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Relative Mutation Rates in Nucleomorph-Bearing Algae.

ABSTRACT: Chlorarachniophyte and cryptophyte algae are unique among plastid-containing species in that they have a nucleomorph genome: a compact, highly reduced nuclear genome from a photosynthetic eukaryotic endosymbiont. Despite their independent origins, the nucleomorph genomes of these two lineages have similar genomic architectures, but little is known about the evolutionary pressures impacting nucleomorph DNA, particularly how their rates of evolution compare to those of the neighboring genetic compartments (the mitochondrion, plastid, and nucleus). Here, we use synonymous substitution rates to estimate relative mutation rates in the four genomes of nucleomorph-bearing algae. We show that the relative mutation rates of the host versus endosymbiont nuclear genomes are similar in both chlorarachniophytes and cryptophytes, despite the fact that nucleomorph gene sequences are notoriously highly divergent. There is some evidence, however, for slightly elevated mutation rates in the nucleomorph DNA of chlorarachniophytes-a feature not observed in that of cryptophytes. For both lineages, relative mutation rates in the plastid appear to be lower than those in the nucleus and nucleomorph (and, in one case, the mitochondrion), which is consistent with studies of other plastid-bearing protists. Given the divergent nature of nucleomorph genes, our finding of relatively low evolutionary rates in these genomes suggests that for both lineages a burst of evolutionary change and/or decreased selection pressures likely occurred early in the integration of the secondary endosymbiont.

SUBMITTER: Grisdale CJ

PROVIDER: S-EPMC6456004 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Relative Mutation Rates in Nucleomorph-Bearing Algae.

Grisdale Cameron J CJ Smith David R DR Archibald John M JM

Genome biology and evolution 20190401 4

Chlorarachniophyte and cryptophyte algae are unique among plastid-containing species in that they have a nucleomorph genome: a compact, highly reduced nuclear genome from a photosynthetic eukaryotic endosymbiont. Despite their independent origins, the nucleomorph genomes of these two lineages have similar genomic architectures, but little is known about the evolutionary pressures impacting nucleomorph DNA, particularly how their rates of evolution compare to those of the neighboring genetic comp ...[more]

PMID: 30859201

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Project description:Nucleomorphs are residual nuclei derived from eukaryotic endosymbionts in chlorarachniophyte and cryptophyte algae. The endosymbionts that gave rise to nucleomorphs and plastids in these two algal groups were green and red algae, respectively. Despite their independent origin, the chlorarachniophyte and cryptophyte nucleomorph genomes share similar genomic features such as extreme size reduction and a three-chromosome architecture. This suggests that similar reductive evolutionary forces have acted to shape the nucleomorph genomes in the two groups. Thus far, however, only a single chlorarachniophyte nucleomorph and plastid genome has been sequenced, making broad evolutionary inferences within the chlorarachniophytes and between chlorarachniophytes and cryptophytes difficult. We have sequenced the nucleomorph and plastid genomes of the chlorarachniophyte Lotharella oceanica in order to gain insight into nucleomorph and plastid genome diversity and evolution.The L. oceanica nucleomorph genome was found to consist of three linear chromosomes totaling ~610 kilobase pairs (kbp), much larger than the 373 kbp nucleomorph genome of the model chlorarachniophyte Bigelowiella natans. The L. oceanica plastid genome is 71 kbp in size, similar to that of B. natans. Unexpectedly long (~35 kbp) sub-telomeric repeat regions were identified in the L. oceanica nucleomorph genome; internal multi-copy regions were also detected. Gene content analyses revealed that nucleomorph house-keeping genes and spliceosomal intron positions are well conserved between the L. oceanica and B. natans nucleomorph genomes. More broadly, gene retention patterns were found to be similar between nucleomorph genomes in chlorarachniophytes and cryptophytes. Chlorarachniophyte plastid genomes showed near identical protein coding gene complements as well as a high level of synteny.We have provided insight into the process of nucleomorph genome evolution by elucidating the fine-scale dynamics of sub-telomeric repeat regions. Homologous recombination at the chromosome ends appears to be frequent, serving to expand and contract nucleomorph genome size. The main factor influencing nucleomorph genome size variation between different chlorarachniophyte species appears to be expansion-contraction of these telomere-associated repeats rather than changes in the number of unique protein coding genes. The dynamic nature of chlorarachniophyte nucleomorph genomes lies in stark contrast to their plastid genomes, which appear to be highly stable in terms of gene content and synteny.

Dataset Information

Relative Mutation Rates in Nucleomorph-Bearing Algae.

Publications

Relative Mutation Rates in Nucleomorph-Bearing Algae.

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