Unformatted text preview: EMBO reports Ecological fitness, genomic islands and bacterial
A Darwinian view of the evolution of microbes
Jörg Hacker+ & Elisabeth Carniel1
Institut für Molekulare Infektionsbiologie der Universität Würzburg, Röntgenring 11, 97070 Würzburg, Germany and 1Institut Pasteur, Unité de Bactériologie
Moléculaire et Médicale, Yersinia laboratory, 28 rue du Dr Roux, 75724 Paris Cedex 15, France
Received October 26, 2000; revised March 14, 2001; accepted March 26, 2001 The compositions of bacterial genomes can be changed
rapidly and dramatically through a variety of processes
including horizontal gene transfer. This form of change is key
to bacterial evolution, as it leads to ‘evolution in quantum
leaps’. Horizontal gene transfer entails the incorporation of
genetic elements transferred from another organism—perhaps
in an earlier generation—directly into the genome, where they
form ‘genomic islands’, i.e. blocks of DNA with signatures of
mobile genetic elements. Genomic islands whose functions
increase bacterial fitness, either directly or indirectly, have
most likely been positively selected and can be termed ‘fitness
islands’. Fitness islands can be divided into several subtypes:
‘ecological islands’ in environmental bacteria and ‘saprophytic
islands’, ‘symbiosis islands’ or ‘pathogenicity islands’ (PAIs) in
microorganisms that interact with living hosts. Here we discuss
ways in which PAIs contribute to the pathogenic potency of
bacteria, and the idea that genetic entities similar to genomic
islands may also be present in the genomes of eukaryotes. Introduction
Bacteria, which have existed for more than 3 billion years,
represent the most ancient forms of life on the earth. The
enormous evolutionary potential of these organisms is illustrated
by the fact that the innumerable species currently living differ in
many properties including metabolic capacities, cell surface
compositions, life styles, ecological niches and host specificities
(Doolittle, 1999). From a Darwinian point of view, every living
organism is a result of the driving forces of evolution, which
include the plasticity of the genome and the rate of phenotype +Corresponding generation, as well as the selective pressures exerted by the
environment (Arber, 2000). The capacity for change, as determined by these factors, forms the basis of evolutionary progress.
In eukaryotes, genetic variability is primarily the result of
sexual reproduction, which involves chromosomal recombination
during meiosis. In prokaryotes, where this form of shuffling is not
available, other factors determine the rate of evolution. These
include the frequent occurrence of point mutants, high levels of
recombination and gene silencing, and the transfer of genetic
material between different bacterial species—even genera. In
particular the latter process, referred to as horizontal gene
transfer, represents a cornerstone of bacterial evolution, and it
has led to dramatic changes in the composition of microbial
genomes over relatively short time periods (Ochman et al.,
2000). Prokaryotic genomes: core and
flexible gene pools
Bacterial genes may be transmitted between different organisms
via conjugation, transduction and natural transformation. The
former two processes require specific gene ferries, such as
plasmids or bacterial viruses, which transport bacterial DNA
along with their own sequences from donor to recipient cells.
The majority of the horizontally transferred DNA is part of the
flexible bacterial gene pool. In addition to phages and plasmids,
the flexible gene pool comprises conjugative transposons,
‘simple’ transposons, integrons, ‘genomic islets’ (<10 kb), and
‘genomic islands’ (>10 kb) (Figure 1). In contrast, the core gene author. Tel: +49 931 312575; Fax: +49 931 312578; E-mail: [email protected] 376 EMBO reports vol. 2 | no. 5 | pp 376–381 | 2001 © 2001 European Molecular Biology Organization review
Microbial evolution Fig. 2. Schematic model of a genomic island of bacteria (upper part). The
formerly transferred DNA block is linked to a tRNA gene and flanked by
direct repeats (DR). The guanine plus cytosine (G+C) content of the genomic
island is different from that of the core genome (lower part). Other
abbreviations: int, integrase gene; abc, def and ghi, genes encoding specific
functions; IS, insertion sequence element; bp, base pair. Fig. 1. Model of the DNA pools in the genomes of prokaryotes. The DNA
elements comprising the core as well as the flexible gene pools are presented
in the circles. Functions encoded by the pools are given in the lower part of
the diagram. pool is restricted to genes that are part of the bacterial chromosome, except in a few species (e.g. in Streptomyces) for which
plasmids also may be included (del Solar et al., 1995). The
majority of the genes of the core gene pool encode proteins that
play roles in basic cellular functions (e.g. translation, metabolism,
architecture) and exhibit rather homogeneous G+C contents and
codon usage. DNA elements from the flexible gene pool, on the
other hand, often have features characteristic of transferred
elements (different G+C content and codon usage, presence of
mobility genes) and encode additional functions that are not
essential for bacterial growth but provide advantages under
particular conditions (changes in the environment, entry into a
new host, etc.). Although the majority of the genes of the flexible
gene pool seem to confer selective advantages to their bacterial
recipients, a few (IS elements, prophages, restriction/modification
systems) represent ‘selfish’ DNA-molecules, whose only mission
is to promote their own spread (Lilley et al., 2000). As indicated
in Figure 1, some genes may belong to both the core and flexible
pools, but the majority belong to either one or the other. Perhaps
not surprisingly, the number of genes within a cell that belong to
the flexible pool may vary from 18% (Escherichia coli K-12) to
<1% (Mycoplasma) of the total genome (Lawrence and
Ochman, 1998; Ochman et al., 2000). Genomic islands: elements of the
flexible gene pool
In recent years, ‘pathogenicity islands’ (PAIs) have attracted a
great deal of attention (Kaper and Hacker, 1999). First described
in the genomes of pathogenic E. coli, they were subsequently also found in other pathogens, where they form specific entities
associated with bacterial pathogenicity (Blum et al., 1994).
Sequencing of several entire genomes revealed that PAIs are
much more widespread than previously thought, and represent a
paradigm of more general genetic entities that are present in the
genomes of many bacterial species and are termed genomic
islands (Strauss and Falkow, 1997; Hacker and Kaper, 2000).
Genomic islands are part of the flexible bacterial gene pool
and are somewhere between 10 and 100 kilobases (kb) in length
(see Figure 2). They frequently harbor phage- and/or plasmidderived sequences, including transfer genes or integrases and
IS elements. These particular blocks of DNA are most often
inserted into tRNA genes and may be unstable. This instability
appears to be mediated by flanking direct repeats which are
often homologous to phage attachment sites and promote
integration into, and excision out of, the bacterial genome
(Hacker et al., 1997; Buchrieser et al., 1998). In addition to
mobility loci, genomic islands carry gene clusters with specific
functions. As for other elements of the flexible gene pool, the
majority of these islands differ from the core genome with
respect to their G+C content and codon usage. The evolutionary
advantage of genomic islands over smaller inserts (‘islets’) is that
a large number of genes (e.g. operons, gene clusters encoding
related functions) may be transferred and incorporated en bloc
into the recipient genome. This transfer may lead to dramatic
changes in the behavior of the organism, resulting ultimately in
‘evolution in quantum leaps’ (Groisman and Ochman, 1996;
Finlay and Falkow, 1997). A wide range of functions
Sequence analysis revealed that genomic islands carry selfish
genes, especially of the type that encode proteins with transfer,
recombination and restriction/modification properties. However,
the majority of the clusters located on these genetic elements
encode functions that can be useful for the survival and
EMBO reports vol. 2 | no. 5 | 2001 377 review
J. Hacker & E. Carniel
Table I. Functions encoded by fitness islands
Subtypes of fitness islands Function Organism Increased pathogenicity PAI iron uptake Yersinia spp. + SAI iron uptake fecal E. coli – ECI iron uptake Klebsiella spp. – ECI sucrose uptake Salmonella senftenberg – ECI degradation of phenols Pseudomonas putida – PAI toxin production Vibrio cholerae + SAI adhesins fecal E. coli – PAI adhesins urinary E. coli ECI methicillin resistance Staphylococcus aureus – ECI multi-resistance Shigella flexneri – SYI nitrogen fixation Mesorhizobium loti – type III-system Salmonella enterica + type III-system Shigella flexneri PAI type III-system PAI Yersinia spp. + type III-system SYI Sinorhizobium fredii – type IV-system + Legionella pneumophila + type IV-system EAI Helicobacter pylori type IV-system E. coli F-plasmid – PAI, pathogenicity island; SYI, symbiosis island; SAI, saprophytic island; ECI, ecological island. transmission of the microbes (Table I). Thus, they may provide a
selective advantage to the island-carrying organisms within a
population. For instance, DNA elements encoding sucroseuptake in Salmonella senftenberg are necessary for metabolic
adaptation of these bacteria to their hosts (Hochhut et al., 1997).
Other genomic islands encode iron-uptake systems which
enhance the capacity of bacteria to grow and disseminate in the
soil or in a host. This holds true for many enterobacteria and for
bacteria of the Pseudomonas group, which are part of the plant
rhizosphere. Other Pseudomonas strains carry genomic islands
that encode enzymes involved in degradation of phenolic
compounds (Ravatn et al., 1998). Genomic islands may also
carry genes encoding factors that confer resistance to antimicrobial substances. For example, the mecA-region of staphylococci
enhances survival of its carriers, both in soil compartments in
which antibiotic-producing microbes exist, and in hospitals with
strong antibiotic pressure (Ito et al., 1999). In addition, the
symbiosis islands of rhizobia carry nitrogen fixation genes
whose products are necessary for the interactions of the bacteria
with plant cells (Sullivan and Ronson, 1998). Other genomic
islands encode toxins or adherence factors involved in pathogenicity. Increasing bacterial fitness and
The progress of evolution is determined by an increase in the
fitness of the organism. Fitness, in this context, is considered to
be a set of properties that enhance the survival, spread, and/or
transmission of an organism within a specific ecological niche
(Preston et al., 1998). The Darwinian laws (‘survival of the 378 EMBO reports vol. 2 | no. 5 | 2001 fittest’) are valid for the development of eukaryotes as well as for
prokaryotes (Arber, 2000). Therefore, carrying a genomic island
may provide a selective advantage under specific environmental
conditions (stress, in vivo conditions, exposure to antibacterial
substances) because it enhances microbial transmission, survival
or colonization within a niche. From a functional point of view,
then, genomic islands that increase the fitness of the recipient
microbes should be termed ‘fitness islands’, as already suggested
by Preston et al. (1998) (Figure 3). Under these circumstances,
genomic, fitness islands confer new properties which enhance
the adaptational capacity of their bacterial host.
Fitness islands can be subdivided into different subsets,
depending on the life-style of the microbe (its niche) (Figure 3),
rather than on the intrinsic composition of the islands. Fitness
islands that help microorganisms to live in the environment or to
persist as saprophytes in a host may be considered ‘ecological
islands’ and ‘saprophytic islands, respectively. Other bacteria reside
temporarily or permanently in a host (another microorganism, a
plant or an animal), where they either provide some benefits to
the host-organism (symbiont) or cause damage to it (pathogen).
Accordingly, a ‘symbiosis island’ is a specific type of fitness
island that helps bacteria to positively interact with their hosts,
while a fitness island that participates directly or indirectly in the
induction of lesions is a true pathogenicity island. Pathogenicity islands may influence
PAIs represent a subset of genomic islands and share the same
general composition and organization (Hacker and Kaper, review
The actions of these pathogenicity factors seems to result from
direct evolutionary pressures. This is true not only for enteric,
but also respiratory pathogens, where the action of
pathogenicity factors supports their transmission and therefore
positively influences microbial evolution. Contributions to ecological adaptation
and to pathogenesis Fig. 3. Model for the development of genomic islands. Following acquisition
of transferred DNA and/or deletion of genetic material, a genomic island is
selected. If the gene products of the island enhance the fitness of the recipient,
the island-harboring bacteria will be positively selected. The gene products of
these foreign blocks of DNA can contribute to survival in the environment,
saprophytic life, symbiosis or pathogenicity. 2000). Like the saprophytic islands and the symbiosis islands,
they exert their action in a host. However, in this case, their gene
products contribute, directly or indirectly, to the pathogenic
potency of bacteria and generate lesions in the infected host
(Groisman and Ochman, 1996; Hacker et al., 1997). PAIs are
components of the genomes of many Gram positive, as well as
Gram negative, bacteria. As the Darwinian laws are also valid
for the generation of PAIs, the presence of PAIs should
contribute to the in vivo fitness of the PAI-positive bacteria and
increase their survival and/or transmission to new hosts.
In certain cases, ‘fitness properties’ are directly related to the
clinical symptoms caused by the pathogenic bacteria. An example
of a direct contribution of PAI-encoded functions to the fitness of
bacteria is found in enteropathogenic organisms. Both Vibrio
cholerae and enterotoxigenic E. coli stimulate efflux of water from
the gut of infected individuals and the resulting bacterial spread via
feces directly contributes to microbial transmission.
More generally, enhanced microbial transmission is often a
direct consequence of the action of pathogenicity factors such as
adhesins and toxins, which are encoded by PAIs, phages, or
plasmids (Waldor and Mekalanos, 1996; Karaolis et al., 1998). As already mentioned, the division of fitness islands into
different subtypes is not based on their intrinsic genetic
composition, but on their effects in a specific niche and within a
particular organism. In other words, the same fitness island may
act as an ecological island when the bacterial recipient resides
outside of a host, but become a pathogenicity island when the
bacterium enters a host. For example, the genes encoding an
iron-uptake system termed yersiniabactin are part of a genomic
island that was first identified in highly pathogenic strains of the
genus Yersinia (Carniel et al., 1996). This ‘high pathogenicity
island’ (HPI), however, is not only present in pathogenic
yersiniae, but also in harmless E. coli of the intestinal flora and
in Klebsiella from the soil (Schubert et al., 1998; Bach et al.,
2000). The iron-uptake system seems to have evolved to adapt
certain enterobacteria specifically to iron-limiting conditions. In
bacteria that reside in the environment, this island can be
considered as an ecological island with a role in cellular metabolism. If, on the other hand, the island is present in a bacterium
with a host, and it carries additional virulence features, it is a
pathogenicity island. If it is integrated in the chromosome of a
non-virulent bacterium, it may constitute a saprophytic island.
Like the iron-uptake system, adhesins may exhibit ‘dual’
functions in bacteria (Finlay and Falkow, 1997). For example,
certain adherence factors in E. coli (e.g. P-, S-, and F1C-fimbriae)
are encoded by genomic islands and are produced by
commensal strains that are part of the normal human gut flora
(Hacker, 2000). If the adhesins are involved in colonization of
the gut, the genetic entity is a saprophytic island. Under special
circumstances, however, P-, S- or F1C-positive E. coli may reach
the urinary tract, where they cause infections of the bladder or
the kidney (Khan et al., 2000), becoming true PAIs. In other
words, the PAIs of uropathogenic E. coli were originally selected
as ‘pure’ fitness islands in the gut, but then helped a particular
bacterial pathotype to emerge as the microbes colonized a new
niche, the kidney or the bladder.
Other PAIs carry genes whose products form secretion systems
of type III or IV. Again, if these secretion systems transport proteins
involved in the infectious process, they can be considered PAIs.
This is true for strains of the Salmonella- (Galán and Collmer,
1999), Shigella- (Parsot and Sansonetti, 1999), and Yersiniagroups (Cornelis et al., 1998) for the type III system, and for
Legionella pneumophila (Vogel et al., 1998) and Helicobacter
pylori (Cesini et al., 1996) for the type IV system (Table I). If,
however, the secretion systems transport proteins or even DNA
molecules of non-pathogenic organisms, as in the case of the
type III system of rhizobia, or the type IV system of F plasmids,
they do not form PAIs but rather symbiotic islands or ecological
islands which enhance the fitness of bacteria in their natural
niche (Preston et al., 1998). Therefore, the subtypes of fitness
islands depend on several criteria including not only the genetic
EMBO reports vol. 2 | no. 5 | 2001 379 review
J. Hacker & E. Carniel
composition of the island itself, but also the genetic background
of its bacterial host, and the ecological habitat of the microorganism. Driving bacterial evolution
PAIs have been selected during evolution because their
presence conferred selective advantages to their bacterial host.
However, in some instances, their acquisition might subsequently have oriented the evolution of their host bacteria. This
has probably been the case for Y. pestis, the agent of plague.
Y. pestis is a highly clonal species that emerged recently (1500
to 20 000 years ago) from Y. pseudotuberculosis (Achtmann et
al., 1999). In contrast to its progenitor which uses the oral route
to contaminate human and animal hosts, Y. pestis is transmitted
by flea bites and the septicemia that systematically occurs in the
host at the pre-mortem stage of plague is a prerequisite for
Y. pestis transmission by fleas. By promoting the systemic
dissemination and thereby the efficient transmission of the
bacteria in vivo, the HPI presumably served as one of the key
factors in the emergence of this highly dangerous microorganism. In other words, Y. pestis would probably not have
evolved from Y. pseudotuberculosis if the genome of the latter
had not already harbored the HPI. Genomic islands in eukaryotes?
Horizontal gene transfer represents an important mechanism in
the evolution of eubacteria, and genomic islands belong to the
group of genetic elements that are involved in evolutionary
progress. Recently, it has become evident that laterally transferred DNA is also present in the genomes of archeabacteria
(Doolittle, 1999), and questions regarding a role for horizontal
gene transfer in the evolution of eukaryotes (de la Cruz and
Davis, 2000; Kurland, 2000) have arisen. From our point of
view, there are good indications that this is the case, and genetic
elements with features of genomic islands have been found in
eukaryotic genomes. First, mobile genetic elements such as
retrotransposons are present even in the genomes of mammals,
where they have the capacity to jump into 3′ ends of tRNA
genes, a process that was first identified in bacterial genomes.
Secondly, the well-characterized Ti plasmid is able to transfer
genes from a prokaryotic organism, Agrobacterium tumefaciens,
to the genomes of plants, and the transferred DNA (T-region)
was recently assimilated to a PAI (Winans et al., 1999). Thirdly,
mitochondria and plastids exhibit DNA-signatures that are also
found in the genomes of prokaryotes such as rickettsia or cyanobacteria. There is speculation that these organelles were derived
from genomes of former bacterial endosymbionts (Hentschel et
al., 2000), and are thus special types of genomic islands. Last,
but not least, large ‘pathogenicity loci’, which share common
features with bacterial PAIs have been identified in the pathogenic fungus, Ustilago hordei (Lee et al., 1999). Further analysis
of eukaryotic genomes will certainly define more clearly the
roles of these elements in eukaryotic evolution by quantum
We thank Cesare Montecucco (Padua) and Ute Hentschel
(Würzburg) for discussions, Claudia Borde and Hilde Merkert for
editorial assistance. Part of the article was composed during a 380 EMBO reports vol. 2 | no. 5 | 2001 sabbatical of J.H. in the laboratory of E.C. at the Institut Pasteur,
Paris. Our own work, related to the subject of the article is
supported by the DFG (SFB 479) and the Fonds der Chemischen
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