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Morphology and molecular phylogeny of a marine interstitial tetraflagellate with putative endosymbionts: Auranticordis quadriverberis n. gen. et sp. (Cercozoa).

Chantangsi C, Esson HJ, Leander BS - BMC Microbiol. (2008)

Bottom Line: This combination of morphological features did not allow us to assign A. quadriverberis to any known eukaryotic supergroup.Thus, we sequenced the small subunit rDNA sequence from two different isolates and demonstrated that this lineage evolved from within the Cercozoa.Our discovery and characterization of A. quadriverberis underscores how poorly we understand the diversity of cercozoans and, potentially, represents one of the few independent cases of primary endosymbiosis within the Cercozoa and beyond.

View Article: PubMed Central - HTML - PubMed

Affiliation: Canadian Institute for Advanced Research, Program in Integrated Microbial Biodiversity, Department of Zoology, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada. cchantan@interchange.ubc.ca

ABSTRACT

Background: Comparative morphological studies and environmental sequencing surveys indicate that marine benthic environments contain a diverse assortment of microorganisms that are just beginning to be explored and characterized. The most conspicuous predatory flagellates in these habitats range from about 20-150 mum in size and fall into three major groups of eukaryotes that are very distantly related to one another: dinoflagellates, euglenids and cercozoans. The Cercozoa is a diverse group of amoeboflagellates that cluster together in molecular phylogenies inferred mainly from ribosomal gene sequences. These molecular phylogenetic studies have demonstrated that several enigmatic taxa, previously treated as Eukaryota insertae sedis, fall within the Cercozoa, and suggest that the actual diversity of this group is largely unknown. Improved knowledge of cercozoan diversity is expected to help resolve major branches in the tree of eukaryotes and demonstrate important cellular innovations for understanding eukaryote evolution.

Results: A rare tetraflagellate, Auranticordis quadriverberis n. gen. et sp., was isolated from marine sand samples. Uncultured cells were in low abundance and were individually prepared for electron microscopy and DNA sequencing. These flagellates possessed several novel features, such as (1) gliding motility associated with four bundled recurrent flagella, (2) heart-shaped cells about 35-75 microm in diam., and (3) bright orange coloration caused by linear arrays of muciferous bodies. Each cell also possessed about 2-30 pale orange bodies (usually 4-5 microm in diam.) that were enveloped by two membranes and sac-like vesicles. The innermost membrane invaginated to form unstacked thylakoids that extended towards a central pyrenoid containing tailed viral particles. Although to our knowledge, these bodies have never been described in any other eukaryote, the ultrastructure was most consistent with photosynthetic endosymbionts of cyanobacterial origin. This combination of morphological features did not allow us to assign A. quadriverberis to any known eukaryotic supergroup. Thus, we sequenced the small subunit rDNA sequence from two different isolates and demonstrated that this lineage evolved from within the Cercozoa.

Conclusion: Our discovery and characterization of A. quadriverberis underscores how poorly we understand the diversity of cercozoans and, potentially, represents one of the few independent cases of primary endosymbiosis within the Cercozoa and beyond.

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Transmission electron micrographs (TEM) of Auranticordis quadriverberis n. gen. et sp., showing different cytoplasmic components. A. High magnification TEM showing a vacuolated cytoplasm (arrowheads) and fibrous material (fs) distributed beneath the cell periphery (Bar = 0.5 μm). B. High magnification view of the black inclusions (arrowheads) (Bar = 2 μm). C. An ingested bacterium found within cytoplasm of A. quadriverberis (Bar = 0.25 μm). D. A section through the nucleus (N) showing nucleoli (arrowheads) and an invaginated area (double arrowhead) (Bar = 2 μm). E. High magnification TEM showing the nuclear envelope (arrow), the nucleus (N), and a striated band (double arrowhead) positioned between the nuclear tip and a microtubular root (arrowhead) (Bar = 0.5 μm). F. Tangential section through the flagella (arrowheads) lying within the ventral groove (gr) (Bar = 1 μm). G. A putative mitochondrion positioned near the cell periphery (Bar = 0.2 μm). An inset showing two putative mitochondria (Bar = 0.5 μm). H. TEM showing lipid globules (lg) near the posterior part of the cell (Bar = 1 μm). I. High magnification view of a Golgi apparatus (Bar = 0.5 μm).
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Figure 4: Transmission electron micrographs (TEM) of Auranticordis quadriverberis n. gen. et sp., showing different cytoplasmic components. A. High magnification TEM showing a vacuolated cytoplasm (arrowheads) and fibrous material (fs) distributed beneath the cell periphery (Bar = 0.5 μm). B. High magnification view of the black inclusions (arrowheads) (Bar = 2 μm). C. An ingested bacterium found within cytoplasm of A. quadriverberis (Bar = 0.25 μm). D. A section through the nucleus (N) showing nucleoli (arrowheads) and an invaginated area (double arrowhead) (Bar = 2 μm). E. High magnification TEM showing the nuclear envelope (arrow), the nucleus (N), and a striated band (double arrowhead) positioned between the nuclear tip and a microtubular root (arrowhead) (Bar = 0.5 μm). F. Tangential section through the flagella (arrowheads) lying within the ventral groove (gr) (Bar = 1 μm). G. A putative mitochondrion positioned near the cell periphery (Bar = 0.2 μm). An inset showing two putative mitochondria (Bar = 0.5 μm). H. TEM showing lipid globules (lg) near the posterior part of the cell (Bar = 1 μm). I. High magnification view of a Golgi apparatus (Bar = 0.5 μm).

Mentions: The four flagella of A. quadriverberis originated from an anterior flagellar pocket and nestled tightly within the ventral groove, making them nearly invisible under the light microscope (Figures 1B, 1D–E, 1G, 2A–B, 2E, 4F). Electron microscopy demonstrated that the flagella were arranged in two pairs and covered with flagellar hairs or mastigomenes (Figure 2E). Except for very slight differences in length, all four flagella were morphologically identical and slightly longer than the cell (Figures 1B, D–E). The flagella were also homodynamic and associated with gliding motility along the substratum. Pseudopodia were not observed.


Morphology and molecular phylogeny of a marine interstitial tetraflagellate with putative endosymbionts: Auranticordis quadriverberis n. gen. et sp. (Cercozoa).

Chantangsi C, Esson HJ, Leander BS - BMC Microbiol. (2008)

Transmission electron micrographs (TEM) of Auranticordis quadriverberis n. gen. et sp., showing different cytoplasmic components. A. High magnification TEM showing a vacuolated cytoplasm (arrowheads) and fibrous material (fs) distributed beneath the cell periphery (Bar = 0.5 μm). B. High magnification view of the black inclusions (arrowheads) (Bar = 2 μm). C. An ingested bacterium found within cytoplasm of A. quadriverberis (Bar = 0.25 μm). D. A section through the nucleus (N) showing nucleoli (arrowheads) and an invaginated area (double arrowhead) (Bar = 2 μm). E. High magnification TEM showing the nuclear envelope (arrow), the nucleus (N), and a striated band (double arrowhead) positioned between the nuclear tip and a microtubular root (arrowhead) (Bar = 0.5 μm). F. Tangential section through the flagella (arrowheads) lying within the ventral groove (gr) (Bar = 1 μm). G. A putative mitochondrion positioned near the cell periphery (Bar = 0.2 μm). An inset showing two putative mitochondria (Bar = 0.5 μm). H. TEM showing lipid globules (lg) near the posterior part of the cell (Bar = 1 μm). I. High magnification view of a Golgi apparatus (Bar = 0.5 μm).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2500021&req=5

Figure 4: Transmission electron micrographs (TEM) of Auranticordis quadriverberis n. gen. et sp., showing different cytoplasmic components. A. High magnification TEM showing a vacuolated cytoplasm (arrowheads) and fibrous material (fs) distributed beneath the cell periphery (Bar = 0.5 μm). B. High magnification view of the black inclusions (arrowheads) (Bar = 2 μm). C. An ingested bacterium found within cytoplasm of A. quadriverberis (Bar = 0.25 μm). D. A section through the nucleus (N) showing nucleoli (arrowheads) and an invaginated area (double arrowhead) (Bar = 2 μm). E. High magnification TEM showing the nuclear envelope (arrow), the nucleus (N), and a striated band (double arrowhead) positioned between the nuclear tip and a microtubular root (arrowhead) (Bar = 0.5 μm). F. Tangential section through the flagella (arrowheads) lying within the ventral groove (gr) (Bar = 1 μm). G. A putative mitochondrion positioned near the cell periphery (Bar = 0.2 μm). An inset showing two putative mitochondria (Bar = 0.5 μm). H. TEM showing lipid globules (lg) near the posterior part of the cell (Bar = 1 μm). I. High magnification view of a Golgi apparatus (Bar = 0.5 μm).
Mentions: The four flagella of A. quadriverberis originated from an anterior flagellar pocket and nestled tightly within the ventral groove, making them nearly invisible under the light microscope (Figures 1B, 1D–E, 1G, 2A–B, 2E, 4F). Electron microscopy demonstrated that the flagella were arranged in two pairs and covered with flagellar hairs or mastigomenes (Figure 2E). Except for very slight differences in length, all four flagella were morphologically identical and slightly longer than the cell (Figures 1B, D–E). The flagella were also homodynamic and associated with gliding motility along the substratum. Pseudopodia were not observed.

Bottom Line: This combination of morphological features did not allow us to assign A. quadriverberis to any known eukaryotic supergroup.Thus, we sequenced the small subunit rDNA sequence from two different isolates and demonstrated that this lineage evolved from within the Cercozoa.Our discovery and characterization of A. quadriverberis underscores how poorly we understand the diversity of cercozoans and, potentially, represents one of the few independent cases of primary endosymbiosis within the Cercozoa and beyond.

View Article: PubMed Central - HTML - PubMed

Affiliation: Canadian Institute for Advanced Research, Program in Integrated Microbial Biodiversity, Department of Zoology, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada. cchantan@interchange.ubc.ca

ABSTRACT

Background: Comparative morphological studies and environmental sequencing surveys indicate that marine benthic environments contain a diverse assortment of microorganisms that are just beginning to be explored and characterized. The most conspicuous predatory flagellates in these habitats range from about 20-150 mum in size and fall into three major groups of eukaryotes that are very distantly related to one another: dinoflagellates, euglenids and cercozoans. The Cercozoa is a diverse group of amoeboflagellates that cluster together in molecular phylogenies inferred mainly from ribosomal gene sequences. These molecular phylogenetic studies have demonstrated that several enigmatic taxa, previously treated as Eukaryota insertae sedis, fall within the Cercozoa, and suggest that the actual diversity of this group is largely unknown. Improved knowledge of cercozoan diversity is expected to help resolve major branches in the tree of eukaryotes and demonstrate important cellular innovations for understanding eukaryote evolution.

Results: A rare tetraflagellate, Auranticordis quadriverberis n. gen. et sp., was isolated from marine sand samples. Uncultured cells were in low abundance and were individually prepared for electron microscopy and DNA sequencing. These flagellates possessed several novel features, such as (1) gliding motility associated with four bundled recurrent flagella, (2) heart-shaped cells about 35-75 microm in diam., and (3) bright orange coloration caused by linear arrays of muciferous bodies. Each cell also possessed about 2-30 pale orange bodies (usually 4-5 microm in diam.) that were enveloped by two membranes and sac-like vesicles. The innermost membrane invaginated to form unstacked thylakoids that extended towards a central pyrenoid containing tailed viral particles. Although to our knowledge, these bodies have never been described in any other eukaryote, the ultrastructure was most consistent with photosynthetic endosymbionts of cyanobacterial origin. This combination of morphological features did not allow us to assign A. quadriverberis to any known eukaryotic supergroup. Thus, we sequenced the small subunit rDNA sequence from two different isolates and demonstrated that this lineage evolved from within the Cercozoa.

Conclusion: Our discovery and characterization of A. quadriverberis underscores how poorly we understand the diversity of cercozoans and, potentially, represents one of the few independent cases of primary endosymbiosis within the Cercozoa and beyond.

Show MeSH
Related in: MedlinePlus