[en] Eukaryotes most often synthesize storage polysaccharides in the cytosol or vacuoles in the form of either alpha (glycogen/starch)- or beta-glucosidic (chrysolaminarins and paramylon) linked glucan polymers. In both cases, the glucose can be packed either in water-soluble (glycogen and chrysolaminarins) or solid crystalline (starch and paramylon) forms with different impacts, respectively, on the osmotic pressure, the glucose accessibility, and the amounts stored. Glycogen or starch accumulation appears universal in all free-living unikonts (metazoa, fungi, amoebozoa, etc.), as well as Archaeplastida and alveolata, while other lineages offer a more complex picture featuring both alpha- and beta-glucan accumulators. We now infer the distribution of these polymers in stramenopiles through the bioinformatic detection of their suspected metabolic pathways. Detailed phylogenetic analysis of key enzymes of these pathways correlated to the phylogeny of Stramenopila enables us to retrace the evolution of storage polysaccharide metabolism in this diverse group of organisms. The possible ancestral nature of glycogen metabolism in eukaryotes and the underlying source of its replacement by beta-glucans are discussed.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Chabi, Malika ✱; Université de Lille > CNRS - UMR8576 > UGSF - Unité de Glycobiologie Structurale et Fonctionnelle
Leleu, Marie ✱; Université de Liège - ULiège > InBioS
Fermont, Léa; Université de Lille > CNRS - UMR 8576 > UGSF - Unité de Glycobiologie Structurale et Fonctionnelle
Colpaert, Matthieu; Université de Lille > CNRS - UMR8576 > UGSF - Unité de Glycobiologie Structurale et Fonctionnelle
Colleoni, Christophe; Université de Lille > CNRS - UMR8576 > UGSF - Unité de Glycobiologie Structurale et fonctionnelle
Ball, Steven; Université de Lille > CNRS- UMR8576 > UGSF - Unité de Glycobiologie Structurale et Fonctionnelle
Cenci, Ugo ; Université de Lille > CNRS - UMR8576 > UGSF - Unité de Glycobiologie Structurale et Fonctionnelle
✱ These authors have contributed equally to this work.
Language :
English
Title :
Retracing Storage Polysaccharide Evolution in Stramenopila
Almagro Armenteros J. J., Salvatore M., Emanuelsson O., Winther O., von Heijne G., Elofsson A., et al. (2019). Detecting sequence signals in targeting peptides using deep learning. Life Sci. Alliance 2 e201900429. 10.26508/lsa.201900429 31570514
Ball S., Colleoni C., Cenci U., Raj J. N., Tirtiaux C., (2011). The evolution of glycogen and starch metabolism in eukaryotes gives molecular clues to understand the establishment of plastid endosymbiosis. J. Exp. Bot. 62 1775–1801. 10.1093/jxb/erq411 21220783
Baurain D., Brinkmann H., Petersen J., Rodriguez-Ezpeleta N., Stechmann A., Demoulin V., et al. (2010). Phylogenomic evidence for separate acquisition of plastids in cryptophytes, haptophytes, and stramenopiles. Mol. Biol. Evol. 27 1698–1709. 10.1093/molbev/msq059 20194427
Bowen S., Wheals A., (2004). Incorporation of Sed1p into the cell wall of involves. FEMS Yeast Res. 4 731–735. 10.1016/j.femsyr.2004.02.006 15093776
Burki F., Kaplan M., Tikhonenkov D. V., Zlatogursky V., Minh B. Q., Radaykina L. V., et al. (2016). Untangling the early diversification of eukaryotes: a phylogenomic study of the evolutionary origins of Centrohelida, Haptophyta and Cryptista. Proc. R. Soc. B Biol. Sci. 283 20152802. 10.1098/rspb.2015.2802 26817772
Cavalier-Smith T., (1999). Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J. Eukaryot. Microbiol. 46 347–366. 10.1111/j.1550-7408.1999.tb04614.x 18092388
Cenci U., Moog D., Curtis B. A., Tanifuji G., Eme L., Lukeš J., et al. (2016). Heme pathway evolution in kinetoplastid protists. BMC Evol. Biol. 16:109. 10.1186/s12862-016-0664-6 27193376
Cenci U., Nitschke F., Steup M., Minassian B. A., Colleoni C., Ball S. G., (2014). Transition from glycogen to starch metabolism in Archaeplastida. Trends Plant Sci. 19 18–28. 10.1016/j.tplants.2013.08.004 24035236
Cenci U., Qiu H., Pillonel T., Cardol P., Remacle C., Colleoni C., et al. (2018a). Host-pathogen biotic interactions shaped vitamin K metabolism in Archaeplastida. Sci. Rep. 8:15243. 10.1038/s41598-018-33663-w 30323231
Cenci U., Sibbald S. J., Curtis B. A., Kamikawa R., Eme L., Moog D., et al. (2018b). Nuclear genome sequence of the plastid-lacking cryptomonad Goniomonas avonlea provides insights into the evolution of secondary plastids. BMC Biol. 16:137. 10.1186/s12915-018-0593-5 30482201
Corteggiani Carpinelli E., Telatin A., Vitulo N., Forcato C., D’Angelo M., Schiavon R., et al. (2014). Chromosome scale genome assembly and transcriptome profiling of nannochloropsis gaditana in nitrogen depletion. Mol. Plant 7 323–335. 10.1093/mp/sst120 23966634
Criscuolo A., Gribaldo S., (2010). BMGE (Block Mapping and Gathering with Entropy): a new software for selection of phylogenetic informative regions from multiple sequence alignments. BMC Evol. Biol. 10:210. 10.1186/1471-2148-10-210 20626897
Derelle R., López-García P., Timpano H., Moreira D., (2016). A phylogenomic framework to study the diversity and evolution of stramenopiles (= Heterokonts). Mol. Biol. Evol. 33 2890–2898. 10.1093/molbev/msw168 27512113
Dinadayala P., Sambou T., Daffe M., Lemassu A., (2008). Comparative structural analyses of the -glucan and glycogen from Mycobacterium bovis. Glycobiology 18 502–508. 10.1093/glycob/cwn031 18436565
Edgar R. C., (2004). MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32 1792–1797. 10.1093/nar/gkh340 15034147
Eme L., Gentekaki E., Curtis B., Archibald J. M., Roger A. J., (2017). Lateral gene transfer in the adaptation of the anaerobic parasite blastocystis to the gut. Curr. Biol. 27 807–820. 10.1016/j.cub.2017.02.003 28262486
Field C. B., (1998). Primary production of the biosphere: integrating terrestrial and oceanic components. Science 281 237–240. 10.1126/science.281.5374.237 9657713
Gentekaki E., Curtis B. A., Stairs C. W., Klimeš V., Eliáš M., Salas-Leiva D. E., et al. (2017). Extreme genome diversity in the hyper-prevalent parasitic eukaryote Blastocystis. PLoS Biol. 15:e2003769. 10.1371/journal.pbio.2003769 28892507
Graiff A., Ruth W., Kragl U., Karsten U., (2016). Chemical characterization and quantification of the brown algal storage compound laminarin — a new methodological approach. J. Appl. Phycol. 28 533–543. 10.1007/s10811-015-0563-z
Gruber A., Kroth P. G., (2017). Intracellular metabolic pathway distribution in diatoms and tools for genome-enabled experimental diatom research. Philos. Trans. R. Soc. Lond. B Biol. Sci. 372:20160402. 10.1098/rstb.2016.0402 28717012
Harding T., Brown M. W., Simpson A. G. B., Roger A. J., (2016). Osmoadaptative strategy and its molecular signature in obligately halophilic heterotrophic protists. Genome Biol. Evol. 8 2241–2258. 10.1093/gbe/evw152 27412608
Huang W., Haferkamp I., Lepetit B., Molchanova M., Hou S., Jeblick W., et al. (2018). Reduced vacuolar β-1,3-glucan synthesis affects carbohydrate metabolism as well as plastid homeostasis and structure in Phaeodactylum tricornutum. Proc. Natl. Acad. Sci. U.S.A. 115 4791–4796. 10.1073/pnas.1719274115 29669920
Huang W., Río Bártulos C., Kroth P. G., (2016). Diatom vacuolar 1,6-β-Transglycosylases can functionally complement the respective yeast mutants. J. Eukaryot. Microbiol. 63 536–546. 10.1111/jeu.12298 26785404
Kadam S. U., Tiwari B. K., O’Donnell C. P., (2015). Extraction, structure and biofunctional activities of laminarin from brown algae. Int. J. Food Sci. Technol. 50 24–31. 10.1111/ijfs.12692
Katoh K., Standley D. M., (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30 772–780. 10.1093/molbev/mst010 23329690
Keeling P., Burki F., Wilcox J., Allam B., (2014). The Marine Microbial Eukaryote Transcriptome Sequencing Project (MMETSP): illuminating the functional diversity of eukaryotic life in the oceans through transcriptome sequencing. PLoS Biol. 12:e1001889. 10.1371/journal.pbio.1001889 24959919
Kitaoka M., Matsuoka Y., Mori K., Nishimoto M., Hayashi K., (2012). Characterization of a bacterial laminaribiose phosphorylase. Biosci. Biotechnol. Biochem. 76 343–348. 10.1271/bbb.110772 22313784
Krogh A., Larsson B., von Heijne G., Sonnhammer E. L. L., (2001). Predicting transmembrane protein topology with a hidden markov model: application to complete genomes. J. Mol. Biol. 305 567–580. 10.1006/jmbi.2000.4315 11152613
Kroth P. G., Chiovitti A., Gruber A., Martin-Jezequel V., Mock T., Parker M. S., et al. (2008). A model for carbohydrate metabolism in the diatom phaeodactylum tricornutum deduced from comparative whole genome analysis. PLoS One 3:e1426. 10.1371/journal.pone.0001426 18183306
Kuhaudomlarp S., Patron N. J., Henrissat B., Rejzek M., Saalbach G., Field R. A., (2018). Identification of Euglena gracilis β-1,3-glucan phosphorylase and establishment of a new glycoside hydrolase (GH) family GH149. J. Biol. Chem. 293 2865–2876. 10.1074/jbc.RA117.000936 29317507
Kuhaudomlarp S., Pergolizzi G., Patron N. J., Henrissat B., Field R. A., (2019). Unraveling the subtleties of β-(1→3)-glucan phosphorylase specificity in the GH94, GH149 and GH161 glycoside hydrolase families. J. Biol. Chem. 294 6483–6493. 10.1074/jbc.RA119.007712 30819804
Lee Chang K. J., Dunstan G. A., Abell G. C. J., Clementson L. A., Blackburn S. I., Nichols P. D., et al. (2012). Biodiscovery of new Australian thraustochytrids for production of biodiesel and long-chain omega-3 oils. Appl. Microbiol. Biotechnol. 93 2215–2231. 10.1007/s00253-011-3856-4 22252264
Lombard V., Golaconda Ramulu H., Drula E., Coutinho P. M., Henrissat B., (2014). The carbohydrate-active enzymes database (CAZy) in 2013. Nucleic Acids Res. 42 D490–D495. 10.1093/nar/gkt1178 24270786
Maruyama S., Eveleigh R. J., Archibald J. M., (2013). Treetrimmer: a method for phylogenetic dataset size reduction. BMC Res. Notes 6:145. 10.1186/1756-0500-6-145 23587045
Michel G., Tonon T., Scornet D., Cock J. M., Kloareg B., (2010). The cell wall polysaccharide metabolism of the brown alga Ectocarpus siliculosus. Insights into the evolution of extracellular matrix polysaccharides in Eukaryotes. New Phytol. 188 82–97. 10.1111/j.1469-8137.2010.03374.x 20618907
Mistry J., Finn R. D., Eddy S. R., Bateman A., Punta M., (2013). Challenges in homology search: HMMER3 and convergent evolution of coiled-coil regions. Nucleic Acids Res. 41:e121. 10.1093/nar/gkt263 23598997
Moreira D., López-García P., (2017). Protist evolution: stealing genes to gut it out. Curr. Biol. 27 R223–R225. 10.1016/j.cub.2017.02.010 28324738
Mouille G., Maddelein M.-L., Libessart N., Talaga P., Decq A., Delrue B., et al. (1996). Preamylopectin processing: a mandatory step for starch biosynthesis in plants. Plant Cell 8 1353–1366. 10.2307/3870306
Nishikawa S., Zinkl G. M., Swanson R. J., Maruyama D., Preuss D., (2005). Callose (beta-1,3 glucan) is essential for Arabidopsis pollen wall patterning, but not tube growth. BMC Plant Biol. 5:22. 10.1186/1471-2229-5-22 16212660
O’Neill E. C., Trick M., Hill L., Rejzek M., Dusi R. G., Hamilton C. J., et al. (2015). The transcriptome of Euglena gracilis reveals unexpected metabolic capabilities for carbohydrate and natural product biochemistry. Mol. BioSyst. 11 2808–2820. 10.1039/C5MB00319A 26289754
Petsalaki E. I., Bagos P. G., Litou Z. L., Hamodrakas S. J., (2006). PredSL: A Tool for the N-terminal Sequence-based Prediction Protein Subcellular Localization. Genom. Proteom. Bioinform. 4 48–55. 10.1016/S1672-0229(06)60016-8
Price M. N., Dehal P. S., Arkin A. P., (2010). FastTree 2–approximately maximum-likelihood trees for large alignments. PLoS One 5:e9490. 10.1371/journal.pone.0009490 20224823
Stiller J. W., Schreiber J., Yue J., Guo H., Ding Q., Huang J., (2014). The evolution of photosynthesis in chromist algae through serial endosymbioses. Nat. Commun. 5:5764. 10.1038/ncomms6764 25493338
Sullivan M. A., O’Connor M. J., Umana F., Roura E., Jack K., Stapleton D. I., et al. (2012). Molecular insights into glycogen α-particle formation. Biomacromolecules 13 3805–3813. 10.1021/bm3012727 23004915
Teste M. A., Enjalbert B., Parrou J. L., François J. M., (2000). The Saccharomyces cerevisiae YPR184w gene encodes the glycogen debranching enzyme. FEMS Microbiol. Lett. 193 105–110. 10.1111/j.1574-6968.2000.tb09410.x 11094287
Viborg A. H., Terrapon N., Lombard V., Michel G., Czjzek M., Henrissat B., et al. (2019). A subfamily roadmap of the evolutionarily diverse glycoside hydrolase family 16 (GH16). J. Biol. Chem. 294 15973–15986. 10.1074/jbc.RA119.010619 31501245
Vlierberghe M. V., Léonard R. R., Cornet L., Bouzin Y., Baurain D., (2021). Curated sequence database “Life-OF-Mick” first used in Cornet, Magain et al. Exploring syntenic conservation across genomes for phylogenetic studies of organisms subjected to horizontal gene transfers: a case study with Cyanobacteria. 10.6084/M9.FIGSHARE.13550267.V2
Wilson W. A., Roach P. J., Montero M., Baroja-Fernández E., Muñoz F. J., Eydallin G., et al. (2010). Regulation of glycogen metabolism in yeast and bacteria. FEMS Microbiol. Rev. 34 952–985. 10.1111/j.1574-6976.2010.00220.x 20412306
Yin Y., Mao X., Yang J., Chen X., Mao F., Xu Y., (2012). dbCAN: a web resource for automated carbohydrate-active enzyme annotation. Nucleic Acids Res. 40 W445–W451. 10.1093/nar/gks479 22645317
Yoshimi A., Miyazawa K., Abe K., (2017). Function and biosynthesis of cell wall α-1,3-Glucan in fungi. J. Fungi 3:63. 10.3390/jof3040063 29371579
