S
ymbionts and pathogens
are comparable in that
they colonize eukaryotic
hosts. Many pathogenic and
symbiotic genetic determi-
nants are located on mobile
genetic elements. Horizontal
gene transfer contributes to
the genetic variability of or-
ganisms, which drives the
evolution of the microorgan-
ism–host interaction. Whereas
pathogenic interactions result
in damage or death of the re-
spective host, symbiotic inter-
actions are characterized by an
overall benefit (Table 1). In
spite of these different out-
comes, similar mechanisms of pathogenesis and sym-
biosis exist in bacteria to facilitate successful col-
onization of a particular niche. The most notable
mechanisms include quorum sensing and the two-
component regulatory systems, which allow adap-
tation to the constantly changing conditions found in
a new niche. Furthermore, pathogens and possibly
also symbionts are able to modulate the host environ-
ment by type III secretion of effector molecules that
interfere directly with host cellular functions. Of
equal importance is the contribution of the host, an
aspect which has been difficult to address because of
the lack of experimental tractability. Clearly, features
such as host immunity and susceptibility play an im-
portant role in the bacteria–host interaction and a full
understanding of this interaction will therefore only
be accomplished by taking an integrated approach.
Horizontal gene transfer
Genetic variability plays an important role in the evo-
lution of pathogenic and symbiotic interactions. In
addition to the chromosome, most prokaryotes pos-
sess different classes of mobile genetic elements
that allow the acquisition, loss or structural change of
sometimes large regions of the bacterial genome.
Horizontal gene transfer represents a powerful
mechanism by which the outcome of a bacteria–host
interaction can be permanently altered.
Horizontal gene transfer is mediated by genomic
islands, plasmids, transposons and IS elements, and
phages (Table 2). Genomic islands encode functions
relevant for bacteria–host interactions and are found
in diverse animal and plant pathogens (where they are
known as pathogenicity is-
lands) and also in the sym-
biont Mesorhizobium loti (a
symbiosis island)
1
. Plasmids
can also encode many impor-
tant pathogenic determinants
such as toxins, type III secre-
tion systems and invasion
determinants
2
. The plasmids
of the aphid endosymbiont
Buchnera aphidicola contain
biosynthetic operons that
complement the amino acid
deficiency of the host
3
. The
sym-plasmid of Rhizobium,
which carries essential genes
for symbiotic competence,
might have been derived from
the plant pathogen Agrobacterium tumefaciens
4
.
Lysogenic phages integrated in the bacterial genome
are often associated with the production of virulence
factors, such as toxins, in diverse pathogens and also
in the symbiont Xenorhabdus nematophilus
2,5
. There
is also evidence for horizontal gene transfer of the IS
element IS1312 from the plant symbiont Rhizobium
meliloti to the plant pathogen A. tumefaciens
6
. Taken
together, there is increasing evidence of horizontal
gene transfer between animal and plant pathogens
and between plant pathogens and symbionts. This
suggests that horizontal gene transfer might be a
mechanism by which genetic information can be ex-
changed between pathogens and symbionts in general.
Quorum sensing
Quorum sensing describes the ability of bacteria to
sense cell densities and to regulate specific sets of
genes accordingly
7
. It is mediated via specific sig-
nalling molecules called autoinducers (AI), which
accumulate extracellularly as cell density increases.
When a threshold concentration of the AI is reached,
gene expression of density-dependent genes is initi-
ated. Fundamental to this phenomenon are two genes,
one synthesizing the AI (LuxI or a homologue) and
the other serving as an AI receptor (LuxR or a
homologue). Most but not all quorum-sensing mech-
anisms analysed play a specific role in symbiont– or
pathogen–host interactions.
Quorum sensing regulates the virulence properties
of various plant and animal pathogens. Examples in-
clude the production of cell wall degrading enzymes
and carbapenem antibiotics in the plant pathogen
Traditionally, symbiotic and pathogenic
interactions were considered different
manifestations of the bacteria–host
interaction. However, the molecular
mechanisms that mediate communication
between and cellular modulation of the
involved partners are quite similar. With
this review we aim to contribute to a
reduction of the traditional gap between
symbiosis and pathogenesis research.
U. Hentschel*, M. Steinert and J. Hacker are in the
Institut für Molekulare Infektionsbiologie,
Universität Würzburg, Röntgenring, 11,
D-97070 Würzburg, Germany.
*tel: +49 931 312588,
fax: +49 931 312578,
e-mail: ute.hentschel@mail.uni-wuerzburg.de
R EVIEWS
TRENDS IN MICROBIOLOGY
226
VOL. 8 NO. 5 MAY 2000
0966-842X/00/$ - see front matter © 2000 Elsevier Science Ltd. All rights reserved. PII: S0966-842X(00)01758-3
Common molecular mechanisms of
symbiosis and pathogenesis
Ute Hentschel, Michael Steinert and Jörg Hacker