Evidence for the Transport of Maltose by the Sucrose Permease,
CscB, of Escherichia coli
Yang Peng Æ Sanath Kumar Æ Ricardo L. Hernandez Æ
Suzanna E. Jones Æ Kathleen M. Cadle Æ
Kenneth P. Smith Æ Manuel F. Varela
Received: 18 July 2008 / Accepted: 16 February 2009 / Published online: 18 March 2009
Ó Springer Science+Business Media, LLC 2009
Abstract The purpose of this study was to examine the
sugar recognition and transport properties of the sucrose
permease (CscB), a secondary active transporter from
Escherichia coli. We tested the hypothesis that maltose
transport is conferred by the wild-type CscB transporter.
Cells of E. coli HS4006 harboring pSP72/cscB were red on
maltose MacConkey agar indicator plates. We were able to
measure ‘‘downhill’’ maltose transport and establish
deﬁnitive kinetic behavior for maltose entry in such cells.
Maltose was an effective competitor of sucrose transport in
cells with CscB, suggesting that the respective maltose and
sucrose binding sites and translocation pathways through
the CscB channel overlap. Accumulation (‘‘uphill’’ trans-
port) of maltose by cells with CscB was profound,
demonstrating active transport of maltose by CscB.
Sequencing of cscB encoded on plasmid pSP72/cscB used
in cells for transport studies indicate an unaltered primary
CscB structure, ruling out the possibility that mutation
conferred maltose transport by CscB. We conclude that
maltose is a bona ﬁde substrate for the sucrose permease of
E. coli. Thus, future studies of sugar binding, transport, and
permease structure should consider maltose, as well as
Keywords Maltose Á Sucrose Á CscB Á Permease Á
Transporter Á Secondary active transport Á Sugar Á
Substrate selection Á Symport Á Bacteria
Sucrose is a central and universal nutrient for all living
organisms, ranging from humans to bacteria. Thus, the
transport of sucrose across the biological membrane is of
major importance (Bockmann et al. 1992; Davidson and
Maloney 2007; Drozdowski and Thomson 2006; Iyer and
Camilli 2007; Neilands 1978; Neuhaus 2007; Sauer 2007).
Microorganisms such as the bacteria are useful model
organisms for the investigation of sugar transport systems.
In addition to facilitative diffusion pore systems, bacteria
utilize phosphoenolpyruvate:sugar phosphotransferase
(PTS), primary active transport, and secondary active
transport systems for the translocation of sugars across the
membrane (Davidson and Maloney 2007; Forst et al. 1998;
Nikaido and Vaara 1985; Saier et al. 1988; Varela and
The sucrose-proton permease (CscB) of Escherichia coli
is a secondary active transporter that was ﬁrst investigated
in the sucrose utilizing isolate EC3132 (Alaeddinoglu and
Charles 1979; Bockmann et al. 1992; Jahreis et al. 2002).
The cscB gene (
chromosomally encoded sucrose utilizing
gene) was cloned, sequenced, and mapped to the E. coli
chromosome locus 51 min. alongside the genes cscK
-fructokinase), cscA (sucrose hydrolase or
invertase), and cscR (repressor) (Bockmann et al. 1992;
Jahreis et al. 2002). The CscB permease is one member of
the well-known and large major facilitator superfamily
(MFS) of transporters that share conserved amino acid
sequence motifs, exhibit similar predicted two-dimensional
structures within the membrane, and are thus predicted to
have a common mechanism for solute transport across the
membrane (Baldwin and Henderson 1989; Grifﬁth et al.
1992; Maloney 1994; Marger and Saier 1993; Pao et al.
1998; Saier et al. 1999). Yet the members of the MFS
possess a diverse array of structurally distinct substrates,
such as various carbohydrates, amino acids, ions, metabolic
Yang Peng and Sanath Kumar contributed equally to this paper.
Y. Peng Á S. Kumar Á R. L. Hernandez Á S. E. Jones Á
K. M. Cadle Á K. P. Smith Á M. F. Varela (&)
Department of Biology, Eastern New Mexico University,
Roosevelt Hall, Room 101, Station 33, Portales 88130,
J Membrane Biol (2009) 228:79–88