Deep RNA sequencing reveals the smallest known mitochondrial micro exon in animals: The placozoan cox1 single base pair exon

Osigus, Hans-Jürgen; Eitel, Michael; Schierwater, Bernd

doi:10.1371/journal.pone.0177959

Cited by 13 publications

(12 citation statements)

References 35 publications

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“…The circular H . hongkongensis mitochondrial genome has a size of 36,537 bp and shares a 1-bp exon in the cox1 gene with other placozoans [ 91 ]. It shares all genes and has the identical gene order as the two already published placozoan mitogenomes of clade V (haplotypes H4 and H15; [ 61 , 90 ]).…”

Section: Methodsmentioning

confidence: 99%

Comparative genomics and the nature of placozoan species

et al. 2018

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Placozoans are a phylum of nonbilaterian marine animals currently represented by a single described species, Trichoplax adhaerens, Schulze 1883. Placozoans arguably show the simplest animal morphology, which is identical among isolates collected worldwide, despite an apparently sizeable genetic diversity within the phylum. Here, we use a comparative genomics approach for a deeper appreciation of the structure and causes of the deeply diverging lineages in the Placozoa. We generated a high-quality draft genome of the genetic lineage H13 isolated from Hong Kong and compared it to the distantly related T. adhaerens. We uncovered substantial structural differences between the two genomes that point to a deep genomic separation and provide support that adaptation by gene duplication is likely a crucial mechanism in placozoan speciation. We further provide genetic evidence for reproductively isolated species and suggest a genus-level difference of H13 to T. adhaerens, justifying the designation of H13 as a new species, Hoilungia hongkongensis nov. gen., nov. spec., now the second described placozoan species and the first in a new genus. Our multilevel comparative genomics approach is, therefore, likely to prove valuable for species distinctions in other cryptic microscopic animal groups that lack diagnostic morphological characters, such as some nematodes, copepods, rotifers, or mites.

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Section: Methodsmentioning

confidence: 99%

Comparative genomics and the nature of placozoan species

et al. 2018

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“…The nucleotide sequence and annotation data of H13 mitogenomes were downloaded from the genome repository ( https://bitbucket.org/molpalmuc/hoilungia-genome/src/master/mitochondrial_genome/ : last accessed August 2, 2018). Cox1 annotation was conducted using KY310743.1 ( Osigus et al. 2017 ) as a reference.…”

Section: Methodsmentioning

confidence: 99%

“…2018 ); 2) cis- and trans- splicing group I and trans- splicing group II introns ( Burger et al. 2009 ); 3) a single nucleotide exon in cox1 ( Osigus et al. 2017 ; Eitel et al.…”

Section: Introductionmentioning

confidence: 99%

Mitochondrial Genome Evolution of Placozoans: Gene Rearrangements and Repeat Expansions

Miyazawa

Osigus

Rolfes

et al. 2020

Genome Biology and Evolution

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Placozoans, non-bilaterian animals with the simplest known metazoan bauplan, are currently classified into 20 haplotypes belonging to three genera, Polyplacotoma, Trichoplax, and Hoilungia. The latter two comprise two and five clades, respectively. In Trichoplax and Hoilungia, previous studies on six haplotypes belonging to four different clades have shown that their mtDNA are circular chromosomes of 32-43 kbp in size, which encode 12 protein-coding genes, 24 tRNAs, and 2 rRNAs. These mitochondrial genomes (mitogenomes) also show unique features rarely seen in other metazoans, including open reading frames (ORFs) of unknown function, and group I and II introns. Here, we report seven new mitogenomes, covering the five previously described haplotypes H2, H17, H19, H9, and H11, as well as two new haplotypes, H23 (clade III) and H24 (clade VII). The overall gene content is shared between all placozoan mitochondrial genomes, but genome sizes, gene orders, and several exon-intron boundaries vary among clades. Phylogenomic analyses strongly support a tree topology different from previous 16S rRNA analyses, with clade VI as the sister group to all other Hoilungia clades. We found small inverted repeats in all 13 mitochondrial genomes of the Trichoplax and Hoilungia genera and evaluated their distribution patterns among haplotypes. Since P. mediterranea (H0), the sister to the remaining haplotypes, has a small mitochondrial genome with few small inverted repeats and ORFs, we hypothesized that the proliferation of inverted repeats and ORFs substantially contributed to the observed increase in the size and GC content of the Trichoplax and Hoilungia mitochondrial genomes.

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“…Assembly completeness for the H2 genome was estimated by mapping the 150 bp paired-end reads against the H2 assembly, the endosymbiont assembly and the mitochondrial genome 54 [Osigus et al ., in prep] with BWA MEM 55 and calling the mapping rate with Samtools 1.2 56 . The completeness was also assessed by estimating the presence of core eukaryotic and core metazoan genes using CEGMA v2.5 21 and BUSCO v1.1b1 22 , respectively.…”

Section: Methodsmentioning

confidence: 99%

Trichoplax genomes reveal profound admixture and suggest stable wild populations without bisexual reproduction

Kamm

Osigus

Stadler

et al. 2018

Sci Rep

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The phylum Placozoa officially consists of only a single described species, Trichoplax adhaerens, although several lineages can be separated by molecular markers, geographical distributions and environmental demands. The placozoan 16S haplotype H2 (Trichoplax sp. H2) is the most robust and cosmopolitan lineage of placozoans found to date. In this study, its genome was found to be distinct but highly related to the Trichoplax adhaerens reference genome, for remarkably unique reasons. The pattern of variation and allele distribution between the two lineages suggests that both originate from a single interbreeding event in the wild, dating back at least several decades ago, and both seem not to have engaged in sexual reproduction since. We conclude that populations of certain placozoan haplotypes remain stable for long periods without bisexual reproduction. Furthermore, allelic variation within and between the two Trichoplax lineages indicates that successful bisexual reproduction between related placozoan lineages might serve to either counter accumulated negative somatic mutations or to cope with changing environmental conditions. On the other hand, enrichment of neutral or beneficial somatic mutations by vegetative reproduction, combined with rare sexual reproduction, could instantaneously boost genetic variation, generating novel ecotypes and eventually species.

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Deep RNA sequencing reveals the smallest known mitochondrial micro exon in animals: The placozoan cox1 single base pair exon

Cited by 13 publications

References 35 publications

Comparative genomics and the nature of placozoan species

Comparative genomics and the nature of placozoan species

Mitochondrial Genome Evolution of Placozoans: Gene Rearrangements and Repeat Expansions

Trichoplax genomes reveal profound admixture and suggest stable wild populations without bisexual reproduction

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