Evolution of anaerobic ciliates from the gastrointestinal tract: phylogenetic analysis of the ribosomal repeat from Nyctotherus ovalis and its relatives

Hoek, Angela H.A.M. van; Alen, Theo A. van; Sprakel, Vera S. I.; Hackstein, J.H.P.; Vogels, Godfried D.

doi:10.1093/oxfordjournals.molbev.a026027

Cited by 64 publications

(36 citation statements)

References 42 publications

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“…We used N. ovalis as an outgroup, because this anaerobic ciliate is paraphyletic to spirotrichs (20). Phylogenetic analyses were con-ducted by using PAUP 4.0 (21) for optimality criteria maximum parsimony (MP) and minimum evolution (ME) and TREEPUZZLE 5.0 (22) for quartet-puzzling (QP) tree reconstruction.…”

Section: Methodsmentioning

confidence: 99%

The evolutionary origin of a complex scrambled gene

Chang

Bryson

Liang

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

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Some species of ciliates undergo massive DNA elimination and genome rearrangement to construct gene-sized ''chromosomes'' in their somatic nucleus. An example is the extensively scrambled DNA polymerase ␣ gene that is broken into 48 pieces and distributed over two unlinked loci in Stylonychia. To understand the emergence of this complex phenomenon during evolution, we examined DNA polymerase ␣ genes in several earlier diverging species, representing evolutionary intermediates. Mapping these data onto an evolutionary tree suggests that this gene became extensively fragmented and scrambled over evolutionary time through a series of steps, each leading to greater complexity. Our results also suggest a possible mechanism for intron loss by deletion of intron sequences as DNA during development of the somatic nucleus.ciliate ͉ DNA polymerase ͉ hypotrich ͉ intron loss ͉ spirotrich C iliates comprise a diverse group of microbial eukaryotes, or protists. These organisms contain two types of nuclei: a somatic macronucleus that is active during vegetative growth and a germ-line micronucleus that is quiescent except during sexual recombination (1). During sexual conjugation, the two mating cells exchange haploid micronuclei, after which the old macronucleus degrades, and the new diploid micronucleus develops into the new macronucleus. Extensive loss of DNA from the long micronuclear chromosomes, coupled to DNA rearrangement, removes transposons and most intergenic spacer DNA between genes, as well as intragenic spacer DNA, known as internal eliminated segments (IESs). In spirotrichous (formerly hypotrichous) ciliates, the remaining DNA sequences, known as macronuclear destined segments (MDSs), can occupy as little as 2-5% of the germ-line genome. These mostly coding regions assemble together to form Ϸ24,000 types of DNA molecules in the somatic nucleus. Because their average size is just 2.2 kbp and they usually contain only one gene, they are sometimes called ''nano-chromosomes.'' Short telomeres are added to both ends before these molecules are amplified several-thousand-fold (1-3).Furthermore, the germ-line order of the coding regions in 20-30% of the genes in stichotrichous ciliates (a subset of spirotrichous ciliates) are permuted, or scrambled, relative to their linear order in the macronucleus. Although the mechanism of reordering these segments is not well understood, short direct repeats, called pointers, may guide the unscrambling process (1, 4). Invariably, one copy of a repeated word pair is present at the 3Ј end of germ-line segment n and at the 5Ј end of segment n ϩ 1, providing the information to link them together, with only one copy of the repeated word retained in the final DNA molecule (1). Although fragmented genes do occur in other organisms [examples include V(D)J recombination in the vertebrate immune system and split ribosomal RNA genes in the mitochondria of fungi (5) and protists (6, 7)], rarely are they sewn back together at the DNA level.Three different scrambled genes, actin I (8-10), ␣ telomer...

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Section: Methodsmentioning

confidence: 99%

The evolutionary origin of a complex scrambled gene

Chang

Bryson

Liang

et al. 2005

Proc. Natl. Acad. Sci. U.S.A.

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“…The hydrogenosomes of ciliates have been viewed as problematic because they are found among clades of anaerobic ciliates that are near relatives of aerobic clades with mitochondria (54,62,183,184). Thus, the phylogenetic reconstructions suggest that the hydrogenosomes in these clades of ciliates must have arisen independently several times.…”

Section: Hydrogen Exporter-earlymentioning

confidence: 99%

Origin and Evolution of the Mitochondrial Proteome

Kurland

Andersson

2000

Microbiol Mol Biol Rev

362

272

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SUMMARY The endosymbiotic theory for the origin of mitochondria requires substantial modification. The three identifiable ancestral sources to the proteome of mitochondria are proteins descended from the ancestral α-proteobacteria symbiont, proteins with no homology to bacterial orthologs, and diverse proteins with bacterial affinities not derived from α-proteobacteria. Random mutations in the form of deletions large and small seem to have eliminated nonessential genes from the endosymbiont-mitochondrial genome lineages. This process, together with the transfer of genes from the endosymbiont-mitochondrial genome to nuclei, has led to a marked reduction in the size of mitochondrial genomes. All proteins of bacterial descent that are encoded by nuclear genes were probably transferred by the same mechanism, involving the disintegration of mitochondria or bacteria by the intracellular membranous vacuoles of cells to release nucleic acid fragments that transform the nuclear genome. This ongoing process has intermittently introduced bacterial genes to nuclear genomes. The genomes of the last common ancestor of all organisms, in particular of mitochondria, encoded cytochrome oxidase homologues. There are no phylogenetic indications either in the mitochondrial proteome or in the nuclear genomes that the initial or subsequent function of the ancestor to the mitochondria was anaerobic. In contrast, there are indications that relatively advanced eukaryotes adapted to anaerobiosis by dismantling their mitochondria and refitting them as hydrogenosomes. Accordingly, a continuous history of aerobic respiration seems to have been the fate of most mitochondrial lineages. The initial phases of this history may have involved aerobic respiration by the symbiont functioning as a scavenger of toxic oxygen. The transition to mitochondria capable of active ATP export to the host cell seems to have required recruitment of eukaryotic ATP transport proteins from the nucleus. The identity of the ancestral host of the α-proteobacterial endosymbiont is unclear, but there is no indication that it was an autotroph. There are no indications of a specific α-proteobacterial origin to genes for glycolysis. In the absence of data to the contrary, it is assumed that the ancestral host cell was a heterotroph.

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“…ovalis, found in the hindgut of the cockroaches Periplaneta americana and Blaberus spp. 5 , has numerous hydrogenosomes that are intimately associated with endosymbiotic methane-producing Archaea, which use hydrogen produced by the hydrogenosomes (Fig. 1a).…”

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“…Modern birds have diverse and hostspecific ectoparasites 4,5 , with many birds being host to several different orders on different parts of the body 6 . The earliest undisputed fossil feathers, of Archaeopteryx from the Upper Jurassic period of Bavaria, Germany 7 , indicate that ectoparasites could have been using feathers for more than 140 million years.…”

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confidence: 99%