45
General Overview
The red alga eventually evolved chlorophyll c plastids and engaged in several subsequent higherorder endosymbiosis with phylogenetically diverse hosts (in an order still to be resolved), hence giving rise to all the extant photosynthetic lineages. The derivation of chlorophyll c containing plastids
from the red algal lineage is still somewhat conjectural, but recent analyses of both gene sequences
and gene content are consistent with this conclusion.
The cryptophytes were the first group in which secondary plastids were recognized, on the basis
of their complex four-membrane structure. Like red algae, they have chlorophyll a and phycobiliproteins, but these are distributed in the intrathylakoidal space rather than in the phycobilisomes
found in red algae, Glaucophyta, and Cyanophyta. In addition, cryptomonads possess a second type
of chlorophyll, chlorophyll c, which is found in the plastids of the remaining red lineage clades,
retain the nucleomorph, vestigial nucleus of their symbiont, and have starch the reserve polysaccharide of red algae in the periplastid space.
Ochrophyta (including kelps, diatoms, chrysophytes, and related groups), Haptophyta (the coccolithophorids), and probably those dinoflagellates (Myzozoa) pigmented with peridinin, have chlorophylls a and c, along with a variety of carotenoids. Stacked thylakoids are found in those lineages
that lack phycobilisomes.
The plastid situation in dinoflagellate is exceptionally complex; most of the phototrophic species harbor a plastid of red algal origin bound by three membranes and characterized by the
carotenoid peridinin, chlorophylls a and c 2 . It has been speculated that the ancestral peridinincontaining chloroplast was replaced by one from a cryptophyte, a haptophyte, a diatom, or a
green alga, that is, by additional endosymbiotic events, namely tertiary endosymbiosis in the
first three cases, and serial secondary endosymbiosis for the green alga. All these symbiotic relationships have not reached the same level of permanence, and sometimes it is disputed whether
the plastids are the traces of a stable symbiosis or rather they are kleptoplastids, that is, plastids obtained from ingested algal prey and retained, which may remain temporarily functional
and be used for photosynthesis by the predator. In some cases, the endosymbiont is present in
an almost unchanged form and was therefore established more recently (e.g., Kryptoperidinium
foliaceum). In other cases, the symbiont has almost lost all organelles and only the chloroplast
remains (e.g., peridinin-containing species, Heterocapsa, Peridinium), indicating an older, more
well- established symbiosis.
Members of the Kareniaceae (Karenia mikimotoi, Karlodinium micrum) possess fucoxanthins
as accessory pigment instead of peridinin; molecular data confirmed that the peridinin-containing chloroplast in this group has been superseded by a haptophyte-type-containing fucoxanthin. Other dinoflagellates such as Dinophysis acuminata have established a stable symbiosis
with a cryptophyte symbiont, of which only the chloroplast remains, surrounded by three membranes. A diatom symbiont is present in a small group of closely related dinoflagellates named
“dinotoms” consisting of only 10 species such as Durinskia baltica, K. foliaceum, Peridinium
quinquecorne, and other species belonging to the genera Galeidinium and Gymnodinium. The
endosymbionts have been shown to originate from three different diatom lineages, one pennate and two centric. Despite the loss of a distinctive cell wall, motility, and ability to divide
mitotically, these endosymbionts have retained a large nucleus with vast amount of DNA, a large
volume of cytoplasm, separate from the host by a single membrane, and their own mitochondria
in addition to the chloroplasts. Another unique symbiosis is present in the dinoflagellate genus
Lepidodinium; members of this genus such as L. viride (Figure 1.1bh; courtesy of Francisco
Rodriguez Hernandez) and Lepidodinium chlorophorum (formerly Gymnodinium chlorophorum) possess green-colored plastids containing chlorophylls a and b. The pigment composition,
phylogenetic analyses of plastid-encoded genes, and a survey of nuclear genes encoding plastidtargeted proteins in L. chlorophorum clearly indicated that the ancestral Lepidodinium cells
replaced the original Chl-a + c-containing plastids with the Chl-a + b-containing plastids of
an endosymbiotic green alga belonging to the core chlorophytes. Only the symbiont chloroplast
General Overview
The red alga eventually evolved chlorophyll c plastids and engaged in several subsequent higherorder endosymbiosis with phylogenetically diverse hosts (in an order still to be resolved), hence giving rise to all the extant photosynthetic lineages. The derivation of chlorophyll c containing plastids
from the red algal lineage is still somewhat conjectural, but recent analyses of both gene sequences
and gene content are consistent with this conclusion.
The cryptophytes were the first group in which secondary plastids were recognized, on the basis
of their complex four-membrane structure. Like red algae, they have chlorophyll a and phycobiliproteins, but these are distributed in the intrathylakoidal space rather than in the phycobilisomes
found in red algae, Glaucophyta, and Cyanophyta. In addition, cryptomonads possess a second type
of chlorophyll, chlorophyll c, which is found in the plastids of the remaining red lineage clades,
retain the nucleomorph, vestigial nucleus of their symbiont, and have starch the reserve polysaccharide of red algae in the periplastid space.
Ochrophyta (including kelps, diatoms, chrysophytes, and related groups), Haptophyta (the coccolithophorids), and probably those dinoflagellates (Myzozoa) pigmented with peridinin, have chlorophylls a and c, along with a variety of carotenoids. Stacked thylakoids are found in those lineages
that lack phycobilisomes.
The plastid situation in dinoflagellate is exceptionally complex; most of the phototrophic species harbor a plastid of red algal origin bound by three membranes and characterized by the
carotenoid peridinin, chlorophylls a and c 2 . It has been speculated that the ancestral peridinincontaining chloroplast was replaced by one from a cryptophyte, a haptophyte, a diatom, or a
green alga, that is, by additional endosymbiotic events, namely tertiary endosymbiosis in the
first three cases, and serial secondary endosymbiosis for the green alga. All these symbiotic relationships have not reached the same level of permanence, and sometimes it is disputed whether
the plastids are the traces of a stable symbiosis or rather they are kleptoplastids, that is, plastids obtained from ingested algal prey and retained, which may remain temporarily functional
and be used for photosynthesis by the predator. In some cases, the endosymbiont is present in
an almost unchanged form and was therefore established more recently (e.g., Kryptoperidinium
foliaceum). In other cases, the symbiont has almost lost all organelles and only the chloroplast
remains (e.g., peridinin-containing species, Heterocapsa, Peridinium), indicating an older, more
well- established symbiosis.
Members of the Kareniaceae (Karenia mikimotoi, Karlodinium micrum) possess fucoxanthins
as accessory pigment instead of peridinin; molecular data confirmed that the peridinin-containing chloroplast in this group has been superseded by a haptophyte-type-containing fucoxanthin. Other dinoflagellates such as Dinophysis acuminata have established a stable symbiosis
with a cryptophyte symbiont, of which only the chloroplast remains, surrounded by three membranes. A diatom symbiont is present in a small group of closely related dinoflagellates named
“dinotoms” consisting of only 10 species such as Durinskia baltica, K. foliaceum, Peridinium
quinquecorne, and other species belonging to the genera Galeidinium and Gymnodinium. The
endosymbionts have been shown to originate from three different diatom lineages, one pennate and two centric. Despite the loss of a distinctive cell wall, motility, and ability to divide
mitotically, these endosymbionts have retained a large nucleus with vast amount of DNA, a large
volume of cytoplasm, separate from the host by a single membrane, and their own mitochondria
in addition to the chloroplasts. Another unique symbiosis is present in the dinoflagellate genus
Lepidodinium; members of this genus such as L. viride (Figure 1.1bh; courtesy of Francisco
Rodriguez Hernandez) and Lepidodinium chlorophorum (formerly Gymnodinium chlorophorum) possess green-colored plastids containing chlorophylls a and b. The pigment composition,
phylogenetic analyses of plastid-encoded genes, and a survey of nuclear genes encoding plastidtargeted proteins in L. chlorophorum clearly indicated that the ancestral Lepidodinium cells
replaced the original Chl-a + c-containing plastids with the Chl-a + b-containing plastids of
an endosymbiotic green alga belonging to the core chlorophytes. Only the symbiont chloroplast