Antonie van Leeuwenhoek 81: 233–243, 2002.
© 2002 Kluwer Academic Publishers. Printed in the Netherlands.
233
Cell to cell communication by autoinducing peptides in gram-positive
bacteria
Mark H.J. Sturme
1,*
, Michiel Kleerebezem
2,3
, Jiro Nakayama
4
, Antoon D.L. Akkermans
1
,
Elaine E. Vaughan
1,3
& Willem M. de Vos
1,3
1
Laboratory of Microbiology, Wageningen University, Hesselink van Suchtelenweg 4, 6703 CT, Wageningen, the
Netherlands;
2
NIZO Food Research, Kernhemseweg 2, PO Box 20, 6710 BA Ede, the Netherlands;
3
Wageningen
Centre for Food Sciences, Wageningen, the Netherlands;
4
Department of Bioscience and Biotechnology, Faculty of
Agriculture, Kyushu University, 6-10-1 Hakozaki, Higashi-ku, Fukuoka 812-8581, Japan (
*
Corresponding author:
E-mail: mark.sturme@algemeen.micr.wau.nl)
Key words: autoinducing peptides, Gram-positive bacteria, quorum sensing, two-component regulatory systems
Abstract
While intercellular communication systems in Gram-negative bacteria are often based on homoserine lactones as
signalling molecules, it has been shown that autoinducing peptides are involved in intercellular communication in
Gram-positive bacteria. Many of these peptides are exported by dedicated systems, posttranslationally modified
in various ways, and finally sensed by other cells via membrane-located receptors that are part of two-component
regulatory systems. In this way the expression of a variety of functions including virulence, genetic competence and
the production of antimicrobial compounds can be modulated in a co-ordinated and cell density- and growth phase-
dependent manner. Occasionally the autoinducing peptide has a dual function, such as in the case of nisin that is
both a signalling pheromone involved in quorum sensing and an antimicrobial peptide. Moreover, biochemical,
genetic and genomic studies have shown that bacteria may contain multiple quorum sensing systems, underlining
the importance of intercellular communication. Finally, in some cases different peptides may be recognised by
the same receptor, while also hybrid receptors have been constructed that respond to new peptides or show novel
responses. This paper provides an overview of the characteristics of autoinducing peptide-based quorum sensing
systems, their application in various gram-positive bacteria, and the discovery of new systems in natural and
engineered ecosystems.
Introduction
It has been shown for several bacteria that a variety
of physiological changes in the bacterial population
are dependent on specific cell densities and growth
phases. This phenomenon of cell density-dependent
gene expression has been termed quorum sensing,
and was first found in the control of biolumines-
cence in Vibrio fischeri (Fuqua et al. 1994). Usually
quorum sensing occurs at high cell densities, but in
some cases also at relatively low densities, as was
shown for genetic competence in Streptococcus pneu-
moniae (Håvarstein et al. 1995b). Many other quorum
sensing systems have been discovered since, in both
Gram-negative and Gram-positive bacteria. Examples
in Gram-negative bacteria include biofilm-formation
and virulence in Pseudomonas aeroginosa (Winson et
al. 1995; Singh et al. 2000), root-nodule formation
by Rhizobium leguminosarum (Gray et al. 1996), and
swarming motility of Serratia liquefaciens (Eberl et
al. 1996). A comprehensive review on quorum sens-
ing in Gram-negative bacteria is given in Whitehead et
al. (2001). In Gram-positive bacteria quorum sensing
regulation has been shown for: genetic competence in
Bacillus subtilis (Tortosa & Dubnau 1999) and Strep-
tococcus pneumoniae (Cheng et al. 1997), virulence
in Staphylococcus aureus (Novick 1999), and the pro-
duction of antimicrobial peptides, including bacteri-
ocins and lantibiotics, in lactic acid bacteria (Kleere-
bezem et al. 1997a; Risøen et al. 2000). In these
quorum sensing systems bacteria produce extracellular
signalling molecules that are responsible for the com-