production, at the end of filaments, of conidia, cells that allow
them to resist and spread in the environment. Multicellularity
has, in the same way, emerged six times in eukaryotes: in
Metazoa and Fungi (Opisthokonta), in Amoebobionta
(Dictyostelium), in Rhodobionta and Viridiplantae
(Archaeplastida), and in Chromobionta (Stramenopiles). It
should be noted that unicellular organisms may be derived
from multicellular ancestors, which is the case of some Saccharomyces and Candida (Fungi, Opisthokonta).
There remains the question of where to place coenocytic
eukaryotes such as Oobionta (Stramenopiles) and Caulerpa
(Viridiplantae). Should they be considered as a single cell?
Or should as multicellular because of the many nuclei
(sometimes millions) in their cytoplasm? (Fig. 5.6d).
Although Oobionta can be microscopic, some species are
macroscopic. The vegetative apparatus of Caulerpa can
measure several tens of centimeters or several meters. The
Dinobionta Haplozoon axiothellae, who lives in the intestine
of the annelid (Axiothella rubrocincta; Leander et al. 2002),
is an intermediate situation between cellular and syncytial
structures, a filament is outlined, with some unseparated
cells and several nuclei (Fig. 5.6e).
There is also the case of giant cells, such as Acetabularia
(Viridiplantae, eukaryotes). The organism consists of a single cell with a calcified wall, can measure up to 10 cm in
length (Fig. 5.6a), exhibits a single nucleus, and is therefore
undoubtedly unicellular, although, as for Caulerpa, it does
not correspond to the idea usually associated with the notion
of unicellularity: the microscopic size.
Finally, we must take into account the practices of
microbiologists who regarded microorganisms as (1) all
prokaryotes, even when they are clearly multicellular; (2)
single-celled eukaryotes; (3) most taxa which lie on the
borderline between unicellularity and multicellularity, primarily when they are microscopic or submicroscopic; and
(4) a number of organisms traditionally grouped under the
term “fungi” (customary meaning) (cf. Chap. 7). For the
latter, the reason is understandable: they are unicellular or
clearly multicellular, fungi represent, with some prokaryotes
and unicellular eukaryotes, a significant risk to humans
(human health, agriculture, aquaculture, etc.).
5.3
The Role of Gene Transfers
in the Evolution of Life
Our vision of the evolution of the living world initially based
solely on vertical gene transfers has been modified to take
into account horizontal gene transfers (HGT; cf. Chap. 12).
These transfers were demonstrated for the first time based on
work on antibiotic resistance, which can spread rapidly
between bacteria in hospitals. This spread has been shown
to occur through the transfer of resistance factors, later
identified as DNA. Thus, the transmission of genetic information and the evolution of the bacterial world are not only
vertical but also horizontal. Bacteria exchange DNA
fragments by various means such as cell-cell conjugation,
transformation with naked DNA, or through transduction
brought about by bacteriophages. These mechanisms allow
the exchange of genes between very distant taxa, such as that
between Escherichia coli and the yeast Saccharomyces
cerevisiae (Nishikawa et al. 1992). The quantitative importance and frequency of such transfers in the evolution of life
are increasingly taken into account. In Escherichia coli, 755
of its 4,288 genes could come from horizontal transfers
(Lawrence and Ochman 1998), although this number is
hotly debated (Daubin et al. 2001).
Environments where bacteria coexist in great abundance
are particularly favorable to gene exchanges (e.g., rhizosphere, biofilms, and microbial mats).
The DNA molecule is intrinsically resistant, much more
so than RNA, which explains that it can maintain itself in the
environment (soil, sediment, etc.) long after cell death. It can
bind to charged regions of solid components, e.g., to calcium
ions on clays. It can then be incorporated into naturally
transformable bacteria that will then express a new phenotype. The quantitative importance of this type of exchange
remains difficult to assess at this time.
Extracellular DNA in the environment thus constitutes
an important reservoir of genetic information for
microorganisms that can have access to it. The conditions
under which microorganisms can incorporate some of the
“metagenome” remain little known. There may be enzyme
systems that facilitate such a “fishing,” or specific physiological or physicochemical conditions such as acidification
of the environment, or a reduction in size which allows
bacteria to penetrate crevices where the metagenomic
DNA lies. In addition, meteorological phenomena such as
lightning create strong electric fields which cause the
incorporation of extracellular DNA by the phenomenon
of transformative electroporation of bacteria (Ce ´re ´monie
et al. 2004).
Insertion sequence (IS)* allows the insertion of a DNA
fragment into the genome of its host cell. There are several
types of IS, and they are present in almost all organisms.
Each IS tends to increase its number of copies per genome.
We thus find up to 26 copies of IS981 in Lactococcus lactis
(Polzin and McKay 1991).
Overall, the tree of life, especially that of Bacteria and
Archaea, is certainly far from the regularly connecting
one that has dichotomous branchings found in traditional
phylogenetic trees. It probably looks more like the one
proposed by Doolittle (1999) called the “reticulated” or
“cross-linked” tree (Fig. 5.7).
5 Systematic and Evolution of Microorganisms: General Concepts
121
them to resist and spread in the environment. Multicellularity
has, in the same way, emerged six times in eukaryotes: in
Metazoa and Fungi (Opisthokonta), in Amoebobionta
(Dictyostelium), in Rhodobionta and Viridiplantae
(Archaeplastida), and in Chromobionta (Stramenopiles). It
should be noted that unicellular organisms may be derived
from multicellular ancestors, which is the case of some Saccharomyces and Candida (Fungi, Opisthokonta).
There remains the question of where to place coenocytic
eukaryotes such as Oobionta (Stramenopiles) and Caulerpa
(Viridiplantae). Should they be considered as a single cell?
Or should as multicellular because of the many nuclei
(sometimes millions) in their cytoplasm? (Fig. 5.6d).
Although Oobionta can be microscopic, some species are
macroscopic. The vegetative apparatus of Caulerpa can
measure several tens of centimeters or several meters. The
Dinobionta Haplozoon axiothellae, who lives in the intestine
of the annelid (Axiothella rubrocincta; Leander et al. 2002),
is an intermediate situation between cellular and syncytial
structures, a filament is outlined, with some unseparated
cells and several nuclei (Fig. 5.6e).
There is also the case of giant cells, such as Acetabularia
(Viridiplantae, eukaryotes). The organism consists of a single cell with a calcified wall, can measure up to 10 cm in
length (Fig. 5.6a), exhibits a single nucleus, and is therefore
undoubtedly unicellular, although, as for Caulerpa, it does
not correspond to the idea usually associated with the notion
of unicellularity: the microscopic size.
Finally, we must take into account the practices of
microbiologists who regarded microorganisms as (1) all
prokaryotes, even when they are clearly multicellular; (2)
single-celled eukaryotes; (3) most taxa which lie on the
borderline between unicellularity and multicellularity, primarily when they are microscopic or submicroscopic; and
(4) a number of organisms traditionally grouped under the
term “fungi” (customary meaning) (cf. Chap. 7). For the
latter, the reason is understandable: they are unicellular or
clearly multicellular, fungi represent, with some prokaryotes
and unicellular eukaryotes, a significant risk to humans
(human health, agriculture, aquaculture, etc.).
5.3
The Role of Gene Transfers
in the Evolution of Life
Our vision of the evolution of the living world initially based
solely on vertical gene transfers has been modified to take
into account horizontal gene transfers (HGT; cf. Chap. 12).
These transfers were demonstrated for the first time based on
work on antibiotic resistance, which can spread rapidly
between bacteria in hospitals. This spread has been shown
to occur through the transfer of resistance factors, later
identified as DNA. Thus, the transmission of genetic information and the evolution of the bacterial world are not only
vertical but also horizontal. Bacteria exchange DNA
fragments by various means such as cell-cell conjugation,
transformation with naked DNA, or through transduction
brought about by bacteriophages. These mechanisms allow
the exchange of genes between very distant taxa, such as that
between Escherichia coli and the yeast Saccharomyces
cerevisiae (Nishikawa et al. 1992). The quantitative importance and frequency of such transfers in the evolution of life
are increasingly taken into account. In Escherichia coli, 755
of its 4,288 genes could come from horizontal transfers
(Lawrence and Ochman 1998), although this number is
hotly debated (Daubin et al. 2001).
Environments where bacteria coexist in great abundance
are particularly favorable to gene exchanges (e.g., rhizosphere, biofilms, and microbial mats).
The DNA molecule is intrinsically resistant, much more
so than RNA, which explains that it can maintain itself in the
environment (soil, sediment, etc.) long after cell death. It can
bind to charged regions of solid components, e.g., to calcium
ions on clays. It can then be incorporated into naturally
transformable bacteria that will then express a new phenotype. The quantitative importance of this type of exchange
remains difficult to assess at this time.
Extracellular DNA in the environment thus constitutes
an important reservoir of genetic information for
microorganisms that can have access to it. The conditions
under which microorganisms can incorporate some of the
“metagenome” remain little known. There may be enzyme
systems that facilitate such a “fishing,” or specific physiological or physicochemical conditions such as acidification
of the environment, or a reduction in size which allows
bacteria to penetrate crevices where the metagenomic
DNA lies. In addition, meteorological phenomena such as
lightning create strong electric fields which cause the
incorporation of extracellular DNA by the phenomenon
of transformative electroporation of bacteria (Ce ´re ´monie
et al. 2004).
Insertion sequence (IS)* allows the insertion of a DNA
fragment into the genome of its host cell. There are several
types of IS, and they are present in almost all organisms.
Each IS tends to increase its number of copies per genome.
We thus find up to 26 copies of IS981 in Lactococcus lactis
(Polzin and McKay 1991).
Overall, the tree of life, especially that of Bacteria and
Archaea, is certainly far from the regularly connecting
one that has dichotomous branchings found in traditional
phylogenetic trees. It probably looks more like the one
proposed by Doolittle (1999) called the “reticulated” or
“cross-linked” tree (Fig. 5.7).
5 Systematic and Evolution of Microorganisms: General Concepts
121