Small subunit ribosomal RNA+ of Hexamita inflata and the quest for the first branch in the eukaryotic tree

Leipe, Detlef D.; Gunderson, John H.; Nerad, Thomas A.; Sogin, Mitchell L.

doi:10.1016/0166-6851(93)90005-i

Cited by 220 publications

(137 citation statements)

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“…Patterson (1988) used Metamonadida more narrowly for retortamonads and diplomonads and enteromonads, a grouping later called Eopharyngia (Cavalier-Smith, 1993a) or simply Metamonada (Cavalier-Smith, 1999). Initially, 18S rRNA trees appeared to confirm the deep divergence of diplomonads and Parabasalia by placing them at the root of the eukaryotic tree (Leipe et al, 1993;Cavalier-Smith, 1993a). For some years, I argued that parabasalian hydrogenosomes had evolved from mitochondria (Cavalier-Smith, 1987b), which is now thoroughly established (Dyall & Johnson, 2000;van der Giezen et al, 2002), but thought that Metamonada might be primitively amitochondrial (Cavalier-Smith, 1983, 1987a and therefore that the two groups were not a clade.…”

Section: Changing Views Of the Metamonadamentioning

confidence: 99%

The excavate protozoan phyla Metamonada Grasse emend. (Anaeromonadea, Parabasalia, Carpediemonas, Eopharyngia) and Loukozoa emend. (Jakobea, Malawimonas): their evolutionary affinities and new higher taxa

Cavalier‐Smith

2003

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLO

103

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It is argued here that the anaerobic protozoan zooflagellate Parabasalia, Carpediemonas and Eopharyngia (diplomonads, enteromonads, retortamonads) constitute a holophyletic group, for which the existing name Trichozoa is adopted as a new subphylum. Ancestrally, Trichozoa probably had hydrogenosomes, stacked Golgi dictyosomes, three anterior centrioles and one posterior centriole: the typical tetrakont pattern. It is also argued that the closest relatives of Trichozoa are Anaeromonada (Trimastix, oxymonads), and the two groups are classified as subphyla of a revised phylum Metamonada. Returning Parabasalia and Anaeromonadea to Metamonada, as in Grassé 's original classification, simplifies classification of the kingdom Protozoa by reducing the number of phyla within infrakingdom Excavata from five to four. Percolozoa (Heterolobosea plus Percolatea classis nov.) and Metamonada are probably both ancestrally quadriciliate with a kinetid of four centrioles attached to the nucleus; the few biciliates among them are probably secondarily derived. Metamonada ancestrally probably had two divergent centriole pairs, whereas, in Percolozoa, all four centrioles are parallel. It is suggested that Discicristata (Percolozoa, Euglenozoa) are holophyletic, ancestrally with two parallel centrioles. In the phylum Loukozoa, Malawimonadea classis nov. is established for Malawimonas (with a new family and order also) and Diphyllatea classis nov., for Diphylleida (Diphylleia, Collodictyon), is transferred back to Apusozoa. A new class, order and family are established for the anaerobic, biciliate, tricentriolar Carpediemonas, transferring it from Loukozoa to Trichozoa because of its triply flanged cilia; like Retortamonas, it may be secondarily biciliate -its unique combination of putative hydrogenosomes and flanged cilia agree with molecular evidence that Carpediemonas is sister to Eopharyngia, diverging before their ancestor lost hydrogenosomes and acquired a cytopharynx. Removal of anaeromonads and Carpediemonas makes Loukozoa more homogeneous, being basically biciliate, aerobic and free-living, in contrast to Metamonada. A new taxon-rich rRNA tree supports holophyly of Discicristata and Trichozoa strongly, holophyly of Metamonada and Excavata and paraphyly of Loukozoa weakly. Mitochondria were probably transformed into hydrogenosomes independently in the ancestors of lyromonad Percolozoa and Metamonada and further reduced in the ancestral eopharyngian. Evidence is briefly discussed that Metamonada and all other excavates share a photosynthetic ancestry with Euglenozoa and are secondarily non-photosynthetic, as predicted by the cabozoan hypothesis for a single secondary symbiogenetic acquisition of green algal plastids by the last common ancestor of Euglenozoa and Cercozoa. Excavata plus core Rhizaria (Cercozoa, Retaria) probably form an ancestrally photophagotrophic clade. The origin from a benthic loukozoan ancestor of the characteristic cellular features of Percolozoa and Euglenozoa through divergent adaptations for feeding on or ...

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Section: Changing Views Of the Metamonadamentioning

confidence: 99%

The excavate protozoan phyla Metamonada Grasse emend. (Anaeromonadea, Parabasalia, Carpediemonas, Eopharyngia) and Loukozoa emend. (Jakobea, Malawimonas): their evolutionary affinities and new higher taxa

Cavalier‐Smith

2003

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLO

103

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“…It was thus enormously useful as a guide to study. It gained considerable support when the first phylogenetic trees based upon molecular sequence data (Vossbrinck et al 1987;Sogin et al 1989;Leipe et al 1993;Hashimoto et al 1997) did indeed place key archezoans before other eukaryotes with mitochondria. Doubts were expressed about the veracity of these trees (e.g.…”

Section: Introductionmentioning

confidence: 99%

Multiple secondary origins of the anaerobic lifestyle in eukaryotes

Embley

2006

Phil. Trans. R. Soc. B

111

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Classical ideas for early eukaryotic evolution often posited a period of anaerobic evolution producing a nucleated phagocytic cell to engulf the mitochondrial endosymbiont, whose presence allowed the host to colonize emerging aerobic environments. This idea was given credence by the existence of contemporary anaerobic eukaryotes that were thought to primitively lack mitochondria, thus providing examples of the type of host cell needed. However, the groups key to this hypothesis have now been shown to contain previously overlooked mitochondrial homologues called hydrogenosomes or mitosomes; organelles that share common ancestry with mitochondria but which do not carry out aerobic respiration. Mapping these data on the unfolding eukaryotic tree reveals that secondary adaptation to anaerobic habitats is a reoccurring theme among eukaryotes. The apparent ubiquity of mitochondrial homologues bears testament to the importance of the mitochondrial endosymbiosis, perhaps as a founding event, in eukaryotic evolution. Comparative study of different mitochondrial homologues is needed to determine their fundamental importance for contemporary eukaryotic cells.

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“…G. intestinalis, G. lamblia) is a flagellated protozoan parasite of medical significance because it is a major cause of waterborne enteric disease worldwide (Adam, 1991). The biology of this parasite is of particular interest because it represents one of the earliest branching lineages of eukaryotic descent, based on phylogenetic analysis of ribosomal and protein coding sequences (Sogin et al, 1989;Leipe et al, 1993;Gupta et al, 1994;Drouin et al, 1995;Roger et al, 1999). Giardia also lacks organelles typical for higher eukaryotes such as mitochondria and peroxisomes.…”

Section: Introductionmentioning

confidence: 99%

Stage-Specific Expression and Targeting of Cyst Wall Protein–Green Fluorescent Protein Chimeras inGiardia

Hehl

Marti

Kohler

2000

MBoC

141

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In preparation for being shed into the environment as infectious cysts, trophozoites of Giardia spp. synthesize and deposit large amounts of extracellular matrix into a resistant extracellular cyst wall. Functional aspects of this developmentally regulated process were investigated by expressing a series of chimeric cyst wall protein 1 (CWP1)-green fluorescent protein (GFP) reporter proteins. It was demonstrated that a short 110 bp 5Ј flanking region of the CWP1 gene harbors all necessary cis-DNA elements for strictly encystation-specific expression of a reporter during in vitro encystation, whereas sequences in the 3Ј flanking region are involved in modulation of steady-state levels of its mRNA during encystation. Encysting Giardia expressing CWP1-GFP chimeras showed formation and maturation of labeled dense granule-like vesicles and subsequent incorporation of GFP-tagged protein into the cyst wall, dependent on which domains of CWP1 were included. The N-terminal domain of CWP1 was required for targeting GFP to regulated compartments of the secretory apparatus, whereas a central domain containing leucine-rich repeats mediated association of the chimera with the extracellular cyst wall. We show that analysis of protein transport using GFP-tagged molecules is feasible in an anaerobic organism and provides a useful tool for investigating the organization of primitive eukaryotic vesicular transport. INTRODUCTIONGiardia duodenalis (syn. G. intestinalis, G. lamblia) is a flagellated protozoan parasite of medical significance because it is a major cause of waterborne enteric disease worldwide (Adam, 1991). The biology of this parasite is of particular interest because it represents one of the earliest branching lineages of eukaryotic descent, based on phylogenetic analysis of ribosomal and protein coding sequences (Sogin et al., 1989;Leipe et al., 1993;Gupta et al., 1994;Drouin et al., 1995;Roger et al., 1999). Giardia also lacks organelles typical for higher eukaryotes such as mitochondria and peroxisomes. Asexually dividing, motile trophozoites colonize the upper intestine of humans and other mammals, where they attach to the intestinal epithelium (Adam, 1991). Encysting Giardia trophozoites undergo a series of developmental changes in the course of which they synthesize, export, and assemble an extensive fibrillar extracellular matrix composed of proteins but also a large proportion of carbohydrate, mainly in the form of N-acetylgalactosamine (Manning et al., 1992). Formation of environmentally resistant cysts is a key step in Giardia development as in other eukaryotic pathogens (Eichinger, 1997;Taratuto and Venturiello, 1997;Dubey et al., 1998) that has not been well characterized on a molecular level. Therefore, a better understanding of the mechanisms that govern stage-specific regulation of genes and the synthesis, transport, and assembly of the cyst wall is needed.Several genes that are up-regulated during Giardia encystation have been identified recently by biochemical approaches, molecular genetics, or metab...

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Small subunit ribosomal RNA+ of Hexamita inflata and the quest for the first branch in the eukaryotic tree

Cited by 220 publications

References 15 publications

The excavate protozoan phyla Metamonada Grasse emend. (Anaeromonadea, Parabasalia, Carpediemonas, Eopharyngia) and Loukozoa emend. (Jakobea, Malawimonas): their evolutionary affinities and new higher taxa

The excavate protozoan phyla Metamonada Grasse emend. (Anaeromonadea, Parabasalia, Carpediemonas, Eopharyngia) and Loukozoa emend. (Jakobea, Malawimonas): their evolutionary affinities and new higher taxa

Multiple secondary origins of the anaerobic lifestyle in eukaryotes

Stage-Specific Expression and Targeting of Cyst Wall Protein–Green Fluorescent Protein Chimeras inGiardia

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