molecule, exclusively uses CO 2 during photosynthesis, concentration mechanisms of CO 2 are necessary. The additional
envelope around the chloroplast (especially the plastidnuclear complex, Fig. 5.14), which characterizes the secondary and tertiary endosymbioses by creating around the
chloroplast a micro-area of acidic pH, promotes the concentration of CO 2 . According to Kugrens and Lee (2000), secondary and tertiary endosymbioses would therefore
represent a key advantage at a time when the CO 2 content
was unusually low and therefore have been selected by
evolution. Paleontological data are consistent with this
hypothesis: fossil taxa from secondary and tertiary
endosymbioses, such as diatoms (Stramenopiles), are all
younger than 260 Ma (Falkowski et al. 2004; Medlin and
Kaczmarska 2004; Raven and Waite 2004).
5.4.4 Mechanisms and Processes
of Endosymbiosis
Phagotrophy and/or parasitism may be the origin of primary
endosymbiosis. Parasitism* of a eukaryotic cell by a nonphotosynthetic bacteria constitutes a very reliable hypothesis
for the origin of the mitochondria. Indeed, parasitism often
precedes mutualism; in other words, mutualism is an
advanced form of parasitism (Combes 1995, 2001). Moreover, K. W. Jeon has shown the relatively high speed of the
shift from parasitism to mutualism-helotism in modern bacteria (Jeon 1972, 1991, 1995; Jeon and Jeon 1976, Box 5.4).
In the case of the origin of the chloroplast, predation
(phagotrophy) of a cyanobacterium by a heterotrophic unicellular eukaryote can be the starting point of the endosymbiosis. The fact that cyanobacteria are retained in the
cytoplasm instead of being digested is not an unrealistic
assumption since in the present environment, nonphotosynthetic eukaryotes host “wild” cyanobacteria, which
are also found as free-living cells. This is the case, for
example, of Nostoc symbioticum found in Glomeromycota
(Fungi, Opisthokonta) Geosiphon pyriformis (Fig. 5.17).
In the case of secondary and tertiary endosymbioses which
allowed non-photosynthetic taxa to acquire photosynthesis,
phagotrophy and kleptoplasty are the most likely mechanism
(Fig. 5.18). Normally, the prey is digested (Fig. 5.18a). However, there are many modern predators which are known to
digest most of their prey but retain its chloroplasts (Fig. 5.18b);
this phenomenon is called kleptoplasty. This is the case, for
example, of the opisthobranch mollusk Elysia viridis (Rahat
and Ben Ishac-Monselise 1979). This sea slug grazes on
Codium (Chlorobionta, Viridiplantae) and sequesters its
chloroplasts which are transferred, via the diverticula of the
digestive tract, in its parapodia cells.
10 In the presence of light,
the sea slug stops moving and displays its parapodia to
allow the activity of chloroplasts, in order to benefit from the
photosynthesis products.
However, the chloroplasts cannot divide because they
are not autonomous; the controlling genes were located in
the nucleus of the prey and were destroyed (digested) with
the rest of the prey. The survival of chloroplasts in the
parapodia of Elysia does not exceed a few days to a few
weeks after which the sea slug must acquire new chloroplasts by grazing again on Codium (Williams and Walker
1999). Kleptoplasty is not uncommon; in addition to
opisthobranchs, it has been observed particularly among
ciliates (Alveolata) and foraminifera (Rhizaria).
To become truly photosynthetic, an organism that
practices kleptoplasty must recover not only the chloroplasts
but also the controlling genes located in the nucleus of its
prey (Fig. 5.18d). This is undoubtedly a very improbable
event, although it already happened in the course of evolution, at least once, as suggested by Cavalier-Smith (2002b),
but more likely several times. An intermediate step is to
recover not only the chloroplast (kleptoplasty) but also the
nucleus (with chloroplast genes; karyoklepty) of the prey
(Fig. 5.18c) (Hansen and Fenchel 2006; Johnson et al. 2007;
Smith and Hansen 2007). In present-day nature, the beginning of the nuclear gene recovery process that controls
chloroplast was observed. In the sea slug Elysia chlorotica,
which feeds on Vaucheria litorea (Chromobionta,
Stramenopile), if the juveniles do not encounter Vaucheria,
they do not survive; chloroplasts survive as long as the life
of the slug, 10 months (Fig. 5.19); kleptoplasty and photosynthesis have then became obligatory in Elysia chlorotica
but not in E. viridis: in the absence of light, the latter
survives via grazing (Rumpho et al. 2000; Pennisi 2006).
Two large fragments of genes of photosynthetic organisms
likely to participate in the survival of the chloroplast were
discovered in the nucleus of Elysia chlorotica (Rumpho
et al. 2000, 2008; Pennisi 2006). A similar discovery was
made in Elysia clarki (Curtis et al. 2006).
Similarly, in the gammaproteobacterium Carsonella
ruddii, an endosymbiont of psyllids, that has a tiny genome
(160,000 bp), genes were lost and others transferred to the
nucleus of the host: this bacterium is thus in a transitory
step to becoming an organelle. Indeed, it is transmitted
vertically by the host (Andersson 2006; Nakabachi et al.
2006). In endosymbiotic bacteria, gene capture by the host
nucleus is not a general case; helotism can occur directly
through loss of unnecessary genes (McCutcheon and
Moran 2011).
It is therefore reasonable to think that kleptoplasty phenomena observed in nature today (mollusks, foraminifera, ciliates,
etc.) are the beginnings of future secondary or tertiary
endosymbioses, known as endosymbiosis in progress by
McFadden (2001). This is really most likely because the period
in which we live (Tertiary Age, Pleistocene) is characterized by
10 The abundance of these chloroplasts gives a green color to Elysia
viridis. Note that viridis means “green” in Latin.
130
C.-F. Boudouresque et al.
envelope around the chloroplast (especially the plastidnuclear complex, Fig. 5.14), which characterizes the secondary and tertiary endosymbioses by creating around the
chloroplast a micro-area of acidic pH, promotes the concentration of CO 2 . According to Kugrens and Lee (2000), secondary and tertiary endosymbioses would therefore
represent a key advantage at a time when the CO 2 content
was unusually low and therefore have been selected by
evolution. Paleontological data are consistent with this
hypothesis: fossil taxa from secondary and tertiary
endosymbioses, such as diatoms (Stramenopiles), are all
younger than 260 Ma (Falkowski et al. 2004; Medlin and
Kaczmarska 2004; Raven and Waite 2004).
5.4.4 Mechanisms and Processes
of Endosymbiosis
Phagotrophy and/or parasitism may be the origin of primary
endosymbiosis. Parasitism* of a eukaryotic cell by a nonphotosynthetic bacteria constitutes a very reliable hypothesis
for the origin of the mitochondria. Indeed, parasitism often
precedes mutualism; in other words, mutualism is an
advanced form of parasitism (Combes 1995, 2001). Moreover, K. W. Jeon has shown the relatively high speed of the
shift from parasitism to mutualism-helotism in modern bacteria (Jeon 1972, 1991, 1995; Jeon and Jeon 1976, Box 5.4).
In the case of the origin of the chloroplast, predation
(phagotrophy) of a cyanobacterium by a heterotrophic unicellular eukaryote can be the starting point of the endosymbiosis. The fact that cyanobacteria are retained in the
cytoplasm instead of being digested is not an unrealistic
assumption since in the present environment, nonphotosynthetic eukaryotes host “wild” cyanobacteria, which
are also found as free-living cells. This is the case, for
example, of Nostoc symbioticum found in Glomeromycota
(Fungi, Opisthokonta) Geosiphon pyriformis (Fig. 5.17).
In the case of secondary and tertiary endosymbioses which
allowed non-photosynthetic taxa to acquire photosynthesis,
phagotrophy and kleptoplasty are the most likely mechanism
(Fig. 5.18). Normally, the prey is digested (Fig. 5.18a). However, there are many modern predators which are known to
digest most of their prey but retain its chloroplasts (Fig. 5.18b);
this phenomenon is called kleptoplasty. This is the case, for
example, of the opisthobranch mollusk Elysia viridis (Rahat
and Ben Ishac-Monselise 1979). This sea slug grazes on
Codium (Chlorobionta, Viridiplantae) and sequesters its
chloroplasts which are transferred, via the diverticula of the
digestive tract, in its parapodia cells.
10 In the presence of light,
the sea slug stops moving and displays its parapodia to
allow the activity of chloroplasts, in order to benefit from the
photosynthesis products.
However, the chloroplasts cannot divide because they
are not autonomous; the controlling genes were located in
the nucleus of the prey and were destroyed (digested) with
the rest of the prey. The survival of chloroplasts in the
parapodia of Elysia does not exceed a few days to a few
weeks after which the sea slug must acquire new chloroplasts by grazing again on Codium (Williams and Walker
1999). Kleptoplasty is not uncommon; in addition to
opisthobranchs, it has been observed particularly among
ciliates (Alveolata) and foraminifera (Rhizaria).
To become truly photosynthetic, an organism that
practices kleptoplasty must recover not only the chloroplasts
but also the controlling genes located in the nucleus of its
prey (Fig. 5.18d). This is undoubtedly a very improbable
event, although it already happened in the course of evolution, at least once, as suggested by Cavalier-Smith (2002b),
but more likely several times. An intermediate step is to
recover not only the chloroplast (kleptoplasty) but also the
nucleus (with chloroplast genes; karyoklepty) of the prey
(Fig. 5.18c) (Hansen and Fenchel 2006; Johnson et al. 2007;
Smith and Hansen 2007). In present-day nature, the beginning of the nuclear gene recovery process that controls
chloroplast was observed. In the sea slug Elysia chlorotica,
which feeds on Vaucheria litorea (Chromobionta,
Stramenopile), if the juveniles do not encounter Vaucheria,
they do not survive; chloroplasts survive as long as the life
of the slug, 10 months (Fig. 5.19); kleptoplasty and photosynthesis have then became obligatory in Elysia chlorotica
but not in E. viridis: in the absence of light, the latter
survives via grazing (Rumpho et al. 2000; Pennisi 2006).
Two large fragments of genes of photosynthetic organisms
likely to participate in the survival of the chloroplast were
discovered in the nucleus of Elysia chlorotica (Rumpho
et al. 2000, 2008; Pennisi 2006). A similar discovery was
made in Elysia clarki (Curtis et al. 2006).
Similarly, in the gammaproteobacterium Carsonella
ruddii, an endosymbiont of psyllids, that has a tiny genome
(160,000 bp), genes were lost and others transferred to the
nucleus of the host: this bacterium is thus in a transitory
step to becoming an organelle. Indeed, it is transmitted
vertically by the host (Andersson 2006; Nakabachi et al.
2006). In endosymbiotic bacteria, gene capture by the host
nucleus is not a general case; helotism can occur directly
through loss of unnecessary genes (McCutcheon and
Moran 2011).
It is therefore reasonable to think that kleptoplasty phenomena observed in nature today (mollusks, foraminifera, ciliates,
etc.) are the beginnings of future secondary or tertiary
endosymbioses, known as endosymbiosis in progress by
McFadden (2001). This is really most likely because the period
in which we live (Tertiary Age, Pleistocene) is characterized by
10 The abundance of these chloroplasts gives a green color to Elysia
viridis. Note that viridis means “green” in Latin.
130
C.-F. Boudouresque et al.