the group of Alphaproteobacteria. It is capable of surviving strain, a gene for a proton symporter (glcP) has been
and growing in macrophages and other phagocytes. This characterized that mediates the assimilation of glucose
bacterium has been reported to grow on various carbohy- (Zhang et al., 1989). Further analyses of GlcP revealed that
drates including glucose, galactose, and fructose (McCullough this transporter belongs to the major facilitator superfamily,
& Beal, 1951). Transport of glucose was determined with a sharing the highest similarity to the glucose permeases Glf
Km of 160 mM. Interestingly, the only common glucose from Z. mobilis and GlcP from Streptomyces coelicolor
analogue transported was 2-deoxyglucose, with an apparent (Snoep et al., 1994; van Wezel et al., 2005).
Ki of 0.73 mM. The observation that the uptake was sensitive
to various inhibitors led to the suggestion of a proton- Thermus thermophilus
coupled rather than a PTS-dependent uptake mechanism
(Rest & Robertson, 1974). By heterologous expression in a Glucose uptake systems have also been described from
glucose transport-deficient E. coli strain, a screen of a T. thermophilus that uses two ABC transport systems, desig-
genomic B. abortus library revealed the identification of the nated as a glucose/mannose ABC and a trehalose, maltose,
gluP gene (Essenberg et al., 1997). This gene encodes a sucrose, and palatinose (TMSP)ABC (Chevance et al.,
glucose/galactose transporter, which belongs to the major 2006). The glucose/mannose transport system is encoded
facilitator superfamily with the fucose-transporter FucP of by the glcEFG genes. The glcE gene codes for an extracellular
E. coli as the closest relative (Pao et al., 1998). substrate-binding protein, while the two membrane-em-
bedded permeases of the system are encoded by glcF and
glcG. TMSPABC is encoded by the malEFG genes, where
Zymomonas mobilis malE encodes the binding protein, which has broader sugar
In terms of glucose transport systems, the Gram-negative specificity. The two permeases are encoded by malF and
ethanol producer Z. mobilis constitutes an exception. This malG. These systems transport glucose with a Km of 0.15 mM
bacterium obviously has a glucose facilitator (Glf) that also and a Vmax of 4.22 nmol min1 mL1 OD1 600 nm via the

glucose/mannose ABC transporter and with a Km of 1.4 mM xylosus (Fiegler et al., 1999), could be a candidate for the
and a Vmax of 7.6 nmol min1 mL1 OD1 600 nm via the unknown uptake system in B. subtilis. The gene glcU is
TMSPABC transporter. It could be experimentally demon- encoded upstream of and is cotranscribed with the glucose
strated that the presence of glucose induces both systems dehydrogenase gene gdh (Nakatani et al., 1989). Transcrip-
and that the glucose/mannose-binding protein specifically tion of this operon has been shown to occur in the forespore
binds to glucose, mannose, and galactose with a determined about two hours after the onset of sporulation (Nakatani
KD of 20 mM and binding saturation at 2.1 mM for glucose, et al., 1989), but expression in the early exponential growth
and galactose, and a KD of 134 mM and binding saturation at phase has not been tested. Despite the availability of the
4.76 mM for mannose. The ATPase that provides the energy B. subtilis genome sequence (Kunst et al., 1997), the com-
for both ABC transporters is encoded by the malK1 gene. plete set of glucose uptake systems in this organism is still
Interestingly, the genes are regulated by an Mlc-like unknown.
transcription factor. However, in T. thermophilus no evi- Although some details of glucose uptake in B. subtilis are
dence for a glucosePTS could be found, which means that missing, it is clear that the ptsG-encoded PTS permease is
the induction mechanism must be different compared with the major GLT. Expression of the ptsG gene is glucose
E. coli. Consequently, it could be demonstrated that binding inducible by transcriptional antitermination and involves
of glucose by MlcTth eliminates its ability to bind to its the antiterminator protein GlcT, an RNA switch, and the
operator (Chevance et al., 2006). In the absence of glucose, PtsG permease (Stulke et al., 1997) (Fig. 3). The antitermi-

MlcTth represses the expression of a gene locus, which nator protein GlcT, whose gene is located immediately
encompasses the mlc gene itself, the glucose/mannose ABC upstream of ptsG, consists of three domains: an RNA-
transport genes, and two other genes for permeases. BLAST binding domain, and two PTS regulation domains (PRD-I,
analysis of the permease genes revealed homology to mem- PRD-II) (Stulke et al., 1998). In the absence of glucose,
brane components of ABC transporters. Further in silico PRD-I is phosphorylated by the IIB domain of PtsG
analysis identified five other ABC transporters in this (Schmalisch et al., 2003) and the antiterminator protein is
organism. It has been suggested that MalK1 is a general inactivated. Under these conditions, the transcriptional
energy provider for these ABC systems. terminator in the ptsG RNA switch is generated and ptsG-
mRNA, which is transcribed by a constitutive promoter, is
prematurely terminated. In contrast, if glucose is trans-
Low GC gram-positive bacteria ported by PtsG, the phosphate-group is transferred to the
carbohydrate. In turn, nonphosphorylated GlcT can bind to
Bacillus subtilis
a sequence in the ptsG riboswitch designated RNA anti-
In B. subtilis, glucose transport is realized by at least two terminator (RAT) (Aymerich & Steinmetz, 1992). GlcT
different systems: a glucose-specific PTS permease (IIC-
BAGlc) and a hexose/H1 symporter (GlcP) (Sutrina et al.,
Bacillus subtilis
1990; Paulsen et al., 1998). The glucose permease is the
product of the ptsG gene and is the first gene of the ptsGHI glc + glc
(GlcT~P inactive) (GlcT active)
operon, which in addition encodes the two general PTS
proteins HPr and EI (Stulke et al., 1998). The glucose/H1 Glc
symporter is the gene product of glcP, which was originally IIC IIC
described as a single transcriptional unit (Paulsen et al., IIB P IIB
IIA P Glc-P IIA
1998). GlcT P
Glucose uptake measurements in B. subtilis cells that were
grown in the presence of glucose showed that GlcP con-
tributed about 30% of the glucose transport under these ptsG ptsG
ptsGP ptsGP
conditions (Paulsen et al., 1998). In a DptsGHI background,
Terminator GlcT
however, GlcP did not contribute significantly to glucose
RAT
transport. This result was taken as an indication that glcP RAT
expression relies on a functional PTS (Paulsen et al., 1998).
The study also revealed that there is at least one more uptake Fig. 3. Regulation of the major glucose transport system IICBAGlc (en-
coded by ptsG) in Bacillus subtilis. In the absence of glucose, the
system operative in B. subtilis. A double mutant devoid of
antiterminator protein GlcT is phosphorylated by the IICBAGlc, which
IIGlc and GlcP still transported glucose. Because ptsHI is also leads to an inactivation of the protein. In the presence of glucose,
deleted in the IIGlc-deficient strain, residual glucose uptake GlcTP is dephosphorylated by the PTS transporter and thus activated.
must be due to a non-PTS system. The glucose uptake Activated GlcT binds to the RNA-antiterminator sequence (RAT) and
protein, GlcU, which was first described in Staphylococcus leads to a transcriptional read-through allowing expression of ptsG.

binding to RAT prevents formation of the terminator 2007). The same regulation appears to be realized in
structure with transcriptional readthrough as a consequence Streptococcus mitis and Streptococcus sanguinis.
(Stulke et al., 1998). GlcT can also be phosphorylated at At least in Streptococcus mutans and L. lactis, there is clear
PRD-II by HPr, but this phosphorylation has only a minor evidence that PTS-independent glucose uptake systems exist
impact on protein activity (Schmalisch et al., 2003). (Keevil et al., 1984, 1986; Cvitkovitch et al., 1995; Luesink
In contrast to the detailed knowledge of ptsG regulation, et al., 1999), but those have not been identified at the
very few regulatory details have been worked out for molecular level.
glcP. Relatively recently, it was shown that the gene is
cotranscribed with genes whose gene products act in the Lactobacillus
production of the amino-sugar antibiotic compound neo-
In lactobacilli, fermentative bacteria that are frequently used
trehalosadiamine (Inaoka & Ochi, 2007). Interestingly, ex-
in the dairy industry, the above-mentioned mannose/GLT
pression of this operon relies on the catabolite control
(PTSMan) is also the main glucose transport system. The
protein CcpA as a positive effector. While mechanistic
genes encoding PTSMan are organized in operons (Veyrat
details of this apparent indirect regulation are still missing,
et al., 1996; Yebra et al., 2006). In Lactobacillus casei, for
CcpA-mediated activation of glcP expression may offer an
example, the genetic organization manLMN is the same as in
explanation for the reported PTS dependency of glcP
most of the streptococcal species. The gene manO is located
expression mentioned above (Paulsen et al., 1998). Without
downstream of the PTSMan-encoding genes. Although

HPr, CcpA activity is considerably diminished in B. subtilis
manO is cotranscribed with the manLMN genes, insertional
(Bruckner & Titgemeyer, 2002).
inactivation of the gene did not result in a recognizable
phenotype (Yebra et al., 2006). Thus, the function of the
Streptococcus /Enterococcus /Lactococcus ManO protein remains enigmatic. The mannose operon in
Lactobacillus curvatus is one of the examples where the IIA
In many streptococci, a bacterial group consisting of com-
and IIB domains are encoded by separate genes (Veyrat
mensal but also pathogenic species, the major glucose
et al., 1996).
uptake system belongs to the mannose class of PTS per-
Apart from the function as the main GLT in quite a
meases (Zuniga et al., 2005). These PTS permeases, quite
number of bacteria, PTSMan has gained considerable atten-
often referred to as mannose/glucose (PTSMan) transporters,
tion as a target for the activity of class II bateriocins (Diep
can have relatively broad substrate specificity, being able to
et al., 2007). It has been demonstrated that the membrane
transport mannose, glucose, N-acetylglucosamine, fructose,
IIC and IID components render bacteria sensitive to these
and 2-deoxyglucose. Transporters of the mannose class
types of bacteriocins. Thus, while providing a growth
contain an additional IID domain, and PTSMan transporters
advantage by means of their efficient carbohydrate uptake,
characteristically possess fused IIAB domains (Zuniga et al.,
PTSMan-containing bacteria face the disadvantage of being
2005). The genes for PTSMan transporters are organized in
susceptible to bacteriocins secreted by competitors.
operons with the gene order manLMN (IIAB, IIC, IID)
An L. casei mutant deficient in PTSMan can still take up
(Lortie et al., 2000; Abranches et al., 2003; Cochu et al.,
glucose and mannose (Veyrat et al., 1994; Yebra et al., 2006).
2003; Asanuma et al., 2004; Zuniga et al., 2005). In many,
The transport can be blocked in the presence of an uncou-
but not all manLMN operons, a fourth gene encoding a
pler that increases the proton permeability of the mem-
protein of unknown function is located downstream of the
brane. The same treatment in the wild-type strain had only a
operon. This gene is designated manO. While manO is
slight effect on glucose uptake (Veyrat et al., 1994). Thus, a
found in a number of other firmicutes, it appears to be
proton motif force-driven permease is also involved in
absent from Gammaproteobacteria (Zuniga et al., 2005). In
glucose transport in this organism. Unfortunately, the gene
S. salivarius and S. vestibularis, an additional IIAB (IIABMan
H )
for this permease is still unknown. Likewise, a glucose/H1
is found, which is larger than IIABMan encoded by manL.
symporter in Lactobacillus brevis has been characterized
IIABMan
H is related to but not identical to IIABMan. The
biochemically, but the corresponding gene was not isolated
function of this protein remains to be determined (Pelletier
(Ye et al., 1994). In L. casei, mutants deficient in PTSMan or
et al., 1998). The mannose PTS is also found in Enterococcus
in the general PTS are still able to take up glucose (Veyrat
faecalis and Lactococcus lactis (Thompson & Chassy, 1983,
et al., 1996), but again, the non-PTS transport system(s)
1985; Thompson et al., 1985).
have not been characterized.
Expression of the manLMN operon is generally consid-
ered constitutive at least with regard to the source of
carbohydrates. However, the manLMN promoter has been
Staphylococcus
shown recently to be under direct negative control by the Glucose transport systems have been investigated in two
two-component regulatory system CiaRH (Halfmann et al., nonpathogenic staphylococcal species, Staphylococcus

xylosus and Staphylococcus carnosus, which are both applied sporulating corynebacteria and mycobacteria, and from gut
in meat fermentation. In S. xylosus, a PTS-independent commensals, the probiotic bifidobacteria.
glucose uptake system, consisting of the glucose uptake
protein GlcU and the glucokinase GlkA, has been described Streptomyces coelicolor
(Wagner et al., 1995; Fiegler et al., 1999). The system,
Streptomyces coelicolor is the model organism for sporulat-
encoded by glcU and glkA at different genetic loci, substan-
ing, antibiotic-producing streptomycetes, a genus of major
tially contributes to glucose catabolism in S. xylosus and its
importance for pharmacological and industrial exploitation
presence sufficiently explains the ability of a ptsI mutant to
(Chater, 1999; Demain, 2000). These bacteria grow in the
utilize glucose as a carbon source (Jankovic et al., 2003). The
soil as a vegetative fungus-like mycelium, from which they
mechanism by which GlcU mediates glucose uptake, how-
develop under nutrient-worsening conditions aerial hyphae
ever, remains to be clarified.
and exospores. The glucose permease GlcP, a member of the
In S. carnosus, which also contains the GlcU/GlkA system
major facilitator super family, was detected by similarity
(Bruckner & Rosenstein, 2006), two glucosePTS permeases
searches with the glucose permease sequences of Z. mobilis
were identified (Christiansen & Hengstenberg, 1999). The
and Synechocystis (Zhang et al., 1989; Weisser et al., 1995;
genes glcA and glcB, located in tandem, each encode an
van Wezel et al., 2005). Two almost identical glucose
enzyme II denominated IICBAGlc1 and IICBAGlc2, which
permease genes, glcP1 and glcP2, which differ in four
share 69% amino acid identity. In vitro PTS-dependent

nucleotides but translate to identical proteins, were detected
phosphorylation of glucose demonstrated that IICBAGlc1 has
in the genome of S. coelicolor A3(2) (Bentley et al., 2002).
a Km of 12 mM and IICBAGlc2 of 19 mM. Both enzymes
The kinetic features of GlcP1 were derived from heterolo-
exhibited similar affinities for glucose, but they reacted differ-
gous production in an E. coli glucose transport mutant
ently with glucoside analogues. IICBAGlc1was inhibited by 2-
strain. The Km could be determined with 41 5 mM and
deoxy-glucose and methyl-b-D-glucoside, whereas IICBAGlc2
the Vmax with 23 1 nmol min1 OD1 600 nm, demonstrating
was inhibited by methyl-a-D-glucoside, methyl-b-D-glucoside,
that GlcP is a high-affinity GLT. As substrates, glucose and
r-nitrophenyl-a-D-glucoside, o-nitrophenyl-b-D-glucoside, and
2-deoxyglucose were recognized efficiently, indicating nar-
salicin. Moreover, IICBAGlc1 showed a stronger selection for
row substrate specificity. The activity was inhibited by the
substitutions at the C-1 position. It seems that IICBAGlc1 and
ionophore CCCP, which suggests that GlcP operates as a H1
IICBAGlc2 have different arrangements of the active-site
symporter as most permeases of the major facilitator super-
amino acids involved in substrate binding and, consequently,
family do (Pao et al., 1998). Transcription analyses demon-
in their catalytic affinity. The tandem arrangement of the
strated that expression of glcP1 is induced by the presence of
glcA/B genes is so far unique to S. carnosus. In other
glucose in the medium and is essential for glucose uptake,
staphylococcal species, genes encoding glucose-specific PTS
while glcP2 was found to be barely expressed. It has been
permeases are not encoded in close vicinity (Jankovic &
suggested that GlcP2 might be important under different
Bruckner, 2001; Bruckner & Rosenstein, 2006).
growth conditions. GlcP is also found in Streptomyces
Immediately upstream of glcA, a gene, glcT, was detected,
lividans (van Wezel et al., 2005) and Streptomyces avermitilis
whose deduced amino acid sequence shows a high degree of
(Ikeda et al., 2003). Because the genome of the latter is
similarity to bacterial regulators involved in antitermination
known, it was surprising to notice that this species has only
(Stulke et al., 1998). A putative transcriptional terminator
one glcP gene. The promoter region of glcP1 contains a
partially overlapping an inverted repeat, which could be the
conserved 16-bp palindromic sequence, which could parti-
target site for the antiterminator protein GlcT, is situated in
cipate in the regulation. A regulator, however, has not yet
the glcT-glcA intergenic region. This organization resembles
been identified.
the glcT-ptsG region of B. subtilis. Studies of S. carnosus GlcT
activity in the heterologous host B. subtilis indicated that the
Corynebacteria
protein is indeed able to cause antitermination (Knezevic
et al., 2000). While glcA of S. carnosus is apparently Corynebacterium glutamicum is a main producer of amino
controlled by antitermination, glcU regulation in S. xylosus acids, notably glutamate, methionine, and lysine, yielding
has not yet been elucidated. more than 2 million tonnes of flavour compounds and food
additives each year (Eikmanns et al., 1993; Jetten & Sinskey,
1995). Studies on sugar transport revealed that C. glutami-
High-GC gram-positive bacteria cum has PTS permeases for the uptake of glucose, fructose,
In high-GC Gram-positive bacteria that are called Actino- and sucrose (Moon et al., 2007). The PTS components EI,
bacteria, several glucose transport systems have been de- HPr, and IIBCAGlc (ptsG) were identified experimentally
scribed at the molecular level. There is information available and it was shown that the respective mutants could barely
from soil-dwelling sporulating streptomycetes, from non- grow on glucose (Parche et al., 2001a; Moon et al., 2005),

Corynebacterium glutamicum ptsG in C. diphtheriae is, as ptsG of B. subtilis (see Fig. 2),
glc + glc regulated by transcriptional antitermination and thus in a
(SugR active) (SugRFru-6-P inactive) manner totally different from the regulation found in
Glc C. glutamicum.
IIC IIC
IIB P IIB Bifidobacteria
IIA P Glc6-P IIA
Bifidobacterium species are applied in the dairy industry as
Fru6-P probiotic cultures that beneficially influence the host (Sal-
SugR
minen et al., 1998). They can for example stimulate
SugR the immune system, have cholesterol-lowering effects, and
ptsG ptsG prevent cancer recurrence. For the transport of glucose,
ptsGOP ptsGOP
different systems were identified. A glucosePTS was de-
monstrated in Bifidobacterium breve (Degnan & Macfarlane,
Fig. 4. Regulation of the major glucose transport system IIBCAGlc 1993), and a potassium-dependent glucose permease was
(encoded by ptsG) in Corynebacterium glutamicum. In the absence of characterized in Bifidobacterium bifidum (Krzewinski et al.,
glucose, ptsG expression is repressed by the DeoR-type regulator SugR.
1997). The latter showed characteristics of a low-affinity
The transport of glucose causes accumulation of the metabolite fruc-

tose-6-phosphate (Fru6-P). Its binding to SugR prevents DNA binding of
transporter with a Km of 9.16 mM. However, these systems
the regulator to the cognate operator sequence (ptsGop). have so far been characterized biochemically without iden-
tification of the genes. Recently, a proton symporter system
for glucose transport (GlcP) was described in detail in
suggesting that ptsG encodes the major GLT. The permease
Bifidobacterium longum (Parche et al., 2006). This study
has a Km in the low micromolar range and narrow substrate
demonstrated that the glcP gene complemented an E. coli
specificity for glucose and glucose analogues, as well as a low
glucose-deficient strain. Using the heterologous expression
affinity for mannose and fructose (E.F. Pimentel-Schmitt,
system in E. coli, the Km and Vmax for glucose uptake were
unpublished results) (Moon et al., 2007). Phylogenetic
determined as 70 14 mM and 11 2 nmol min1 OD1 600 nm.
analyses showed that IIBCAGlc falls into the subcluster of the
It was further demonstrated that GlcP has the highest
b-glucoside-sucrosetrehalose family of PTS permeases and
affinity for glucose, followed by 2-deoxy-glucose, mannose,
not into the subcluster comprising enzymes II specific for
and galactose, while fructose, arabinose, and xylose were
glucose and N-acetylglucosamine (Parche et al., 2001b).
poorly recognized. The observation that B. longum shows a
This suggests a different evolution of the glucose-specific
reverse diauxic growth behaviour is quite interesting. It
PTS present in corynebacteria. While it was originally
prefers lactose over glucose. Microarray analysis revealed
reported that ptsG expression is constitutive (Parche et al.,
that only the glcP gene was the target of this repression when
2001a; Moon et al., 2007), it turns out that it is regulated by
B. longum was grown in the presence of glucose and lactose
the DeoR-type regulator SugR (Fig. 4) (Engels & Wendisch,
(Parche et al., 2006).
2007). SugR binds to a 75-bp fragment of the ptsG promoter
Adjacent to the glcP gene, genes for a PTS-specific glucose
region and responds to fructose-6-phosphate. A cometabo-
permease (ptsG) and a gene for an antiterminator (glcT) are
lization with gluconeogenic substrates such as acetate results
located (Parche et al., 2006). Although it has been shown
in repression of ptsG, while glucose or any other condition
that the glucose-PTS is functional, its level of expression is
that deliver high internal fructose-6-phosphate concentra-
apparently so low that it merely contributes to glucose
tions leads to ptsG expression. The authors observed further
transport (Parche et al., 2006, 2007). The genetic setting of
that SugR is involved in the regulation of several genes
two glucose permease genes with different mechanistic
including ptsF and ptsS, which encode the PTS permeases
functions is thus far a unique feature. The gene order ptsG
for fructose and sucrose, indicating that SugR serves func-
glcT, however, resembles the situation in C. diphtheriae.
tions in a higher hierarchic manner.
Further analysis is required to describe a possible regulation
In Corynebacterium diphtheriae, the causative agent of
of ptsG and/or glcP by GlcT in B. longum.
diphtheria (Mattos-Guaraldi et al., 2003), bioinformatic
analyses showed the presence of PTS components encoded
Mycobacteria
by the genes ptsH, ptsI, and ptsG (Parche et al., 2001b).
PtsG shares 42% protein identity and the same IIBCA In contrast to the advantageous industrial use of streptomy-
domain order as the one of C. glutamicum. Curiously, a cetes, corynebacteria, and bifidobacteria, the saprophytic
regulatory gene that encodes an antiterminator, designated Mycobacterium smegmatis has been used as a model to
glcT, is found downstream of ptsG (Parche et al., 2001b; understand virulence in mycobacteria. In contrast to pre-
Moon et al., 2007). Based on this, it was suggested that vious reports, a PTS for glucose uptake has been identified

recently by in silico analysis (Titgemeyer et al., 2007). In fact, what can be expected from bacterial systems that have not
all components like HPr, EI, IIBC (ptsG), and IIAGlc (crr) are yet been investigated in such detail.
present in this organism. Additionally, bioinformatic ana-
lyses revealed a putative glucose permease encoded by the
gene msmeg4182 (glcP). The deduced protein belongs to the
major facilitator super family and shares 53% amino acid
Acknowledgements
identity with the main GLT GlcP of S. coelicolor and 34% This study was financially supported by the Deutsche For-
with GlcP of B. longum (van Wezel et al., 2005; Parche et al., schungsgemeinschaft through grants GK805 and SFB473 to
2006). We could confirm by heterologous complementation E.F.P-S. and F.T., and SFB431 to K.J. F.T. and K.J. dedicate
in an E. coli GLT-deficient strain that GlcP of this review to Joseph Lengeler, who has introduced us to this
M. smegmatis is a glucose permease with biochemical fascinating area of research.
features similar to GlcP of S. coelicolor (Pimentel-Schmitt
et al., 2008). Further analysis regarding the function and
regulation of the two M. smegmatis transporters is currently
in progress. Interestingly, both systems are not present in
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Ins and outs of glucose transport systems in eubacteria

Correspondence: Fritz Titgemeyer, Abstract

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Editor: Keith Chater

level in more than 20 different bacterial species (Fig. 1 and

FEMS Microbiol Rev 32 (2008) 891907

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SGLT Vibrio furnissii

Table 1. Bacterial glucose transport systems

PTS MFS ABC SGLT GlcU References

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MFS, major facilitator super family.

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FEMS Microbiol Rev 32 (2008) 891907

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FEMS Microbiol Rev 32 (2008) 891907

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FEMS Microbiol Rev 32 (2008) 891907

Downloaded from http://femsre.oxfordjournals.org/ by guest on April 2, 2016

Downloaded from http://femsre.oxfordjournals.org/ by guest on April 2, 2016

FEMS Microbiol Rev 32 (2008) 891907

Downloaded from http://femsre.oxfordjournals.org/ by guest on April 2, 2016

Downloaded from http://femsre.oxfordjournals.org/ by guest on April 2, 2016

FEMS Microbiol Rev 32 (2008) 891907

Downloaded from http://femsre.oxfordjournals.org/ by guest on April 2, 2016

Downloaded from http://femsre.oxfordjournals.org/ by guest on April 2, 2016

FEMS Microbiol Rev 32 (2008) 891907

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