Literature DB >> 32094163

A cnidarian parasite of salmon (Myxozoa: Henneguya) lacks a mitochondrial genome.

Dayana Yahalomi1, Stephen D Atkinson2, Moran Neuhof3, E Sally Chang4,5, Hervé Philippe6,7, Paulyn Cartwright4, Jerri L Bartholomew2, Dorothée Huchon8,9.   

Abstract

Although aerobic respiration is a hallmark of eukaryotes, a few unicellular lineages, growing in hypoxic environments, have secondarily lost this ability. In the absence of oxygen, the mitochondria of these organisms have lost all or parts of their genomes and evolved into mitochondria-related organelles (MROs). There has been debate regarding the presence of MROs in animals. Using deep sequencing approaches, we discovered that a member of the Cnidaria, the myxozoan Henneguya salminicola, has no mitochondrial genome, and thus has lost the ability to perform aerobic cellular respiration. This indicates that these core eukaryotic features are not ubiquitous among animals. Our analyses suggest that H. salminicola lost not only its mitochondrial genome but also nearly all nuclear genes involved in transcription and replication of the mitochondrial genome. In contrast, we identified many genes that encode proteins involved in other mitochondrial pathways and determined that genes involved in aerobic respiration or mitochondrial DNA replication were either absent or present only as pseudogenes. As a control, we used the same sequencing and annotation methods to show that a closely related myxozoan, Myxobolus squamalis, has a mitochondrial genome. The molecular results are supported by fluorescence micrographs, which show the presence of mitochondrial DNA in M. squamalis, but not in H. salminicola. Our discovery confirms that adaptation to an anaerobic environment is not unique to single-celled eukaryotes, but has also evolved in a multicellular, parasitic animal. Hence, H. salminicola provides an opportunity for understanding the evolutionary transition from an aerobic to an exclusive anaerobic metabolism.

Entities:  

Keywords:  Cnidaria; MRO; cristae; mitochondria-related organelle; mitochondrial evolution

Year:  2020        PMID: 32094163      PMCID: PMC7071853          DOI: 10.1073/pnas.1909907117

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  43 in total

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Authors:  Nicolas Lartillot; Hervé Philippe
Journal:  Mol Biol Evol       Date:  2004-03-10       Impact factor: 16.240

2.  The bioenergetic costs of a gene.

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Review 3.  Diversity and origins of anaerobic metabolism in mitochondria and related organelles.

Authors:  Courtney W Stairs; Michelle M Leger; Andrew J Roger
Journal:  Philos Trans R Soc Lond B Biol Sci       Date:  2015-09-26       Impact factor: 6.237

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Journal:  Mitochondrion       Date:  2006-07-21       Impact factor: 4.160

5.  Sea anemone genome reveals ancestral eumetazoan gene repertoire and genomic organization.

Authors:  Nicholas H Putnam; Mansi Srivastava; Uffe Hellsten; Bill Dirks; Jarrod Chapman; Asaf Salamov; Astrid Terry; Harris Shapiro; Erika Lindquist; Vladimir V Kapitonov; Jerzy Jurka; Grigory Genikhovich; Igor V Grigoriev; Susan M Lucas; Robert E Steele; John R Finnerty; Ulrich Technau; Mark Q Martindale; Daniel S Rokhsar
Journal:  Science       Date:  2007-07-06       Impact factor: 47.728

6.  PhyloBayes MPI: phylogenetic reconstruction with infinite mixtures of profiles in a parallel environment.

Authors:  Nicolas Lartillot; Nicolas Rodrigue; Daniel Stubbs; Jacques Richer
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Review 7.  The Origin and Diversification of Mitochondria.

Authors:  Andrew J Roger; Sergio A Muñoz-Gómez; Ryoma Kamikawa
Journal:  Curr Biol       Date:  2017-11-06       Impact factor: 10.834

8.  Genomic insights into the evolutionary origin of Myxozoa within Cnidaria.

Authors:  E Sally Chang; Moran Neuhof; Nimrod D Rubinstein; Arik Diamant; Hervé Philippe; Dorothée Huchon; Paulyn Cartwright
Journal:  Proc Natl Acad Sci U S A       Date:  2015-11-16       Impact factor: 11.205

9.  MAKER2: an annotation pipeline and genome-database management tool for second-generation genome projects.

Authors:  Carson Holt; Mark Yandell
Journal:  BMC Bioinformatics       Date:  2011-12-22       Impact factor: 3.307

10.  NOVOPlasty: de novo assembly of organelle genomes from whole genome data.

Authors:  Nicolas Dierckxsens; Patrick Mardulyn; Guillaume Smits
Journal:  Nucleic Acids Res       Date:  2017-02-28       Impact factor: 16.971

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  17 in total

1.  The Role of Constructive Neutral Evolution in the Development of Complexity from Symbioses: A Microbe-Centric View.

Authors:  Ramakrishnan Sitaraman
Journal:  Results Probl Cell Differ       Date:  2020

2.  Descriptions of Three New Species and New Host or Distribution Records of Five Species of the Genus Kudoa (Myxozoa: Myxosporea: Multivalvulida) in Commercial Fishes Collected from South China Sea.

Authors:  Ying-Chun Li; Ken Inoue; Jin-Yong Zhang; Hiroshi Sato
Journal:  Acta Parasitol       Date:  2022-04-16       Impact factor: 1.440

3.  New data on Henneguya postexilis Minchew, 1977, a parasite of channel catfish Ictalurus punctatus, with notes on resolution of molecular markers for myxozoan phylogeny.

Authors:  Ethan T Woodyard; Thomas G Rosser; Justin M Stilwell; Alvin C Camus; Lester H Khoo; Geoffrey Waldbieser; W Walter Lorenz; Matt J Griffin
Journal:  Syst Parasitol       Date:  2022-01-14       Impact factor: 1.431

4.  Serine protease inhibitors of the whirling disease parasite Myxobolus cerebralis (Cnidaria, Myxozoa): Expression profiling and functional predictions.

Authors:  Edit Eszterbauer; Dóra Szegő; Krisztina Ursu; Dóra Sipos; Ákos Gellért
Journal:  PLoS One       Date:  2021-03-29       Impact factor: 3.240

5.  Revisiting Ceriantharian (Anthozoa) Mitochondrial Genomes: Casting Doubts about Their Structure and Size.

Authors:  David Roy Smith
Journal:  Genome Biol Evol       Date:  2020-08-01       Impact factor: 3.416

6.  The evolution of universal adaptations of life is driven by universal properties of matter: energy, entropy, and interaction.

Authors:  Irun R Cohen; Assaf Marron
Journal:  F1000Res       Date:  2020-06-18

7.  Transcriptome-Wide Comparisons and Virulence Gene Polymorphisms of Host-Associated Genotypes of the Cnidarian Parasite Ceratonova shasta in Salmonids.

Authors:  Gema Alama-Bermejo; Eli Meyer; Stephen D Atkinson; Astrid S Holzer; Monika M Wiśniewska; Martin Kolísko; Jerri L Bartholomew
Journal:  Genome Biol Evol       Date:  2020-08-01       Impact factor: 3.416

8.  Oxygen.

Authors:  Shaun R McCann
Journal:  Bone Marrow Transplant       Date:  2020-05-02       Impact factor: 5.174

9.  Why so Complex? The Intricacy of Genome Structure and Gene Expression, Associated with Angiosperm Mitochondria, May Relate to the Regulation of Embryo Quiescence or Dormancy-Intrinsic Blocks to Early Plant Life.

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Journal:  Plants (Basel)       Date:  2020-05-08

10.  Myxosporea (Myxozoa, Cnidaria) Lack DNA Cytosine Methylation.

Authors:  Ryan Kyger; Agusto Luzuriaga-Neira; Thomas Layman; Tatiana Orli Milkewitz Sandberg; Devika Singh; Dorothée Huchon; Sateesh Peri; Stephen D Atkinson; Jerri L Bartholomew; Soojin V Yi; David Alvarez-Ponce
Journal:  Mol Biol Evol       Date:  2021-01-23       Impact factor: 16.240

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