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Recent expansion of metabolic versatility in Diplonema papillatum, the model species of a highly speciose group of marine eukaryotes

M. Valach, S. Moreira, C. Petitjean, C. Benz, A. Butenko, O. Flegontova, A. Nenarokova, G. Prokopchuk, T. Batstone, P. Lapébie, L. Lemogo, M. Sarrasin, P. Stretenowich, P. Tripathi, E. Yazaki, T. Nara, B. Henrissat, BF. Lang, MW. Gray, TA....

. 2023 ; 21 (1) : 99. [pub] 20230504

Jazyk angličtina Země Anglie, Velká Británie

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/bmc23011485

Grantová podpora
BB/R016437/1 Biotechnology and Biological Sciences Research Council - United Kingdom

BACKGROUND: Diplonemid flagellates are among the most abundant and species-rich of known marine microeukaryotes, colonizing all habitats, depths, and geographic regions of the world ocean. However, little is known about their genomes, biology, and ecological role. RESULTS: We present the first nuclear genome sequence from a diplonemid, the type species Diplonema papillatum. The ~ 280-Mb genome assembly contains about 32,000 protein-coding genes, likely co-transcribed in groups of up to 100. Gene clusters are separated by long repetitive regions that include numerous transposable elements, which also reside within introns. Analysis of gene-family evolution reveals that the last common diplonemid ancestor underwent considerable metabolic expansion. D. papillatum-specific gains of carbohydrate-degradation capability were apparently acquired via horizontal gene transfer. The predicted breakdown of polysaccharides including pectin and xylan is at odds with reports of peptides being the predominant carbon source of this organism. Secretome analysis together with feeding experiments suggest that D. papillatum is predatory, able to degrade cell walls of live microeukaryotes, macroalgae, and water plants, not only for protoplast feeding but also for metabolizing cell-wall carbohydrates as an energy source. The analysis of environmental barcode samples shows that D. papillatum is confined to temperate coastal waters, presumably acting in bioremediation of eutrophication. CONCLUSIONS: Nuclear genome information will allow systematic functional and cell-biology studies in D. papillatum. It will also serve as a reference for the highly diverse diplonemids and provide a point of comparison for studying gene complement evolution in the sister group of Kinetoplastida, including human-pathogenic taxa.

Citace poskytuje Crossref.org

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$a Valach, Matus $u Department of Biochemistry, Robert-Cedergren Centre for Bioinformatics and Genomics, Université de Montréal, Montreal, QC, Canada. matus.a.valach@gmail.com $1 https://orcid.org/0000000186890080
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$a Recent expansion of metabolic versatility in Diplonema papillatum, the model species of a highly speciose group of marine eukaryotes / $c M. Valach, S. Moreira, C. Petitjean, C. Benz, A. Butenko, O. Flegontova, A. Nenarokova, G. Prokopchuk, T. Batstone, P. Lapébie, L. Lemogo, M. Sarrasin, P. Stretenowich, P. Tripathi, E. Yazaki, T. Nara, B. Henrissat, BF. Lang, MW. Gray, TA. Williams, J. Lukeš, G. Burger
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$a BACKGROUND: Diplonemid flagellates are among the most abundant and species-rich of known marine microeukaryotes, colonizing all habitats, depths, and geographic regions of the world ocean. However, little is known about their genomes, biology, and ecological role. RESULTS: We present the first nuclear genome sequence from a diplonemid, the type species Diplonema papillatum. The ~ 280-Mb genome assembly contains about 32,000 protein-coding genes, likely co-transcribed in groups of up to 100. Gene clusters are separated by long repetitive regions that include numerous transposable elements, which also reside within introns. Analysis of gene-family evolution reveals that the last common diplonemid ancestor underwent considerable metabolic expansion. D. papillatum-specific gains of carbohydrate-degradation capability were apparently acquired via horizontal gene transfer. The predicted breakdown of polysaccharides including pectin and xylan is at odds with reports of peptides being the predominant carbon source of this organism. Secretome analysis together with feeding experiments suggest that D. papillatum is predatory, able to degrade cell walls of live microeukaryotes, macroalgae, and water plants, not only for protoplast feeding but also for metabolizing cell-wall carbohydrates as an energy source. The analysis of environmental barcode samples shows that D. papillatum is confined to temperate coastal waters, presumably acting in bioremediation of eutrophication. CONCLUSIONS: Nuclear genome information will allow systematic functional and cell-biology studies in D. papillatum. It will also serve as a reference for the highly diverse diplonemids and provide a point of comparison for studying gene complement evolution in the sister group of Kinetoplastida, including human-pathogenic taxa.
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$a Moreira, Sandrine $u Department of Biochemistry, Robert-Cedergren Centre for Bioinformatics and Genomics, Université de Montréal, Montreal, QC, Canada $1 https://orcid.org/0000000245803566
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$a Petitjean, Celine $u School of Biological Sciences, University of Bristol, Bristol, UK
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$a Flegontova, Olga $u Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic $u Faculty of Science, University of Ostrava, Ostrava, Czech Republic
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$a Prokopchuk, Galina $u Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic $u Faculty of Science, University of South Bohemia, České Budějovice, Czech Republic $1 https://orcid.org/0000000276235354
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$a Batstone, Tom $u School of Biological Sciences, University of Bristol, Bristol, UK $u Present address: High Performance Computing Centre, Bristol, UK
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$a Lapébie, Pascal $u Architecture et Fonction des Macromolécules Biologiques (AFMB), CNRS, Aix Marseille Université, Marseille, France $1 https://orcid.org/0000000340730633
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$a Lemogo, Lionnel $u Department of Biochemistry, Robert-Cedergren Centre for Bioinformatics and Genomics, Université de Montréal, Montreal, QC, Canada $u Present address: Environment Climate Change Canada, Dorval, QC, Canada $1 https://orcid.org/0009000142307671
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$a Sarrasin, Matt $u Department of Biochemistry, Robert-Cedergren Centre for Bioinformatics and Genomics, Université de Montréal, Montreal, QC, Canada $1 https://orcid.org/0000000348490849
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$a Stretenowich, Paul $u Department of Biochemistry, Robert-Cedergren Centre for Bioinformatics and Genomics, Université de Montréal, Montreal, QC, Canada $u Present address: Canadian Centre for Computational Genomics; McGill Genome Centre, McGill University, Montreal, QC, Canada $1 https://orcid.org/0000000316316512
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$a Tripathi, Pragya $u Institute of Parasitology, Biology Centre, Czech Academy of Sciences, České Budějovice, Czech Republic $u Faculty of Science, University of South Bohemia, České Budějovice, Czech Republic $1 https://orcid.org/0000000232906275
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$a Yazaki, Euki $u RIKEN Interdisciplinary Theoretical and Mathematical Sciences Program (iTHEMS), Hirosawa, Wako, Saitama, Japan $1 https://orcid.org/0000000349623340
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$a Nara, Takeshi $u Laboratory of Molecular Parasitology, Graduate School of Life Science and Technology, Iryo Sosei University, Iwaki City, Fukushima, Japan $1 https://orcid.org/0000000340519803
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$a Henrissat, Bernard $u Architecture et Fonction des Macromolécules Biologiques (AFMB), CNRS, Aix Marseille Université, Marseille, France $u Present address: DTU Bioengineering, Technical University of Denmark, Lyngby, Denmark $u Department of Biological Sciences, King Abdulaziz University, Jeddah, Saudi Arabia $1 https://orcid.org/0000000234348588
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$a Lang, B Franz $u Department of Biochemistry, Robert-Cedergren Centre for Bioinformatics and Genomics, Université de Montréal, Montreal, QC, Canada $1 https://orcid.org/0000000310355449
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