These studies appear to confirm the existence of a correlation between phagotrophy and the acquisition of genes by
HGT, but other cases have also been characterized in nonphagotrophic species, such as chlorophytes and fungi. For
example, the analysis of the complete genome sequence of
the unicellular green alga Ostreococcus tauri has revealed
many cases of HGT, likely from bacterial donors. Surprisingly, almost all those genes are concentrated in a single
chromosome of this alga and have no homologues in other
related algal species, suggesting that they were acquired
recently (Derelle et al. 2006). This is in sharp contrast with
the case of another green alga, Chlamydomonas reinhardtii,
for which no HGT at all has been detected (Keeling and
Palmer 2008). In fungi (osmotrophic eukaryotes), a certain
number of genes acquired by HGT has been identified.
For instance, 13 genes are of bacterial origin in the yeast
S. cerevisiae. These genes represent a tiny proportion of the
yeast genome, but their functions are very important, including the capacity to grow in anaerobic conditions and the
synthesis of some vitamins (Hall et al. 2005). This reminds
the case of ciliates and fungi inhabiting the rumen, which
have also acquired bacterial genes that allow them adapting
to this anaerobic habitat, such as the glycosyl hydrolases
involved in the degradation of cellulosic polymers (GarciaVallve et al. 2000). All these examples show that
phagotrophy is not indispensable to acquire genes by HGT
in eukaryotes.
An interesting trend shown by these analyses is that HGT
from bacterial donors has played an important role in the
adaptation of very diverse eukaryotes to anaerobic life. The
example of rumen ciliates and fungi has already been
commented, but many other cases are known. For instance,
in trypanosomatids, parasites belonging to the phylum
Euglenozoa, several dozens of genes of bacterial origin
have been characterized (Berriman et al. 2005). This is
also the case for Cryptosporidium, a parasite belonging to
the phylum Alveolata (Huang et al. 2004), and for several
parasitic diplomonad species such as Giardia lamblia and
Spironucleus salmonicida (Andersson et al. 2007). In all
these protists, genes acquired from bacteria are involved in
functions linked to their anaerobic lifestyle. These genes
have certainly played a crucial role in the adaptation of
these eukaryotes to oxygen-depleted environments, either
permanently in Diplomonadida or transiently in the case of
the complex life cycles of trypanosomatids and Cryptosporidium, which alternate aerobic and anaerobic phases
(Andersson et al. 2007). It is important to note that these
changes in lifestyle have happened several times independently during the evolutionary history of eukaryotes. It is
paradoxical to notice that if these eukaryotes have adapted to
aerobic life thanks to bacteria (through the mitochondrial
endosymbiosis), bacteria have also allowed them to readapt
to anaerobic niches as donors of genes in HGT events.
12.4.2.2 HGT Among Eukaryotes
In the previous section, we have shown that eukaryotes, even
those belonging to sexual multicellular lineages, have experienced HGT and incorporated genes of bacterial origin into
their genomes, but are there also HGT events among eukaryotic species? The dominant view in the scientific community
is that this type of HGT is rare. However, this may rather
reflect the lack of data necessary to address this question and
the persistence of strong preconceptions. Methodological
difficulties explain in part the scarcity of studies focused
on this question. In fact, it is relatively easy to detect genes
of bacterial origin in a eukaryotic genome, but it is much
more difficult to detect a gene acquired from another eukaryotic lineage, since this requires a much more precise phylogenetic signal. Despite these technical limitations, some
cases of HGT between eukaryotic lineages have been
described. Many of them concern EGTs found in photosynthetic eukaryotes with secondary plastids, such as
Cryptophyta, Haptophyta, Heterokonta, Alveolata, and
Chlorarachniophyta. As in the case of mitochondria and
primary plastids (those directly derived from the endosymbiosis of a cyanobacterium, see above), secondary plastids
have very reduced genomes, which in part reflects the massive transfer of genes by EGT from the endosymbiont to the
host nucleus (Timmis et al. 2004). The study of the genome
sequences of some secondary photosynthetic eukaryotes,
such as chlorarachniophytes and diatoms, has shown that
the nuclear genomes of these organisms have acquired a
relatively large number of genes from their secondary
plastids (Archibald et al. 2003; Curtis et al. 2012).
In contrast with the HGT cases of genes of bacterial
origin, which very often have provided new functions, several HGTs among eukaryotes concern genes with functions
that already existed in the receptor cell. Thus, these can be
considered as homologous replacements (Keeling and
Palmer 2008). Those HGTs can even affect essential genes,
such as the alpha-tubulin of the jakobid Andalucia, which
has been replaced by a homologue from a diplomonad species (Simpson et al. 2008). Nevertheless, the acquisition of
new functions by eukaryote-to-eukaryote HGT has also been
described, especially in fungi. As in the case of the bacterial
genes acquired by fungi, those of eukaryotic origin have also
provided important adaptive functions. This is the case, for
example, of the cell recognition systems involved in sexual
reproduction (Inderbitzin et al. 2005), of the systems of
absorption of molecules from the environment (Slot and
Hibbett 2007), or of virulence factors (Friesen et al. 2006).
This latter example is remarkable because it concerns the
very recent acquisition of a toxin-coding gene by a nonpathogenic fungus that has led to the emergence of a new
disease in the 1940s. Cases of HGT in the opposite direction,
namely, from fungi to other unrelated eukaryotes, are also
known. For example, the analysis of the complete genome
478
C. Brochier-Armanet and D. Moreira
HGT, but other cases have also been characterized in nonphagotrophic species, such as chlorophytes and fungi. For
example, the analysis of the complete genome sequence of
the unicellular green alga Ostreococcus tauri has revealed
many cases of HGT, likely from bacterial donors. Surprisingly, almost all those genes are concentrated in a single
chromosome of this alga and have no homologues in other
related algal species, suggesting that they were acquired
recently (Derelle et al. 2006). This is in sharp contrast with
the case of another green alga, Chlamydomonas reinhardtii,
for which no HGT at all has been detected (Keeling and
Palmer 2008). In fungi (osmotrophic eukaryotes), a certain
number of genes acquired by HGT has been identified.
For instance, 13 genes are of bacterial origin in the yeast
S. cerevisiae. These genes represent a tiny proportion of the
yeast genome, but their functions are very important, including the capacity to grow in anaerobic conditions and the
synthesis of some vitamins (Hall et al. 2005). This reminds
the case of ciliates and fungi inhabiting the rumen, which
have also acquired bacterial genes that allow them adapting
to this anaerobic habitat, such as the glycosyl hydrolases
involved in the degradation of cellulosic polymers (GarciaVallve et al. 2000). All these examples show that
phagotrophy is not indispensable to acquire genes by HGT
in eukaryotes.
An interesting trend shown by these analyses is that HGT
from bacterial donors has played an important role in the
adaptation of very diverse eukaryotes to anaerobic life. The
example of rumen ciliates and fungi has already been
commented, but many other cases are known. For instance,
in trypanosomatids, parasites belonging to the phylum
Euglenozoa, several dozens of genes of bacterial origin
have been characterized (Berriman et al. 2005). This is
also the case for Cryptosporidium, a parasite belonging to
the phylum Alveolata (Huang et al. 2004), and for several
parasitic diplomonad species such as Giardia lamblia and
Spironucleus salmonicida (Andersson et al. 2007). In all
these protists, genes acquired from bacteria are involved in
functions linked to their anaerobic lifestyle. These genes
have certainly played a crucial role in the adaptation of
these eukaryotes to oxygen-depleted environments, either
permanently in Diplomonadida or transiently in the case of
the complex life cycles of trypanosomatids and Cryptosporidium, which alternate aerobic and anaerobic phases
(Andersson et al. 2007). It is important to note that these
changes in lifestyle have happened several times independently during the evolutionary history of eukaryotes. It is
paradoxical to notice that if these eukaryotes have adapted to
aerobic life thanks to bacteria (through the mitochondrial
endosymbiosis), bacteria have also allowed them to readapt
to anaerobic niches as donors of genes in HGT events.
12.4.2.2 HGT Among Eukaryotes
In the previous section, we have shown that eukaryotes, even
those belonging to sexual multicellular lineages, have experienced HGT and incorporated genes of bacterial origin into
their genomes, but are there also HGT events among eukaryotic species? The dominant view in the scientific community
is that this type of HGT is rare. However, this may rather
reflect the lack of data necessary to address this question and
the persistence of strong preconceptions. Methodological
difficulties explain in part the scarcity of studies focused
on this question. In fact, it is relatively easy to detect genes
of bacterial origin in a eukaryotic genome, but it is much
more difficult to detect a gene acquired from another eukaryotic lineage, since this requires a much more precise phylogenetic signal. Despite these technical limitations, some
cases of HGT between eukaryotic lineages have been
described. Many of them concern EGTs found in photosynthetic eukaryotes with secondary plastids, such as
Cryptophyta, Haptophyta, Heterokonta, Alveolata, and
Chlorarachniophyta. As in the case of mitochondria and
primary plastids (those directly derived from the endosymbiosis of a cyanobacterium, see above), secondary plastids
have very reduced genomes, which in part reflects the massive transfer of genes by EGT from the endosymbiont to the
host nucleus (Timmis et al. 2004). The study of the genome
sequences of some secondary photosynthetic eukaryotes,
such as chlorarachniophytes and diatoms, has shown that
the nuclear genomes of these organisms have acquired a
relatively large number of genes from their secondary
plastids (Archibald et al. 2003; Curtis et al. 2012).
In contrast with the HGT cases of genes of bacterial
origin, which very often have provided new functions, several HGTs among eukaryotes concern genes with functions
that already existed in the receptor cell. Thus, these can be
considered as homologous replacements (Keeling and
Palmer 2008). Those HGTs can even affect essential genes,
such as the alpha-tubulin of the jakobid Andalucia, which
has been replaced by a homologue from a diplomonad species (Simpson et al. 2008). Nevertheless, the acquisition of
new functions by eukaryote-to-eukaryote HGT has also been
described, especially in fungi. As in the case of the bacterial
genes acquired by fungi, those of eukaryotic origin have also
provided important adaptive functions. This is the case, for
example, of the cell recognition systems involved in sexual
reproduction (Inderbitzin et al. 2005), of the systems of
absorption of molecules from the environment (Slot and
Hibbett 2007), or of virulence factors (Friesen et al. 2006).
This latter example is remarkable because it concerns the
very recent acquisition of a toxin-coding gene by a nonpathogenic fungus that has led to the emergence of a new
disease in the 1940s. Cases of HGT in the opposite direction,
namely, from fungi to other unrelated eukaryotes, are also
known. For example, the analysis of the complete genome
478
C. Brochier-Armanet and D. Moreira