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Ultra-high voltage electron microscopy of primitive algae illuminates 3D ultrastructures of the first photosynthetic eukaryote.

Takahashi T, Nishida T, Saito C, Yasuda H, Nozaki H - Sci Rep (2015)

Bottom Line: The primary phototrophs, glaucophytes, are thought to retain ancestral features of the first photosynthetic eukaryote, but examining the protoplast ultrastructure has previously been problematic in the coccoid glaucophyte Glaucocystis due to its thick cell wall.This 3D feature is essentially identical to that of another glaucophyte genus Cyanophora, as well as the secondary phototrophs in Alveolata.Thus, the common ancestor of glaucophytes and/or the first photosynthetic eukaryote may have shown similar 3D structures.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-0033, Japan.

ABSTRACT
A heterotrophic organism 1-2 billion years ago enslaved a cyanobacterium to become the first photosynthetic eukaryote, and has diverged globally. The primary phototrophs, glaucophytes, are thought to retain ancestral features of the first photosynthetic eukaryote, but examining the protoplast ultrastructure has previously been problematic in the coccoid glaucophyte Glaucocystis due to its thick cell wall. Here, we examined the three-dimensional (3D) ultrastructure in two divergent species of Glaucocystis using ultra-high voltage electron microscopy. Three-dimensional modelling of Glaucocystis cells using electron tomography clearly showed that numerous, leaflet-like flattened vesicles are distributed throughout the protoplast periphery just underneath a single-layered plasma membrane. This 3D feature is essentially identical to that of another glaucophyte genus Cyanophora, as well as the secondary phototrophs in Alveolata. Thus, the common ancestor of glaucophytes and/or the first photosynthetic eukaryote may have shown similar 3D structures.

No MeSH data available.


Related in: MedlinePlus

Diagram of a possible evolutionary scenario from an ancestral flagellate with leaflet-like flattened vesicles to extant primary photosynthetic eukaryotes (Archaeplastida).Based on the present study, Adl et al.2 and Cavalier-Smith19. Extant organisms that possibly retain flattened vesicles are Glaucophyta, Alveolata and Haptophyta. The putative ancestral flagellate of glaucophytes or the first primary photosynthetic eukaryote enslaved a cyanobacterium (Cy) as plastids might have contained nucleus (N), mitochondria (M) and leaflet-like flattened vesicles (FV).
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f5: Diagram of a possible evolutionary scenario from an ancestral flagellate with leaflet-like flattened vesicles to extant primary photosynthetic eukaryotes (Archaeplastida).Based on the present study, Adl et al.2 and Cavalier-Smith19. Extant organisms that possibly retain flattened vesicles are Glaucophyta, Alveolata and Haptophyta. The putative ancestral flagellate of glaucophytes or the first primary photosynthetic eukaryote enslaved a cyanobacterium (Cy) as plastids might have contained nucleus (N), mitochondria (M) and leaflet-like flattened vesicles (FV).

Mentions: In dinophytes and Chromera (Alveolata), similar 3D structures of the plasma membrane and the underlying leaflet-like flattened vesicles or alveolae can be considered based on SEM/FE-SEM and ultrathin section TEM2303132. In addition, some haptophytes possess flattened-vesicle-like ultrastructures or peripheral endoplasmic reticulum (PER) just beneath the plasma membrane33. Thus, fundamentally identical or homologous peripheral ultrastructures may be distributed in separate lineages or different supergoups within corticates or bikonts (corticates plus Excavata, or eukaryotes excluding Amoebozoa and Opisthokonta2) (Fig. 5). On the other hand, no organism in the other two groups of Archaeplastida (Chloroplastida and red algae) and unikonts (composed of opisthokonts and amoebozoans) contains such complicated peripheral ultrastructures. Given that the glaucophytes represent the most ancestral features of Archaeplastida56, the leaflet-like flattened vesicles in the protoplast periphery in glaucophyte cells may have been retained from the first photosynthetic eukaryote in the Precambrian period or a more ancient ancestor within the bikonts, as suggested by Cavalier-Smith19 (Fig. 5). In the ancestors of Chloroplastida and red algae, the flattened vesicles may have been lost during evolution.


Ultra-high voltage electron microscopy of primitive algae illuminates 3D ultrastructures of the first photosynthetic eukaryote.

Takahashi T, Nishida T, Saito C, Yasuda H, Nozaki H - Sci Rep (2015)

Diagram of a possible evolutionary scenario from an ancestral flagellate with leaflet-like flattened vesicles to extant primary photosynthetic eukaryotes (Archaeplastida).Based on the present study, Adl et al.2 and Cavalier-Smith19. Extant organisms that possibly retain flattened vesicles are Glaucophyta, Alveolata and Haptophyta. The putative ancestral flagellate of glaucophytes or the first primary photosynthetic eukaryote enslaved a cyanobacterium (Cy) as plastids might have contained nucleus (N), mitochondria (M) and leaflet-like flattened vesicles (FV).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4593968&req=5

f5: Diagram of a possible evolutionary scenario from an ancestral flagellate with leaflet-like flattened vesicles to extant primary photosynthetic eukaryotes (Archaeplastida).Based on the present study, Adl et al.2 and Cavalier-Smith19. Extant organisms that possibly retain flattened vesicles are Glaucophyta, Alveolata and Haptophyta. The putative ancestral flagellate of glaucophytes or the first primary photosynthetic eukaryote enslaved a cyanobacterium (Cy) as plastids might have contained nucleus (N), mitochondria (M) and leaflet-like flattened vesicles (FV).
Mentions: In dinophytes and Chromera (Alveolata), similar 3D structures of the plasma membrane and the underlying leaflet-like flattened vesicles or alveolae can be considered based on SEM/FE-SEM and ultrathin section TEM2303132. In addition, some haptophytes possess flattened-vesicle-like ultrastructures or peripheral endoplasmic reticulum (PER) just beneath the plasma membrane33. Thus, fundamentally identical or homologous peripheral ultrastructures may be distributed in separate lineages or different supergoups within corticates or bikonts (corticates plus Excavata, or eukaryotes excluding Amoebozoa and Opisthokonta2) (Fig. 5). On the other hand, no organism in the other two groups of Archaeplastida (Chloroplastida and red algae) and unikonts (composed of opisthokonts and amoebozoans) contains such complicated peripheral ultrastructures. Given that the glaucophytes represent the most ancestral features of Archaeplastida56, the leaflet-like flattened vesicles in the protoplast periphery in glaucophyte cells may have been retained from the first photosynthetic eukaryote in the Precambrian period or a more ancient ancestor within the bikonts, as suggested by Cavalier-Smith19 (Fig. 5). In the ancestors of Chloroplastida and red algae, the flattened vesicles may have been lost during evolution.

Bottom Line: The primary phototrophs, glaucophytes, are thought to retain ancestral features of the first photosynthetic eukaryote, but examining the protoplast ultrastructure has previously been problematic in the coccoid glaucophyte Glaucocystis due to its thick cell wall.This 3D feature is essentially identical to that of another glaucophyte genus Cyanophora, as well as the secondary phototrophs in Alveolata.Thus, the common ancestor of glaucophytes and/or the first photosynthetic eukaryote may have shown similar 3D structures.

View Article: PubMed Central - PubMed

Affiliation: Department of Biological Sciences, Graduate School of Science, University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo, 113-0033, Japan.

ABSTRACT
A heterotrophic organism 1-2 billion years ago enslaved a cyanobacterium to become the first photosynthetic eukaryote, and has diverged globally. The primary phototrophs, glaucophytes, are thought to retain ancestral features of the first photosynthetic eukaryote, but examining the protoplast ultrastructure has previously been problematic in the coccoid glaucophyte Glaucocystis due to its thick cell wall. Here, we examined the three-dimensional (3D) ultrastructure in two divergent species of Glaucocystis using ultra-high voltage electron microscopy. Three-dimensional modelling of Glaucocystis cells using electron tomography clearly showed that numerous, leaflet-like flattened vesicles are distributed throughout the protoplast periphery just underneath a single-layered plasma membrane. This 3D feature is essentially identical to that of another glaucophyte genus Cyanophora, as well as the secondary phototrophs in Alveolata. Thus, the common ancestor of glaucophytes and/or the first photosynthetic eukaryote may have shown similar 3D structures.

No MeSH data available.


Related in: MedlinePlus