Pelobionts are Degenerate Protists: Insights from Molecules and Morphology1

Edgcomb, Virginia P.; Simpson, Alastair G. B.; Zettler, Linda A. Amaral; Nerad, Thomas A.; Patterson, David J.; Holder, Michael; Sogin, Mitchell L.

doi:10.1093/oxfordjournals.molbev.a004157

Cited by 27 publications

(15 citation statements)

References 36 publications

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“…Of the named breviate genera, Pygsuia is the deepest branch, with near maximal bootstrap and PP support recovered for the Breviata and Subulatomonas clade to exclusion of Pygsuia (see the electronic supplementary material, figure S11). Although these results confirm that P. biforma is a breviate, the placement of the group in the global SSU rDNA phylogeny of eukaryotes is not well resolved (see the electronic supplementary material, figure S11) [4,13,43].…”

Section: Results and Discussion (A) Pygsuia Is A Novel Breviatementioning

confidence: 82%

Phylogenomics demonstrates that breviate flagellates are related to opisthokonts and apusomonads

et al. 2013

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Most eukaryotic lineages belong to one of a few major groups. However, several protistan lineages have not yet been robustly placed in any of these groups. Both the breviates and apusomonads are two such lineages that appear to be related to the Amoebozoa and Opisthokonta (i.e. the 'unikonts' or Amorphea); however, their precise phylogenetic positions remain unclear. Here, we describe a novel microaerophilic breviate, Pygsuia biforma gen. nov. sp. nov., isolated from a hypoxic estuarine sediment. Ultrastructurally, this species resembles the breviate genera Breviata and Subulatomonas but has two cell morphologies, adherent and swimming. Phylogenetic analyses of the small sub-unit rRNA gene show that Pygsuia is the sister to the other breviates. We constructed a 159-protein supermatrix, including orthologues identified in RNA-seq data from Pygsuia. Phylogenomic analyses of this dataset show that breviates, apusomonads and Opisthokonta form a strongly supported major eukaryotic grouping we name the Obazoa. Although some phylogenetic methods disagree, the balance of evidence suggests that the breviate lineage forms the deepest branch within Obazoa. We also found transcripts encoding a nearly complete integrin adhesome from Pygsuia, indicating that this protein complex involved in metazoan multicellularity may have evolved earlier in eukaryote evolution than previously thought.

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Section: Results and Discussion (A) Pygsuia Is A Novel Breviatementioning

confidence: 82%

Phylogenomics demonstrates that breviate flagellates are related to opisthokonts and apusomonads

et al. 2013

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“…Entamoeba and the ε‐proteobacteria commonly reside within the gut of an animal host, where the LGT could have happened (van der Giezen et al ., 2004). However, because the common ancestor of both Entamoeba and Mastigamoeba is thought to have been a free‐living amoeba (Edgcomb et al ., 2002), we think it is very unlikely that such a transfer occurred in the gut of an animal host. ε‐Proteobacteria have also been detected or isolated from other environments, such as deep subsurface sediments, oil fields, activated sludge and marine snow (Campbell et al ., 2001), where the transfer could have happened.…”

Section: Resultsmentioning

confidence: 99%

Novel mitochondrion‐related organelles in the anaerobic amoeba Mastigamoeba balamuthi

Gill

Díaz-Triviño

Barberà

et al. 2007

Molecular Microbiology

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SummaryUnicellular eukaryotes that lack mitochondria typically contain related organelles such as hydrogenosomes or mitosomes. To characterize the evolutionary diversity of these organelles, we conducted an expressed sequence tag (EST) survey on the freeliving amoeba Mastigamoeba balamuthi, a relative of the human parasite Entamoeba histolytica. From 19 182 ESTs, we identified 21 putative mitochondrial proteins implicated in protein import, amino acid interconversion and carbohydrate metabolism, two components of the iron-sulphur cluster (Fe-S) assembly apparatus as well as two enzymes characteristic of hydrogenosomes. By immunofluorescence microscopy and subcellular fractionation, we show that mitochondrial chaperonin 60 is targeted to small abundant organelles within Mastigamoeba. In transmission electron micrographs, we identified doublemembraned compartments that likely correspond to these mitochondrion-derived organelles, The predicted organellar proteome of the Mastigamoeba organelle indicates a unique spectrum of functions that collectively have never been observed in mitochondrion-related organelles. However, like Entamoeba, the Fe-S cluster assembly proteins in Mastigamoeba were acquired by lateral gene transfer from e-proteobacteria and do not possess obvious organellar targeting peptides. These data indicate that the loss of classical aerobic mitochondrial functions and acquisition of anaerobic enzymes and Fe-S cluster assembly proteins occurred in a free-living member of the eukaryote super-kingdom Amoebozoa.

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“…These incongruences are restricted to clades C2 and C1. Inconsistencies in phylogenetic reconstruction using different marker genes are not uncommon in protists (Edgcomb et al, 2002;Nishi et al, 2005;Philippe & Adoutte, 1996;Shalchian-Tabrizi et al, 2006a, b) and highlight fundamental difficulties in phylogenetic reconstruction (Philippe & Adoutte, 1996). Firstly, evolutionary rates of different genes may be highly variable within the genes as well as between different organisms, resulting in different tree topologies (Philippe et al, 2000).…”

Section: Discussion Single-gene Analysesmentioning

confidence: 99%

Multigene phylogenies of clonal Spumella-like strains, a cryptic heterotrophic nanoflagellate, isolated from different geographical regions

Stoeck¹,

Jost²,

Boenigk³

2008

INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLO

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Many nanoflagellate morphospecies comprise an enormous variation of genotypes, probably indicating cryptic species. One of the best-investigated morphospecies with respect to molecular and ecophysiological variation are flagellates of the Spumella morphotype. Here, we have phylogenetically analysed three protein-coding genes (actin, alpha-tubulin, beta-tubulin), internal transcribed spacers (ITS1, ITS2) and the 5.8S rDNA of 17 Spumella-like strains isolated from soil, freshwater and marine samples in order to (i) test the validity of the current Spumella-like phylogenetic classification system based exclusively on small subunit (SSU) rDNA, (ii) elucidate the phylogenetic associations of SSU rDNA-unresolved strains and (iii) evaluate the validity of the assignment of ecophysiological adaptations to previously identified SSU rDNA sequence clades. All single-gene analyses show different patterns of support, are incongruent and identify a number of conflicting nodes. Likewise, a concatenation of all protein genes fails to recover specific SSU rDNA clades. However, a combined analysis of all genes confidently resolved the conflicts of the single genes and the protein-gene concatenations and resulted in a tree topology that is identical to the SSU rDNA analysis, but with enhanced phylogenetic resolution and decisively greater support. We conclude that, depending on the genes concatenated, a 'supergene' analysis minimizes artefactual effects of single genes and may be superior in its performance in phylogenetically analysing cryptic species. We confirm the validity of the SSU rDNA Spumella-like phyloclades and support the suggestion that these clades indeed seem to reflect certain ecophysiological adaptations. INTRODUCTIONIn protistology, species descriptions often pragmatically conform to the morphological species concept: microbial eukaryotes have traditionally been identified on the basis of their morphological diversity (Finlay et al., 1996). In general, such a concept seems to work well for a number of larger protists. However, numerous smaller species (nanoand picoeukaryotes) are morphologically indistinguishable (Coleman, 2002;Hackstein, 1997;Nanney, 2004), as evolution and speciation in microbial eukaryotes are not necessarily accompanied by a perceptible morphological change (Machelon et al., 1984). As a consequence, distinct microbial eukaryote species are often classified as a single species (5cryptic species). The prevalence of such cryptic species impairs biodiversity estimates and analyses of spatial distribution patterns and ecological functions (Bickford et al., 2006;Coleman, 2002;Hackstein, 1997).A group of organisms that falls into this category are colourless chrysophytes often referred to as 'Spumella-like' flagellates or Spumella spp. (Auer & Arndt, 2001;Cleven & Weisse, 2001;Weitere & Arndt, 2003). These organisms account for a substantial proportion of the heterotrophic nanoflagellate (HNF) biomass, especially in freshwater systems (Domaizon et al., 2003;Felip et al., 1999;Zhao et al., 2003), and...

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Pelobionts are Degenerate Protists: Insights from Molecules and Morphology1

Cited by 27 publications

References 36 publications

Phylogenomics demonstrates that breviate flagellates are related to opisthokonts and apusomonads

Phylogenomics demonstrates that breviate flagellates are related to opisthokonts and apusomonads

Novel mitochondrion‐related organelles in the anaerobic amoeba Mastigamoeba balamuthi

Multigene phylogenies of clonal Spumella-like strains, a cryptic heterotrophic nanoflagellate, isolated from different geographical regions

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