Mobilization of a diatom mutator-like element (MULE) transposon inactivates the uridine monophosphate synthase (UMPS) locus in Phaeodactylum tricornutum.
Phaeodactylum tricornutum
diatom
genome editing
genome stability
selectable marker
transposable element
Journal
The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397
Informations de publication
Date de publication:
08 2023
08 2023
Historique:
revised:
18
04
2023
received:
03
01
2023
accepted:
29
04
2023
medline:
24
8
2023
pubmed:
6
5
2023
entrez:
6
5
2023
Statut:
ppublish
Résumé
Diatoms are photosynthetic unicellular microalgae that drive global ecological phenomena in the biosphere and are emerging as sustainable feedstock for an increasing number of industrial applications. Diatoms exhibit enormous taxonomic and genetic diversity, which often results in peculiar biochemical and biological traits. Transposable elements (TEs) represent a substantial portion of diatom genomes and have been hypothesized to exert a relevant role in enriching genetic diversity and making a core contribution to genome evolution. Here, through long-read whole-genome sequencing, we identified a mutator-like element (MULE) in the model diatom Phaeodactylum tricornutum, and we report the direct observation of its mobilization within the course of a single laboratory experiment. Under selective conditions, this TE inactivated the uridine monophosphate synthase (UMPS) gene of P. tricornutum, one of the few endogenous genetic loci currently targeted for selectable auxotrophy for functional genetics and genome-editing applications. We report the observation of a recently mobilized transposon in diatoms with unique features. These include the combined presence of a MULE transposase with zinc-finger SWIM-type domains and a diatom-specific E3 ubiquitin ligase of the zinc-finger UBR type, which are suggestive of a mobilization mechanism. Our findings provide new elements for the understanding of the role of TEs in diatom genome evolution and in the enrichment of intraspecific genetic variability.
Substances chimiques
Uridine Monophosphate
E2OU15WN0N
Zinc
J41CSQ7QDS
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
926-936Informations de copyright
© 2023 The Authors. The Plant Journal published by Society for Experimental Biology and John Wiley & Sons Ltd.
Références
Armbrust, E.V. (2009) The life of diatoms in the world's oceans. Nature, 459, 185-192.
Backhaus, K., Ludwig-Radtke, L., Xie, X. & Li, S.M. (2017) Manipulation of the precursor supply in yeast significantly enhances the accumulation of prenylated β-Carbolines. ACS Synthetic Biology, 6, 1056-1064.
Berges, J.A., Franklin, D.J. & Harrison, P.J. (2001) Evolution of an artificial seawater medium: improvements in enriched seawater, artificial water over the last two decades. Journal of Phycology, 37, 1138-1145.
Bourque, G., Burns, K.H., Gehring, M., Gorbunova, V., Seluanov, A., Hammell, M. et al. (2018) Ten things you should know about transposable elements. Genome Biology, 19, 199.
Bowler, C., Allen, A.E., Badger, J.H., Grimwood, J., Jabbari, K., Kuo, A. et al. (2008) The Phaeodactylum genome reveals the evolutionary history of diatom genomes. Nature, 456, 239-244.
Brandsen, B.M., Mattheisen, J.M., Noel, T. & Fields, S. (2018) A biosensor strategy for E. coli based on ligand-dependent stabilization. ACS Synthetic Biology, 7, 1990-1999.
Bulankova, P., Sekulić, M., Jallet, D., Nef, C., van Oosterhout, C., Delmont, T.O. et al. (2021) Mitotic recombination between homologous chromosomes drives genomic diversity in diatoms. Current Biology, 31, 3221-3232.e9.
Butler, T., Kapoore, R.V. & Vaidyanathan, S. (2020) Phaeodactylum tricornutum: a diatom cell factory. Trends in Biotechnology, 38, 606-622.
D'Adamo, S., Schiano di Visconte, G., Lowe, G., Szaub-Newton, J., Beacham, T., Landels, A. et al. (2018) Engineering the unicellular alga Phaeodactylum tricornutum for high-value plant triterpenoid production. Plant Biotechnology Journal, 17, 75-87.
Dobin, A., Davis, C.A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S. et al. (2013) STAR: ultrafast universal RNA-seq aligner. Bioinformatics, 29, 15-21.
Dupeyron, M., Singh, K.S., Bass, C. & Hayward, A. (2019) Evolution of mutator transposable elements across eukaryotic diversity. Mobile DNA, 10, 12.
Edgar, R.C. (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792-1797.
Fabris, M., Abbriano, R.M., Pernice, M., Sutherland, D.L., Commault, A.S., Hall, C.C. et al. (2020) Emerging technologies in algal biotechnology: toward the establishment of a sustainable, algae-based bioeconomy. Frontiers in Plant Science, 11, 279.
Fabris, M., George, J., Kuzhiumparambil, U., Lawson, C.A., Jaramillo Madrid, A.C., Abbriano, R.M. et al. (2020) Extrachromosomal genetic engineering of the marine diatom Phaeodactylum tricornutum enables the heterologous production of monoterpenoids. ACS Synthetic Biology, 9, 598-612.
Filloramo, G.V., Curtis, B.A., Blanche, E. & Archibald, J.M. (2021) Re-examination of two diatom reference genomes using long-read sequencing. BMC Genomics, 22, 379.
George, J., Kahlke, T., Abbriano, R.M., Kuzhiumparambil, U., Ralph, P.J. & Fabris, M. (2020) Metabolic engineering strategies in diatoms reveal unique phenotypes and genetic configurations with implications for algal genetics and synthetic biology. Frontiers in Bioengineering and Biotechnology, 8, 513.
Hanada, K., Vallejo, V., Nobuta, K., Slotkin, R.K., Lisch, D., Meyers, B.C. et al. (2009) The functional role of pack-MULEs in rice inferred from purifying selection and expression profile. The Plant Cell, 21, 25-38.
Hao, H., Wang, X., Jia, H., Yu, M., Zhang, X., Tang, H. et al. (2016) Large fragment deletion using a CRISPR/Cas9 system in Saccharomyces cerevisiae. Analytical Biochemistry, 509, 118-123.
Hempel, F., Bozarth, A.S., Lindenkamp, N., Klingl, A., Zauner, S., Linne, U. et al. (2011) Microalgae as bioreactors for bioplastic production. Microbial Cell Factories, 10, 81.
Hempel, F., Lau, J., Klingl, A. & Maier, U.G. (2011) Algae as protein factories: expression of a human antibody and the respective antigen in the diatom Phaeodactylum tricornutum. PLoS One, 6, e28424.
Huerta-Cepas, J., Szklarczyk, D., Heller, D., Hernández-Plaza, A., Forslund, S.K., Cook, H. et al. (2019) eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Research, 47, D309-D314.
Ishii, Y., Maruyama, S., Fujimura-Kamada, K., Kutsuna, N., Takahashi, S., Kawata, M. et al. (2018) Isolation of uracil auxotroph mutants of coral symbiont alga for symbiosis studies. Scientific Reports, 8, 3237.
Jones, P., Binns, D., Chang, H.-Y., Fraser, M., Li, W., McAnulla, C. et al. (2014) InterProScan 5: genome-scale protein function classification. Bioinformatics, 30, 1236-1240.
Kabelitz, T., Brzezinka, K., Friedrich, T., Górka, M., Graf, A., Kappel, C. et al. (2016) A JUMONJI protein with E3 ligase and histone H3 binding activities affects transposon silencing in Arabidopsis. Plant Physiology, 171, 344-358.
Klein, J., Heal, J.R., Hamilton, W.D.O., Boussemghoune, T., Tange, T.Ø., Delegrange, F. et al. (2014) Yeast synthetic biology platform generates novel chemical structures as scaffolds for drug discovery. ACS Synthetic Biology, 3, 314-323.
Kolmogorov, M., Yuan, J., Lin, Y. & Pevzner, P.A. (2019) Assembly of long, error-prone reads using repeat graphs. Nature Biotechnology, 37, 540-546.
Kondo, T., Johnson, C.H. & Hastings, J.W. (1991) Action spectrum for resetting the circadian phototaxis rhythm in the CW15 strain of Chlamydomonas: I. Cells in darkness. Plant Physiology, 95, 197-205.
Larsson, A. (2014) AliView: a fast and lightweight alignment viewer and editor for large datasets. Bioinformatics, 30, 3276-3278.
Li, H. (2018) Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics, 34, 3094-3100.
Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N. et al. (2009). The sequence alignment/map format and SAMtools. Bioinformatics, 25, 2078-2079.
Lv, Y., Edwards, H., Zhou, J. & Xu, P. (2019) Combining 26s rDNA and the Cre-loxP system for iterative gene integration and efficient marker curation in Yarrowia lipolytica. ACS Synthetic Biology, 8, 568-576.
Maclennan, M., García-Cañadas, M., Reichmann, J., Khazina, E., Wagner, G., Playfoot, C.J. et al. (2017) Mobilization of LINE-1 retrotransposons is restricted by Tex19.1 in mouse embryonic stem cells. eLife, 6, e26152.
Maumus, F., Allen, A.E., Mhiri, C., Hu, H., Jabbari, K., Vardi, A. et al. (2009) Potential impact of stress activated retrotransposons on genome evolution in a marine diatom. BMC Genomics, 10, 624.
Minoda, A., Sakagami, R., Yagisawa, F., Kuroiwa, T. & Tanaka, K. (2004) Improvement of culture conditions and evidence for nuclear transformation by homologous recombination in a red alga, Cyanidioschyzon merolae 10D. Plant and Cell Physiology, 45, 667-671.
Negi, P., Rai, A.N. & Suprasanna, P. (2016) Moving through the stressed genome: emerging regulatory roles for transposons in plant stress response. Frontiers in Plant Science, 7, 1448.
Pampuch, M., Walker, E.J.L. & Karas, B.J. (2022) Towards synthetic diatoms: the Phaeodactylum tricornutum Pt-syn 1.0 project. Current Opinion in Green and Sustainable Chemistry, 35, 100611.
Rastogi, A., Maheswari, U., Dorrell, R.G., Vieira, F.R.J., Maumus, F., Kustka, A. et al. (2018) Integrative analysis of large scale transcriptome data draws a comprehensive landscape of Phaeodactylum tricornutum genome and evolutionary origin of diatoms. Scientific Reports, 8(1), 4834.
Robinson, J.T., Thorvaldsdóttir, H., Winckler, W., Guttman, M., Lander, E.S., Getz, G. et al. (2011) Integrative genomics viewer. Nature Biotechnology, 29, 24-26.
Sakaguchi, T., Nakajima, K. & Matsuda, Y. (2011) Identification of the UMP synthase gene by establishment of uracil auxotrophic mutants and the phenotypic complementation system in the marine diatom Phaeodactylum tricornutum. Plant Physiology, 156, 78-89.
Scott, L.H., Mathews, J.C., Flematti, G.R., Filipovska, A. & Rackham, O. (2018) An artificial yeast genetic circuit enables deep mutational scanning of an antimicrobial resistance protein. ACS Synthetic Biology, 7, 1907-1917.
Sedlazeck, F.J., Rescheneder, P., Smolka, M., Fang, H., Nattestad, M., von Haeseler, A. et al. (2018) Accurate detection of complex structural variations using single-molecule sequencing. Nature Methods, 15, 461-468.
Serif, M., Dubois, G., Finoux, A.-L., Teste, M.-A., Jallet, D. & Daboussi, F. (2018) One-step generation of multiple gene knock-outs in the diatom Phaeodactylum tricornutum by DNA-free genome editing. Nature Communications, 9, 3924.
Slattery, S.S., Giguere, D.J., Stuckless, E.E., Shrestha, A., Briere, L.A.K., Galbraith, A. et al. (2022) Phosphate-regulated expression of the SARS-CoV-2 receptor-binding domain in the diatom Phaeodactylum tricornutum for pandemic diagnostics. Scientific Reports, 12, 7010.
Slattery, S.S., Wang, H., Giguere, D.J., Kocsis, C., Urguhart, B.L., Karas, B. et al. (2020) Plasmid-based complementation of large deletion in Phaeodactylum tricornutum biosynthetic genes generated by Cas9 editing. Scientific Reports, 10, 13879.
Standage-Beier, K., Zhang, Q. & Wang, X. (2015) Targeted large-scale deletion of bacterial genomes using CRISPR-nickases. ACS Synthetic Biology, 4, 1217-1225.
Sun, L., Jing, Y., Liu, X., Li, Q., Xue, Z., Cheng, Z. et al. (2020) Heat stress-induced transposon activation correlates with 3D chromatin organization rearrangement in Arabidopsis. Nature Communications, 11, 1886.
Vancaester, E., Depuydt, T., Osuna-cruz, C.M. & Vandepoele, K. (2020) Systematic and functional analysis of horizontal gene transfer events in diatoms. Molecular Biology and Evolution, 37, 3243-3257.
Vandepoele, K., Van Bel, M., Richard, G., Van Landeghem, S., Verhelst, B., Moreau, H. et al. (2013) Pico-PLAZA, a genome database of microbial photosynthetic eukaryotes. Environmental Microbiology, 15, 2147-2153.
Vaser, R., Sović, I., Nagarajan, N. & Šikić, M. (2017) Fast and accurate de novo genome assembly from long uncorrected reads. Genome Research, 27, 737-746.
Wang, Y.K., Das, B., Huber, D.H., Wellington, M., Kabir, M.A., Sherman, F. et al. (2004) Role of the 14-3-3 protein in carbon metabolism of the pathogenic yeast Candida albicans. Yeast, 21, 685-702.
Wellington, M., Kabir, M.A. & Rustchenko, E. (2006) 5-Fluoro-orotic acid induces chromosome alterations in genetically manipulated strains of Candida albicans. Mycologia, 98, 393-398.
Wellington, M. & Rustchenko, E. (2005) 5-Fluoro-orotic acid induces chromosome alterations in Candida albicans. Yeast, 22, 57-70.
Wicker, T., Sabot, F., Hua-van, A., Bennetzen, J.L., Capy, P., Chalhoub, B. et al. (2008) A universal classification of eukaryotic transposable elements implemented in Repbase. Nature Reviews. Genetics, 9, 414. https://doi.org/10.1038/nrg2165-c2
Windhagauer, M., Abbriano, R.M., Pittrich, D.A. & Doblin, M.A. (2022) Phosphate-inducible poly-hydroxy butyrate production dynamics in CO2-supplemented upscaled cultivation of engineered Phaeodactylum tricornutum. Journal of Applied Phycology, 34, 2259-2270.