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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) showing the ultrastructure of putative primary endosymbionts in Auranticordis quadriverberis n. gen. et sp. A. Low magnification TEM showing four putative endosymbionts, each surrounded by sac-like vesicles (sc) defined by an outer membrane (Bar = 2 μm). B. High magnification TEM showing two enveloping inner membranes (arrowheads) and thylakoids (arrows) that are continuous with the innermost enveloping membrane (Bar = 0.2 μm). C. TEM showing the thylakoids, the sac-like vesicle (sc), and a cleavage furrow indicative of division (arrowheads) (Bar = 0.5 μm). D. High magnification TEM showing the central core of an endosymbiont containing viral particles (arrowheads) (Bar = 0.5 μm). E. High magnification TEM showing a pronounced invagination of the innermost enveloping membrane (arrowhead) (Bar = 0.5 μm). F. High magnification TEM showing the membrane (arrowheads) that defines the sac-like vesicle (sc) and the two innermost enveloping membranes (double arrowheads) (Bar = 0.2 μm). G. TEM showing viral particles (arrowhead) consisting of a polygonal head and tail, and positioned within the core of an endosymbiont (Bar = 0.5 μm). An inset showing a complete tailed viral particle (Bar = 0.2 μm).
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Figure 5: Transmission electron micrographs (TEM) showing the ultrastructure of putative primary endosymbionts in Auranticordis quadriverberis n. gen. et sp. A. Low magnification TEM showing four putative endosymbionts, each surrounded by sac-like vesicles (sc) defined by an outer membrane (Bar = 2 μm). B. High magnification TEM showing two enveloping inner membranes (arrowheads) and thylakoids (arrows) that are continuous with the innermost enveloping membrane (Bar = 0.2 μm). C. TEM showing the thylakoids, the sac-like vesicle (sc), and a cleavage furrow indicative of division (arrowheads) (Bar = 0.5 μm). D. High magnification TEM showing the central core of an endosymbiont containing viral particles (arrowheads) (Bar = 0.5 μm). E. High magnification TEM showing a pronounced invagination of the innermost enveloping membrane (arrowhead) (Bar = 0.5 μm). F. High magnification TEM showing the membrane (arrowheads) that defines the sac-like vesicle (sc) and the two innermost enveloping membranes (double arrowheads) (Bar = 0.2 μm). G. TEM showing viral particles (arrowhead) consisting of a polygonal head and tail, and positioned within the core of an endosymbiont (Bar = 0.5 μm). An inset showing a complete tailed viral particle (Bar = 0.2 μm).

Mentions: The cells of A. quadriverberis also contained an accumulation of black material near the anterior part of the cell, lipid globules and Golgi bodies (Figures 1C, 1F, 1I, 4H–I). Although mitochondria with tubular cristae were not definitively observed, several elongated bodies that were highly reminiscent of acristate mitochondria were found near the periphery of the cell (Figures 3A, 4G). The cells also contained 2–30 pale orange bodies that were variable in shape and usually about 4–5 μm in diam.; however, some of these bodies were 14 μm long (Figures 1C, 1F, 1I, 3A, 5A–G, 6). The pale orange bodies were distributed throughout the cell, but were most abundant in the anterior region of the cell. Each pale orange body was enveloped by two tightly pressed inner membranes and surrounded by sac-like vesicles (Figures 5A, 5C, 5F). The innermost membrane invaginated into the lumen of the body and formed several unstacked thylakoids around the periphery (Figures 5A–C, 5E). The sac-like vesicles occasionally butted together to form perpendicular partitions outside of the two inner membranes (Figure 5F). The central core of the pale orange bodies was devoid of membranes and contained a central electron dense region containing tailed viral particles (Figures 5D, 5G).


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) showing the ultrastructure of putative primary endosymbionts in Auranticordis quadriverberis n. gen. et sp. A. Low magnification TEM showing four putative endosymbionts, each surrounded by sac-like vesicles (sc) defined by an outer membrane (Bar = 2 μm). B. High magnification TEM showing two enveloping inner membranes (arrowheads) and thylakoids (arrows) that are continuous with the innermost enveloping membrane (Bar = 0.2 μm). C. TEM showing the thylakoids, the sac-like vesicle (sc), and a cleavage furrow indicative of division (arrowheads) (Bar = 0.5 μm). D. High magnification TEM showing the central core of an endosymbiont containing viral particles (arrowheads) (Bar = 0.5 μm). E. High magnification TEM showing a pronounced invagination of the innermost enveloping membrane (arrowhead) (Bar = 0.5 μm). F. High magnification TEM showing the membrane (arrowheads) that defines the sac-like vesicle (sc) and the two innermost enveloping membranes (double arrowheads) (Bar = 0.2 μm). G. TEM showing viral particles (arrowhead) consisting of a polygonal head and tail, and positioned within the core of an endosymbiont (Bar = 0.5 μm). An inset showing a complete tailed viral particle (Bar = 0.2 μm).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 5: Transmission electron micrographs (TEM) showing the ultrastructure of putative primary endosymbionts in Auranticordis quadriverberis n. gen. et sp. A. Low magnification TEM showing four putative endosymbionts, each surrounded by sac-like vesicles (sc) defined by an outer membrane (Bar = 2 μm). B. High magnification TEM showing two enveloping inner membranes (arrowheads) and thylakoids (arrows) that are continuous with the innermost enveloping membrane (Bar = 0.2 μm). C. TEM showing the thylakoids, the sac-like vesicle (sc), and a cleavage furrow indicative of division (arrowheads) (Bar = 0.5 μm). D. High magnification TEM showing the central core of an endosymbiont containing viral particles (arrowheads) (Bar = 0.5 μm). E. High magnification TEM showing a pronounced invagination of the innermost enveloping membrane (arrowhead) (Bar = 0.5 μm). F. High magnification TEM showing the membrane (arrowheads) that defines the sac-like vesicle (sc) and the two innermost enveloping membranes (double arrowheads) (Bar = 0.2 μm). G. TEM showing viral particles (arrowhead) consisting of a polygonal head and tail, and positioned within the core of an endosymbiont (Bar = 0.5 μm). An inset showing a complete tailed viral particle (Bar = 0.2 μm).
Mentions: The cells of A. quadriverberis also contained an accumulation of black material near the anterior part of the cell, lipid globules and Golgi bodies (Figures 1C, 1F, 1I, 4H–I). Although mitochondria with tubular cristae were not definitively observed, several elongated bodies that were highly reminiscent of acristate mitochondria were found near the periphery of the cell (Figures 3A, 4G). The cells also contained 2–30 pale orange bodies that were variable in shape and usually about 4–5 μm in diam.; however, some of these bodies were 14 μm long (Figures 1C, 1F, 1I, 3A, 5A–G, 6). The pale orange bodies were distributed throughout the cell, but were most abundant in the anterior region of the cell. Each pale orange body was enveloped by two tightly pressed inner membranes and surrounded by sac-like vesicles (Figures 5A, 5C, 5F). The innermost membrane invaginated into the lumen of the body and formed several unstacked thylakoids around the periphery (Figures 5A–C, 5E). The sac-like vesicles occasionally butted together to form perpendicular partitions outside of the two inner membranes (Figure 5F). The central core of the pale orange bodies was devoid of membranes and contained a central electron dense region containing tailed viral particles (Figures 5D, 5G).

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