Long-read DNA sequencing reveals the organization of the mitochondrial genome in the early-branching dinoflagellate Oxyrrhis marina
The mitochondrial genomes of dinoflagellate protists are remarkable for their highly fragmented and heterogeneous organization. Early attempts to determine their structure without ‘next-generation’ DNA sequencing failed to recover a defined genome. Still, it coincided in showing that the proteins co...
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description | The mitochondrial genomes of dinoflagellate protists are remarkable for their highly fragmented and heterogeneous organization. Early attempts to determine their structure without ‘next-generation’ DNA sequencing failed to recover a defined genome. Still, it coincided in showing that the proteins coding genes, three in total, and parts of the ribosomal RNA genes were spread across a diffuse assortment of small linear fragments. In contrast, a recent study employed Illumina sequencing to assemble a 326 kbp long single-molecule, circular mitochondrial genome in the symbiotic dinoflagellate Breviolum minutum. Here, we used a combination of short- and long-read massively-parallel DNA sequencing to analyze further the mitochondrial DNA of the early-branching dinoflagellate Oxyrrhis marina. We found that the mitochondrial genome of O. marina consists of 3 linear chromosomes sized 15.9, 33.8 and 40.6 kbp for a total of 90.3 kbp. It contains the cox1, cox3 and cob genes, the same three proteins encoded in the mitochondrion of all myzozoans (Apicomplexa and Dinophyceae), some fragments of ribosomal RNA genes as well as many non-functional gene fragments and extensive noncoding DNA. Our analysis unveiled segments syntenic patterns and rearrangements encompassing coding and non-coding regions, suggesting that recombination is a pervasive process driving the evolution of these genomes.
•The organization of mitogenomes in dinoflagellates has been elusive due to extensive fragmentation, redundancy and recombination.•Long-read DNA sequencing enabled the assembly of a 90 kbp mitogenome in Oxyrrhis marina, an early-diverging dinoflagellate.•The genome consists of three linear molecules encoding three proteins, rRNA fragments, no tRNA genes, non-functional gene fragments, and noncoding DNA.•Excess of noncoding DNA appears to originate from the mutational degradation of gene duplicates. |
doi_str_mv | 10.1016/j.protis.2024.126071 |
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•The organization of mitogenomes in dinoflagellates has been elusive due to extensive fragmentation, redundancy and recombination.•Long-read DNA sequencing enabled the assembly of a 90 kbp mitogenome in Oxyrrhis marina, an early-diverging dinoflagellate.•The genome consists of three linear molecules encoding three proteins, rRNA fragments, no tRNA genes, non-functional gene fragments, and noncoding DNA.•Excess of noncoding DNA appears to originate from the mutational degradation of gene duplicates.</description><identifier>ISSN: 1434-4610</identifier><identifier>ISSN: 1618-0941</identifier><identifier>EISSN: 1618-0941</identifier><identifier>DOI: 10.1016/j.protis.2024.126071</identifier><identifier>PMID: 39603112</identifier><language>eng</language><publisher>Germany: Elsevier GmbH</publisher><subject>Alveolate ; Dinoflagellida - classification ; Dinoflagellida - genetics ; Dinophyceae ; DNA, Mitochondrial - genetics ; DNA, Protozoan - genetics ; evolution ; genes ; Genome, Mitochondrial - genetics ; Genome, Protozoan - genetics ; High-Throughput Nucleotide Sequencing ; intergenic DNA ; Mitochondria ; mitochondrial DNA ; mitochondrial genome ; Non-coding DNA ; Oxyrrhis marina ; protists ; Recombination ; Ribosomal RNA ; Sequence Analysis, DNA</subject><ispartof>Protist, 2024-12, Vol.175 (6), p.126071, Article 126071</ispartof><rights>2024 The Authors</rights><rights>Copyright © 2024 The Authors. Published by Elsevier GmbH.. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c320t-8f633685b1fa0436a97ed462afc4b196b7127b1ee1c24aac4fdc6a4337d52bd43</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S1434461024000634$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39603112$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Haro, Ronie</creatorcontrib><creatorcontrib>Walunjkar, Nikita</creatorcontrib><creatorcontrib>Jorapur, Soham</creatorcontrib><creatorcontrib>Slamovits, Claudio H.</creatorcontrib><title>Long-read DNA sequencing reveals the organization of the mitochondrial genome in the early-branching dinoflagellate Oxyrrhis marina</title><title>Protist</title><addtitle>Protist</addtitle><description>The mitochondrial genomes of dinoflagellate protists are remarkable for their highly fragmented and heterogeneous organization. Early attempts to determine their structure without ‘next-generation’ DNA sequencing failed to recover a defined genome. Still, it coincided in showing that the proteins coding genes, three in total, and parts of the ribosomal RNA genes were spread across a diffuse assortment of small linear fragments. In contrast, a recent study employed Illumina sequencing to assemble a 326 kbp long single-molecule, circular mitochondrial genome in the symbiotic dinoflagellate Breviolum minutum. Here, we used a combination of short- and long-read massively-parallel DNA sequencing to analyze further the mitochondrial DNA of the early-branching dinoflagellate Oxyrrhis marina. We found that the mitochondrial genome of O. marina consists of 3 linear chromosomes sized 15.9, 33.8 and 40.6 kbp for a total of 90.3 kbp. It contains the cox1, cox3 and cob genes, the same three proteins encoded in the mitochondrion of all myzozoans (Apicomplexa and Dinophyceae), some fragments of ribosomal RNA genes as well as many non-functional gene fragments and extensive noncoding DNA. Our analysis unveiled segments syntenic patterns and rearrangements encompassing coding and non-coding regions, suggesting that recombination is a pervasive process driving the evolution of these genomes.
•The organization of mitogenomes in dinoflagellates has been elusive due to extensive fragmentation, redundancy and recombination.•Long-read DNA sequencing enabled the assembly of a 90 kbp mitogenome in Oxyrrhis marina, an early-diverging dinoflagellate.•The genome consists of three linear molecules encoding three proteins, rRNA fragments, no tRNA genes, non-functional gene fragments, and noncoding DNA.•Excess of noncoding DNA appears to originate from the mutational degradation of gene duplicates.</description><subject>Alveolate</subject><subject>Dinoflagellida - classification</subject><subject>Dinoflagellida - genetics</subject><subject>Dinophyceae</subject><subject>DNA, Mitochondrial - genetics</subject><subject>DNA, Protozoan - genetics</subject><subject>evolution</subject><subject>genes</subject><subject>Genome, Mitochondrial - genetics</subject><subject>Genome, Protozoan - genetics</subject><subject>High-Throughput Nucleotide Sequencing</subject><subject>intergenic DNA</subject><subject>Mitochondria</subject><subject>mitochondrial DNA</subject><subject>mitochondrial genome</subject><subject>Non-coding DNA</subject><subject>Oxyrrhis marina</subject><subject>protists</subject><subject>Recombination</subject><subject>Ribosomal RNA</subject><subject>Sequence Analysis, DNA</subject><issn>1434-4610</issn><issn>1618-0941</issn><issn>1618-0941</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkU-PFCEQxYnRuOvoNzCGo5ceKaDp7ovJZv2bTNyLngkN1T1MumGFno3j1S8us716NF6AwKv3qPoR8hLYFhioN4ftbYqLz1vOuNwCV6yBR-QSFLQV6yQ8LmcpZCUVsAvyLOcDYyA71T4lF6JTTADwS_JrF8NYJTSOvvtyRTN-P2KwPow04R2aKdNljzSm0QT_0yw-BhqH-7vZL9HuY3DJm4mOGOKM1If7NzRpOlV9MsHuz17OhzhMZsRpMgvSmx-nlPY-09kkH8xz8mQoSfjiYd-Qbx_ef73-VO1uPn6-vtpVVnC2VO2ghFBt3cNgmBTKdA06qbgZrOyhU30DvOkBESyXxlg5OKuMFKJxNe-dFBvyevUtgytt5kXPPtvznwLGY9YCasnrlin1H9JiK2pelg2Rq9SmmHPCQd8mXxo7aWD6TEof9EpKn0nplVQpe_WQcOxndH-L_qApgrerAMtI7jwmna0vbND5hHbRLvp_J_wGrO-ooA</recordid><startdate>20241201</startdate><enddate>20241201</enddate><creator>Haro, Ronie</creator><creator>Walunjkar, Nikita</creator><creator>Jorapur, Soham</creator><creator>Slamovits, Claudio H.</creator><general>Elsevier GmbH</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>7S9</scope><scope>L.6</scope></search><sort><creationdate>20241201</creationdate><title>Long-read DNA sequencing reveals the organization of the mitochondrial genome in the early-branching dinoflagellate Oxyrrhis marina</title><author>Haro, Ronie ; Walunjkar, Nikita ; Jorapur, Soham ; Slamovits, Claudio H.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c320t-8f633685b1fa0436a97ed462afc4b196b7127b1ee1c24aac4fdc6a4337d52bd43</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Alveolate</topic><topic>Dinoflagellida - classification</topic><topic>Dinoflagellida - genetics</topic><topic>Dinophyceae</topic><topic>DNA, Mitochondrial - genetics</topic><topic>DNA, Protozoan - genetics</topic><topic>evolution</topic><topic>genes</topic><topic>Genome, Mitochondrial - genetics</topic><topic>Genome, Protozoan - genetics</topic><topic>High-Throughput Nucleotide Sequencing</topic><topic>intergenic DNA</topic><topic>Mitochondria</topic><topic>mitochondrial DNA</topic><topic>mitochondrial genome</topic><topic>Non-coding DNA</topic><topic>Oxyrrhis marina</topic><topic>protists</topic><topic>Recombination</topic><topic>Ribosomal RNA</topic><topic>Sequence Analysis, DNA</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Haro, Ronie</creatorcontrib><creatorcontrib>Walunjkar, Nikita</creatorcontrib><creatorcontrib>Jorapur, Soham</creatorcontrib><creatorcontrib>Slamovits, Claudio H.</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><jtitle>Protist</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Haro, Ronie</au><au>Walunjkar, Nikita</au><au>Jorapur, Soham</au><au>Slamovits, Claudio H.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Long-read DNA sequencing reveals the organization of the mitochondrial genome in the early-branching dinoflagellate Oxyrrhis marina</atitle><jtitle>Protist</jtitle><addtitle>Protist</addtitle><date>2024-12-01</date><risdate>2024</risdate><volume>175</volume><issue>6</issue><spage>126071</spage><pages>126071-</pages><artnum>126071</artnum><issn>1434-4610</issn><issn>1618-0941</issn><eissn>1618-0941</eissn><abstract>The mitochondrial genomes of dinoflagellate protists are remarkable for their highly fragmented and heterogeneous organization. Early attempts to determine their structure without ‘next-generation’ DNA sequencing failed to recover a defined genome. Still, it coincided in showing that the proteins coding genes, three in total, and parts of the ribosomal RNA genes were spread across a diffuse assortment of small linear fragments. In contrast, a recent study employed Illumina sequencing to assemble a 326 kbp long single-molecule, circular mitochondrial genome in the symbiotic dinoflagellate Breviolum minutum. Here, we used a combination of short- and long-read massively-parallel DNA sequencing to analyze further the mitochondrial DNA of the early-branching dinoflagellate Oxyrrhis marina. We found that the mitochondrial genome of O. marina consists of 3 linear chromosomes sized 15.9, 33.8 and 40.6 kbp for a total of 90.3 kbp. It contains the cox1, cox3 and cob genes, the same three proteins encoded in the mitochondrion of all myzozoans (Apicomplexa and Dinophyceae), some fragments of ribosomal RNA genes as well as many non-functional gene fragments and extensive noncoding DNA. Our analysis unveiled segments syntenic patterns and rearrangements encompassing coding and non-coding regions, suggesting that recombination is a pervasive process driving the evolution of these genomes.
•The organization of mitogenomes in dinoflagellates has been elusive due to extensive fragmentation, redundancy and recombination.•Long-read DNA sequencing enabled the assembly of a 90 kbp mitogenome in Oxyrrhis marina, an early-diverging dinoflagellate.•The genome consists of three linear molecules encoding three proteins, rRNA fragments, no tRNA genes, non-functional gene fragments, and noncoding DNA.•Excess of noncoding DNA appears to originate from the mutational degradation of gene duplicates.</abstract><cop>Germany</cop><pub>Elsevier GmbH</pub><pmid>39603112</pmid><doi>10.1016/j.protis.2024.126071</doi><oa>free_for_read</oa></addata></record> |
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subjects | Alveolate Dinoflagellida - classification Dinoflagellida - genetics Dinophyceae DNA, Mitochondrial - genetics DNA, Protozoan - genetics evolution genes Genome, Mitochondrial - genetics Genome, Protozoan - genetics High-Throughput Nucleotide Sequencing intergenic DNA Mitochondria mitochondrial DNA mitochondrial genome Non-coding DNA Oxyrrhis marina protists Recombination Ribosomal RNA Sequence Analysis, DNA |
title | Long-read DNA sequencing reveals the organization of the mitochondrial genome in the early-branching dinoflagellate Oxyrrhis marina |
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