specialized transduction (sometimes qualified as restricted
transduction) (Thomas and Nielsen 2005). The generalized
transduction involves virulent phages (lytic) and allows
transferring any region of a bacterial genome. By contrast,
phages involved in specialized transduction are called temperate. This mechanism allows transferring specific regions
of the bacterial chromosome. The generalized transduction
starts with infection of a bacterium by a virulent phage that
injects its DNA into the cell cytoplasm (Fig. 12.3a). The
viral DNA is replicated by the replication machinery of the
host cell (Fig. 12.3b), whereas the genome of the cell is
degraded (Fig. 12.3c). At the same time, viral capsids are
synthesized. The packaging of the newly synthesized
genomes allows forming new viral particles (Fig. 12.3d).
At this stage, portions of the genome of the infected cell
can be packaged into capsids instead of viral genomes
(Fig. 12.3d). The resulting particles are called transducing
particles. The incorporation of some bacterial genetic material occurs in ~1 % of the new virions. During the lysis of the
infected cells, transducing particles are released into the
environment like other viral particles. They can bind to
(Fig. 12.3e) and infect other cells (Fig. 12.3f). However,
because transducing particles do not contain viral DNA,
they are not replicated into the host cell and do not cause
its lysis. In some cases, the DNA of the transducing particle
is integrated through recombination processes into the chromosome of the host and can thus be transmitted to its
offspring (Fig. 12.3g). If no recombination occurs, the
genes carried by the DNA of the transducing particle can
be expressed for a while, but the corresponding genomic
fragment disappears rapidly because it will be transmitted
to only one of the daughter cells during the division of the
recipient cell. Therefore, it cannot be fixed in the cell population. This phenomenon is called abortive transduction.
The specialized transduction involves temperate phages
that are able to integrate at a specific location of the cell
chromosome. Integrated temperate phages are called
prophages. They lose their replicative autonomy. They are
replicated at the same time that the chromosome of the host
and are transmitted to the two daughter cells during cell
division. The integration sites are very specific, meaning
that a given bacteriophage will always be integrated at
the same location in the genome of its host. For instance,
in E. coli, the integration site of the λ phage is located close
to an operon involved in galactose degradation. A cell
carrying an integrated phage is called a lysogen, and the
replication cycle of the phage is called lysogenic. The viral
genes can be expressed by the cell and impact its phenotype (this is called lysogenic conversion). For example,
some phages encode genes repressing the expression of
their own genes. The main consequence is that host cells
become immunized against infection by phages of the
same type.
The integration of prophages is not irreversible. They can
be excised from the chromosome of the host spontaneously,
but their excision can also be induced by environmental or
physiological stimuli (e.g., exposure to UV or X-rays, stress
of the host cell). The excision of the prophage initiates a lytic
cycle, leading to the formation of virus particles that are
released during the cell lysis. In some cases, the excision of
the prophage can be abnormal, leading to the formation of a
hybrid DNA molecule made of viral and host DNA. In the
case of the λ phage of E. coli, a piece of the galactose operon
can be integrated to the phage genome. In return, a part of
the prophage genome remains integrated into the host chromosome. The viral particles carrying pieces of the host
genome can serve as shuttle for HGT during the next cycle
of infection. Indeed, because they contain a part of viral
DNA, these phages are able to replicate in the newly infected
cells, increasing the probability of inserting the genes they
carry on the bacterial chromosome. The effectiveness of
specialized transduction is thus much higher than that of
generalized transduction, even if only a subset of genes can
be transferred by this mechanism.
Viruses are extremely abundant in many natural
environments. For instance, the amount of viral particles in
marine environments can exceed by several orders of magnitude than that of cells (Suttle 2007). The main consequence is that marine organisms, and especially
microorganisms, are constantly exposed to viral infections.
Viruses are thus major players of the regulation of bacterial
populations and of HGT.
12.2.2 Fate of the Transferred DNA
Following its entry into the recipient cell (Fig. 12.4a), the
“foreign” (or exogenous) DNA is the target of a series of
processes that determine its fate, namely, its maintenance in
the recipient cell and the transmission to its offspring or its
fast disappearance. First, the foreign DNA can be directly
degraded (Fig. 12.4b) or be cut into pieces by the
endonucleases present in the cytoplasm of the recipient cell
(Fig. 12.4c). This cleavage step involves generally a system of
modification/restriction (M/R) such as the hsd system of E.
coli. Several M/R systems have been described in
prokaryotes, but all involve a methylase and an endonuclease,
also called restriction enzyme (for a detailed review of these
systems, see Murray 2000). The functioning of these systems
is simple. The methylase recognizes and methylates specific
bases of the DNA. This methylation process protects the DNA
molecule from the action of the endonuclease. The M/R
systems are highly variable from one species to another and
sometimes even from one strain to another. The main consequence is that the methylation process allows very specific
DNA labeling and therefore an accurate distinction between
450
C. Brochier-Armanet and D. Moreira
transduction) (Thomas and Nielsen 2005). The generalized
transduction involves virulent phages (lytic) and allows
transferring any region of a bacterial genome. By contrast,
phages involved in specialized transduction are called temperate. This mechanism allows transferring specific regions
of the bacterial chromosome. The generalized transduction
starts with infection of a bacterium by a virulent phage that
injects its DNA into the cell cytoplasm (Fig. 12.3a). The
viral DNA is replicated by the replication machinery of the
host cell (Fig. 12.3b), whereas the genome of the cell is
degraded (Fig. 12.3c). At the same time, viral capsids are
synthesized. The packaging of the newly synthesized
genomes allows forming new viral particles (Fig. 12.3d).
At this stage, portions of the genome of the infected cell
can be packaged into capsids instead of viral genomes
(Fig. 12.3d). The resulting particles are called transducing
particles. The incorporation of some bacterial genetic material occurs in ~1 % of the new virions. During the lysis of the
infected cells, transducing particles are released into the
environment like other viral particles. They can bind to
(Fig. 12.3e) and infect other cells (Fig. 12.3f). However,
because transducing particles do not contain viral DNA,
they are not replicated into the host cell and do not cause
its lysis. In some cases, the DNA of the transducing particle
is integrated through recombination processes into the chromosome of the host and can thus be transmitted to its
offspring (Fig. 12.3g). If no recombination occurs, the
genes carried by the DNA of the transducing particle can
be expressed for a while, but the corresponding genomic
fragment disappears rapidly because it will be transmitted
to only one of the daughter cells during the division of the
recipient cell. Therefore, it cannot be fixed in the cell population. This phenomenon is called abortive transduction.
The specialized transduction involves temperate phages
that are able to integrate at a specific location of the cell
chromosome. Integrated temperate phages are called
prophages. They lose their replicative autonomy. They are
replicated at the same time that the chromosome of the host
and are transmitted to the two daughter cells during cell
division. The integration sites are very specific, meaning
that a given bacteriophage will always be integrated at
the same location in the genome of its host. For instance,
in E. coli, the integration site of the λ phage is located close
to an operon involved in galactose degradation. A cell
carrying an integrated phage is called a lysogen, and the
replication cycle of the phage is called lysogenic. The viral
genes can be expressed by the cell and impact its phenotype (this is called lysogenic conversion). For example,
some phages encode genes repressing the expression of
their own genes. The main consequence is that host cells
become immunized against infection by phages of the
same type.
The integration of prophages is not irreversible. They can
be excised from the chromosome of the host spontaneously,
but their excision can also be induced by environmental or
physiological stimuli (e.g., exposure to UV or X-rays, stress
of the host cell). The excision of the prophage initiates a lytic
cycle, leading to the formation of virus particles that are
released during the cell lysis. In some cases, the excision of
the prophage can be abnormal, leading to the formation of a
hybrid DNA molecule made of viral and host DNA. In the
case of the λ phage of E. coli, a piece of the galactose operon
can be integrated to the phage genome. In return, a part of
the prophage genome remains integrated into the host chromosome. The viral particles carrying pieces of the host
genome can serve as shuttle for HGT during the next cycle
of infection. Indeed, because they contain a part of viral
DNA, these phages are able to replicate in the newly infected
cells, increasing the probability of inserting the genes they
carry on the bacterial chromosome. The effectiveness of
specialized transduction is thus much higher than that of
generalized transduction, even if only a subset of genes can
be transferred by this mechanism.
Viruses are extremely abundant in many natural
environments. For instance, the amount of viral particles in
marine environments can exceed by several orders of magnitude than that of cells (Suttle 2007). The main consequence is that marine organisms, and especially
microorganisms, are constantly exposed to viral infections.
Viruses are thus major players of the regulation of bacterial
populations and of HGT.
12.2.2 Fate of the Transferred DNA
Following its entry into the recipient cell (Fig. 12.4a), the
“foreign” (or exogenous) DNA is the target of a series of
processes that determine its fate, namely, its maintenance in
the recipient cell and the transmission to its offspring or its
fast disappearance. First, the foreign DNA can be directly
degraded (Fig. 12.4b) or be cut into pieces by the
endonucleases present in the cytoplasm of the recipient cell
(Fig. 12.4c). This cleavage step involves generally a system of
modification/restriction (M/R) such as the hsd system of E.
coli. Several M/R systems have been described in
prokaryotes, but all involve a methylase and an endonuclease,
also called restriction enzyme (for a detailed review of these
systems, see Murray 2000). The functioning of these systems
is simple. The methylase recognizes and methylates specific
bases of the DNA. This methylation process protects the DNA
molecule from the action of the endonuclease. The M/R
systems are highly variable from one species to another and
sometimes even from one strain to another. The main consequence is that the methylation process allows very specific
DNA labeling and therefore an accurate distinction between
450
C. Brochier-Armanet and D. Moreira