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      Group II intron and repeat-rich red algal mitochondrial genomes demonstrate the dynamic recent history of autocatalytic RNAs

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          Abstract

          Background

          Group II introns are mobile genetic elements that can insert at specific target sequences, however, their origins are often challenging to reconstruct because of rapid sequence decay following invasion and spread into different sites. To advance understanding of group II intron spread, we studied the intron-rich mitochondrial genome (mitogenome) in the unicellular red alga, Porphyridium.

          Results

          Analysis of mitogenomes in three closely related species in this genus revealed they were 3–6-fold larger in size (56–132 kbp) than in other red algae, that have genomes of size 21–43 kbp. This discrepancy is explained by two factors, group II intron invasion and expansion of repeated sequences in large intergenic regions. Phylogenetic analysis demonstrates that many mitogenome group II intron families are specific to Porphyridium, whereas others are closely related to sequences in fungi and in the red alga-derived plastids of stramenopiles. Network analysis of intron-encoded proteins (IEPs) shows a clear link between plastid and mitochondrial IEPs in distantly related species, with both groups associated with prokaryotic sequences.

          Conclusion

          Our analysis of group II introns in Porphyridium mitogenomes demonstrates the dynamic nature of group II intron evolution, strongly supports the lateral movement of group II introns among diverse eukaryotes, and reveals their ability to proliferate, once integrated in mitochondrial DNA.

          Supplementary Information

          The online version contains supplementary material available at 10.1186/s12915-021-01200-3.

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          Most cited references62

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          Canu: scalable and accurate long-read assembly via adaptive k-mer weighting and repeat separation

          Long-read single-molecule sequencing has revolutionized de novo genome assembly and enabled the automated reconstruction of reference-quality genomes. However, given the relatively high error rates of such technologies, efficient and accurate assembly of large repeats and closely related haplotypes remains challenging. We address these issues with Canu, a successor of Celera Assembler that is specifically designed for noisy single-molecule sequences. Canu introduces support for nanopore sequencing, halves depth-of-coverage requirements, and improves assembly continuity while simultaneously reducing runtime by an order of magnitude on large genomes versus Celera Assembler 8.2. These advances result from new overlapping and assembly algorithms, including an adaptive overlapping strategy based on tf-idf weighted MinHash and a sparse assembly graph construction that avoids collapsing diverged repeats and haplotypes. We demonstrate that Canu can reliably assemble complete microbial genomes and near-complete eukaryotic chromosomes using either Pacific Biosciences (PacBio) or Oxford Nanopore technologies and achieves a contig NG50 of >21 Mbp on both human and Drosophila melanogaster PacBio data sets. For assembly structures that cannot be linearly represented, Canu provides graph-based assembly outputs in graphical fragment assembly (GFA) format for analysis or integration with complementary phasing and scaffolding techniques. The combination of such highly resolved assembly graphs with long-range scaffolding information promises the complete and automated assembly of complex genomes.
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            RNAmmer: consistent and rapid annotation of ribosomal RNA genes

            The publication of a complete genome sequence is usually accompanied by annotations of its genes. In contrast to protein coding genes, genes for ribosomal RNA (rRNA) are often poorly or inconsistently annotated. This makes comparative studies based on rRNA genes difficult. We have therefore created computational predictors for the major rRNA species from all kingdoms of life and compiled them into a program called RNAmmer. The program uses hidden Markov models trained on data from the 5S ribosomal RNA database and the European ribosomal RNA database project. A pre-screening step makes the method fast with little loss of sensitivity, enabling the analysis of a complete bacterial genome in less than a minute. Results from running RNAmmer on a large set of genomes indicate that the location of rRNAs can be predicted with a very high level of accuracy. Novel, unannotated rRNAs are also predicted in many genomes. The software as well as the genome analysis results are available at the CBS web server.
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              EMBOSS: The European Molecular Biology Open Software Suite

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                Author and article information

                Contributors
                hsyoon2011@skku.edu
                Journal
                BMC Biol
                BMC Biol
                BMC Biology
                BioMed Central (London )
                1741-7007
                7 January 2022
                7 January 2022
                2022
                : 20
                Affiliations
                [1 ]GRID grid.264381.a, ISNI 0000 0001 2181 989X, Department of Biological Sciences, , Sungkyunkwan University, ; Suwon, 16419 South Korea
                [2 ]GRID grid.258803.4, ISNI 0000 0001 0661 1556, Department of Oceanography, , Kyungpook National University, ; Daegu, 41566 South Korea
                [3 ]GRID grid.430387.b, ISNI 0000 0004 1936 8796, Department of Biochemistry and Microbiology, , Rutgers University, ; New Brunswick, NJ 08901 USA
                Article
                1200
                10.1186/s12915-021-01200-3
                8742464
                34996446
                e4eb1c69-a074-4fbd-bf3b-7e2a75fe21b9
                © The Author(s) 2021

                Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100003566, ministry of oceans and fisheries;
                Award ID: Collaborative Genome Program of the KIMST (20180430)
                Award Recipient :
                Funded by: national research foundation (kr)
                Award ID: NRF-2017R1A2B3001923
                Award Recipient :
                Funded by: FundRef http://dx.doi.org/10.13039/100000104, national aeronautics and space administration;
                Award ID: 80NSSC19K0462
                Award Recipient :
                Funded by: nifa-usda hatch grant
                Award ID: NJ01180
                Award Recipient :
                Categories
                Research Article
                Custom metadata
                © The Author(s) 2022

                Life sciences
                genome expansion,group ii introns,repeated sequences,horizontal gene transfer,red algae

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