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Evolution and phylogenetic distribution of endo -α-mannosidase
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Abstract
While glycans underlie many biological processes, such as protein folding, cell adhesion, and cell–cell recognition, deep evolution of glycosylation machinery remains an understudied topic. N-linked glycosylation is a conserved process in which mannosidases are key trimming enzymes. One of them is the glycoprotein endo-α-1,2-mannosidase which participates in the initial trimming of mannose moieties from an N-linked glycan inside the cis-Golgi. It is unique as the only endo-acting mannosidase found in this organelle. Relatively little is known about its origins and evolutionary history; so far it was reported to occur only in vertebrates. In this work, a taxon-rich bioinformatic survey to unravel the evolutionary history of this enzyme, including all major eukaryotic clades and a wide representation of animals, is presented. The endomannosidase was found to be more widely distributed in animals and other eukaryotes. The protein motif changes in context of the canonical animal enzyme were tracked. Additionally, the data show the two canonical vertebrate endomannosidase genes, MANEA and MANEAL, arose at the second round of the two vertebrate genome duplications and one more vertebrate paralog, CMANEAL, is uncovered. Finally, a framework where N-glycosylation co-evolved with complex multicellularity is described. A better understanding of the evolution of core glycosylation pathways is pivotal to understanding biology of eukaryotes in general, and the Golgi apparatus in particular. This systematic analysis of the endomannosidase evolution is one step toward this goal.
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Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., et al. (2021) · Nature · doi:10.1038/s41586-021-03819-2 · Cited by 43,764
Varki, A. (2017) · Glycobiology · doi:10.1093/glycob/cww086 · Cited by 2,635 · cited 2×
“The specific claims refuted by this analysis are: (1) that endomannosidase is a recent addition to the eukaryotic Nglycan processing machinery, (2) that it is limited in distribution to chordates with the exception of molluscs.”
BackgroundMethodCarlin, A. F., Uchiyama, S., Chang, Y.-C., Lewis, A. L., Nizet, V., & Varki, A. (2009) · Blood · doi:10.1182/blood-2008-11-187302 · Cited by 401
Saunier, B., Kilker, R. D., Tkacz, J. S., Quaroni, A., & Herscovics, A. (1982) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)45358-1 · Cited by 283
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Flagged first, then by citations
Research works printed but not linked: 82
- Amores, 1998, Zebrafish hox clusters and vertebrate genome evolution, Science, 282, 1711, 10.1126/science.282.5394.1711 · DOI
- Bachali, 2002, Phylogenetic analysis of invertebrate lysozymes and the evolution of lysozyme function, J Mol Evol, 54, 652, 10.1007/s00239-001-0061-6 · DOI
- Baïet, 2011, N-Glycans of Phaeodactylum tricornutum diatom and functional characterization of its N-Acetylglucosaminyltransferase I enzyme*, J Biol Chem, 286, 6152, 10.1074/jbc.M110.175711 · DOI
- Banerjee, 2007, The evolution of N-glycan-dependent endoplasmic reticulum quality control factors for glycoprotein folding and degradation, Proc Natl Acad Sci, 104, 11676, 10.1073/pnas.0704862104 · DOI
- Betancur-R, 2017, Phylogenetic classification of bony fishes, BMC Evol Biol, 17, 162, 10.1186/s12862-017-0958-3 · DOI · Paper page
- Brown, 2018, Phylogenomics places orphan protistan lineages in a novel eukaryotic super-group, Genome Biol Evol, 10, 427, 10.1093/gbe/evy014 · DOI
- Burchill, 2023, Structure, function and mechanism of N-glycan processing enzymes: endo-α-1,2-Mannanase and endo-α-1,2-mannosidase, Isr J Chem, 63, e202200067, 10.1002/ijch.202200067 · DOI
- Camacho, 2009, BLAST+: architecture and applications, BMC Bioinformatics, 10, 421, 10.1186/1471-2105-10-421 · DOI · Paper page
- Campo, 2014, The others: our biased perspective of eukaryotic genomes, Trends Ecol Evol, 29, 252, 10.1016/j.tree.2014.03.006 · DOI
- Capella-Gutierrez, 2009, trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses, Bioinformatics, 25, 1972, 10.1093/bioinformatics/btp348 · DOI
- Cavalier-Smith, 2013, Early evolution of eukaryote feeding modes, cell structural diversity, and classification of the protozoan phyla Loukozoa, Sulcozoa, and Choanozoa, Eur J Protistol, 49, 115, 10.1016/j.ejop.2012.06.001 · DOI
- Chen, 2018, Rhodopsin gene evolution in early teleost fishes, PLoS One, 13, e0206918, 10.1371/journal.pone.0206918 · DOI
- Costa, 2020, Cultivation-independent and cultivation-dependent metagenomes reveal genetic and enzymatic potential of microbial community involved in the degradation of a complex microbial polymer, Microbiome, 8, 76, 10.1186/s40168-020-00836-7 · DOI
- Cuskin, 2015, Human gut Bacteroidetes can utilize yeast mannan through a selfish mechanism, Nature, 517, 165, 10.1038/nature13995 · DOI
- Dairaku, 1997, Phylogenetic survey of endomannosidase indicates late evolutionary appearance of this N-linked oligosaccharide processing enzyme, Glycobiology, 7, 579, 10.1093/glycob/7.4.579 · DOI
- Davies, 1997, Nomenclature for sugar-binding subsites in glycosyl hydrolases, Biochem J, 321, 557, 10.1042/bj3210557 · DOI
- Dehal, 2005, Two rounds of whole genome duplication in the ancestral vertebrate, PLoS Biol, 3, e314, 10.1371/journal.pbio.0030314 · DOI · Paper page
- Deorowicz, 2016, FAMSA: fast and accurate multiple sequence alignment of huge protein families, Sci Rep, 6, 33964, 10.1038/srep33964 · DOI
- Drula, 2022, The carbohydrate-active enzyme database: functions and literature, Nucleic Acids Res, 50, D571, 10.1093/nar/gkab1045 · DOI · Paper page
- Edgar, 2004, MUSCLE: multiple sequence alignment with high accuracy and high throughput, Nucleic Acids Res, 32, 1792, 10.1093/nar/gkh340 · DOI · Paper page
- Fu, 2012, CD-HIT: accelerated for clustering the next-generation sequencing data, Bioinformatics, 28, 3150, 10.1093/bioinformatics/bts565 · DOI · Paper page
- Grün, 2006, Mechanism of action of the endo-(1 → 3)-α-glucanase MutAp from the mycoparasitic fungus Trichoderma harzianum, FEBS Lett, 580, 3780, 10.1016/j.febslet.2006.05.062 · DOI
- GTEx Consortium, Laboratory, Data Analysis & Coordinating Center (LDACC), NIH program management, Biospecimen collection, Pathology, eQTL Manuscript Working Group, 2017, Genetic effects on gene expression across human tissues, Nature, 550, 204, 10.1038/nature24277 · DOI · Paper page
- Hakki, 2015, Structural and kinetic dissection of the endo-α-1,2-Mannanase activity of bacterial GH99 glycoside hydrolases from Bacteroides spp, Chem Eur J, 21, 1966, 10.1002/chem.201405539 · DOI
- Hehenberger, 2017, Novel predators reshape holozoan phylogeny and reveal the presence of a two-component signaling system in the ancestor of animals, Curr Biol, 27, 2043, 10.1016/j.cub.2017.06.006 · DOI
- Hoang, 2018, UFBoot2: improving the ultrafast bootstrap approximation, Mol Biol Evol, 35, 518, 10.1093/molbev/msx281 · DOI · Paper page
- Hughes, 2018, Comprehensive phylogeny of ray-finned fishes (Actinopterygii) based on transcriptomic and genomic data, Proc Natl Acad Sci, 115, 6249, 10.1073/pnas.1719358115 · DOI · Paper page
- Huo, 2017, pHMM-tree: phylogeny of profile hidden Markov models, Bioinforma Oxf Engl, 33, 1093, 10.1093/bioinformatics/btw779 · DOI
- Huson, 2012, Dendroscope 3: an interactive tool for rooted phylogenetic trees and networks, Syst Biol, 61, 1061, 10.1093/sysbio/sys062 · DOI
- International Union of Biochemistry and Molecular Biology Nomenclature Committee, 1992, Enzyme nomenclature 1992: recommendations of the nomenclature Committee of the International Union of biochemistry and molecular biology on the nomenclature and classification of enzymes
- Iwamoto, 2017, Endo-α-mannosidase-catalyzed Transglycosylation, Chembiochem, 18, 1376, 10.1002/cbic.201700111 · DOI
- Jaillon, 2004, Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype, Nature, 431, 946, 10.1038/nature03025 · DOI · Paper page
- Kalyaanamoorthy, 2017, ModelFinder: fast model selection for accurate phylogenetic estimates, Nat Methods, 14, 587, 10.1038/nmeth.4285 · DOI · Paper page
- Katoh, 2013, MAFFT multiple sequence alignment software version 7: improvements in performance and usability, Mol Biol Evol, 30, 772, 10.1093/molbev/mst010 · DOI · Paper page
- Kelleher, 2006, An evolving view of the eukaryotic oligosaccharyltransferase, Glycobiology, 16, 47R, 10.1093/glycob/cwj066 · DOI
- Kryuchkova-Mostacci, 2016, Tissue-specificity of gene expression diverges slowly between Orthologs, and rapidly between paralogs, PLoS Comput Biol, 12, e1005274, 10.1371/journal.pcbi.1005274 · DOI
- Kukushkin, 2012, Restricted processing of glycans by endomannosidase in mammalian cells, Glycobiology, 22, 1282, 10.1093/glycob/cws088 · DOI
- Li, 2006, Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences, Bioinformatics, 22, 1658, 10.1093/bioinformatics/btl158 · DOI
- Lin, 2020, Basal teleosts provide new insights into the evolutionary history of teleost-duplicated aromatase, Gen Comp Endocrinol, 291, 113395, 10.1016/j.ygcen.2020.113395 · DOI
- Lubas, 1987, Golgi endo-alpha-D-mannosidase from rat liver, a novel N-linked carbohydrate unit processing enzyme, J Biol Chem, 262, 3775, 10.1016/S0021-9258(18)61422-X · DOI
- Marron, 2016, The evolution of silicon transport in eukaryotes, Mol Biol Evol, 33, 3226, 10.1093/molbev/msw209 · DOI
- Matsuda, 2011, Heterologous expression, purification, and characterization of an α-mannosidase belonging to glycoside hydrolase family 99 of Shewanella amazonensis, Biosci Biotechnol Biochem, 75, 797, 10.1271/bbb.100874 · DOI
- McNicholas, 2011, Presenting your structures: the CCP4mg molecular-graphics software, Acta Crystallogr Biol Crystallogr, 67, 386, 10.1107/S0907444911007281 · DOI
- Minh, 2020, IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era, Mol Biol Evol, 37, 1530, 10.1093/molbev/msaa015 · DOI · Paper page
- Nakatani, 2021, Reconstruction of proto-vertebrate, proto-cyclostome and proto-gnathostome genomes provides new insights into early vertebrate evolution, Nat Commun, 12, 4489, 10.1038/s41467-021-24573-z · DOI · Paper page
- NCBI Resource Coordinators, 2017, Database resources of the National Center for biotechnology information, Nucleic Acids Res, 45, D12, 10.1093/nar/gkw1071 · DOI · Paper page
- Neelamegham, 2019, Updates to the symbol nomenclature for Glycans guidelines, Glycobiology, 29, 620, 10.1093/glycob/cwz045 · DOI
- Nikolayev, 2020, Evolutionary considerations of the oligosaccharyltransferase AglB and other aspects of N-glycosylation across archaea, Mol Phylogenet Evol, 153, 106951, 10.1016/j.ympev.2020.106951 · DOI
- Oborník, 2019, Endosymbiotic evolution of algae, secondary heterotrophy and parasitism, Biomol Ther, 9, 266
- Ocaña-Pallarès, 2022, Divergent genomic trajectories predate the origin of animals and fungi, Nature, 609, 747, 10.1038/s41586-022-05110-4 · DOI
- Paschinger, 2015, Glycoscience: biology and medicine, 795, 10.1007/978-4-431-54841-6_153 · DOI
- Pasquier, 2017, Evolution of gene expression after whole-genome duplication: new insights from the spotted gar genome, J Exp Zoolog B Mol Dev Evol, 328, 709, 10.1002/jez.b.22770 · DOI
- 2023, InterPro in 2022, Nucleic Acids Res, 51, D418, 10.1093/nar/gkac993 · DOI
- Priyam, 2019, Sequenceserver: a modern graphical user Interface for custom BLAST databases, Mol Biol Evol, 36, 2922, 10.1093/molbev/msz185 · DOI
- Prum, 2015, A comprehensive phylogeny of birds (Aves) using targeted next-generation DNA sequencing, Nature, 526, 569, 10.1038/nature15697 · DOI · Paper page
- Ragland, 2017, From bacterial killing to immune modulation: recent insights into the functions of lysozyme, PLoS Pathog, 13, e1006512, 10.1371/journal.ppat.1006512 · DOI
- Richter, 2022, EukProt: a database of genome-scale predicted proteins across the diversity of eukaryotes, Peer Community J, 2, 10.24072/pcjournal.173 · DOI
- Romero, 1985, Comparison between 1-deoxynojirimycin and N-methyl-1-deoxynojirimycin as inhibitors of oligosaccharide processing in intestinal epithelial cells, Biochem J, 226, 733, 10.1042/bj2260733 · DOI
- Sangster, 2022, Phylogenetic definitions for 25 higher-level clade names of birds, Avian Res, 13, 100027, 10.1016/j.avrs.2022.100027 · DOI
- Schiller, 2012, Complicated N-linked glycans in simple organisms, Biol Chem, 393, 661, 10.1515/hsz-2012-0150 · DOI
- Schoch, 2020, NCBI taxonomy: a comprehensive update on curation, resources and tools, Database, 2020, baaa062, 10.1093/database/baaa062 · DOI · Paper page
- Shen, 2016, SeqKit: a cross-platform and ultrafast toolkit for FASTA/Q file manipulation, PLoS One, 11, e0163962, 10.1371/journal.pone.0163962 · DOI · Paper page
- Simakov, 2020, Deeply conserved synteny resolves early events in vertebrate evolution, Nat Ecol Evol, 4, 820, 10.1038/s41559-020-1156-z · DOI · Paper page
- Sobala, 2018, Structural, mechanistic and functional characterization of glycoside hydrolases of family GH99 [phd]
- Sobala, 2020, Structure of human endo-α-1,2-mannosidase (MANEA), an antiviral host-glycosylation target, Proc Natl Acad Sci, 117, 29595, 10.1073/pnas.2013620117 · DOI
- Sobala, 2020, An epoxide intermediate in glycosidase catalysis, ACS Cent Sci, 6, 760, 10.1021/acscentsci.0c00111 · DOI
- Strassert, 2022, Phylogenomic insights into the early diversification of fungi, Curr Biol, 32, 3628, 10.1016/j.cub.2022.06.057 · DOI
- Tabas, 1979, Purification and characterization of a rat liver Golgi alpha-mannosidase capable of processing asparagine-linked oligosaccharides, J Biol Chem, 254, 11655, 10.1016/S0021-9258(19)86534-1 · DOI
- Teufel, 2022, SignalP 6.0 predicts all five types of signal peptides using protein language models, Nat Biotechnol, 40, 1023, 10.1038/s41587-021-01156-3 · DOI
- Thompson, 2012, Structural and mechanistic insight into N-glycan processing by endo-α-mannosidase, Proc Natl Acad Sci, 109, 781, 10.1073/pnas.1111482109 · DOI
- Tikhonenkov, 2020, Insights into the origin of metazoan multicellularity from predatory unicellular relatives of animals, BMC Biol, 18, 39, 10.1186/s12915-020-0762-1 · DOI
- Tikhonenkov, 2020, New lineage of microbial predators adds complexity to reconstructing the evolutionary origin of animals, Curr Biol, 30, 4500, 10.1016/j.cub.2020.08.061 · DOI
- Tulsiani, 1982, Alpha-D-mannosidases of rat liver Golgi membranes. Mannosidase II is the GlcNAcMAN5-cleaving enzyme in glycoprotein biosynthesis and mannosidases Ia and IB are the enzymes converting Man9 precursors to Man5 intermediates, J Biol Chem, 257, 3660, 10.1016/S0021-9258(18)34831-2 · DOI
- Urrutia, 2022, Txikispora philomaios n. sp., n. g., a micro-eukaryotic pathogen of amphipods, reveals parasitism and hidden diversity in class Filasterea, J Eukaryot Microbiol, 69, e12875, 10.1111/jeu.12875 · DOI
- Varki, 2015, Symbol nomenclature for graphical representations of Glycans, Glycobiology, 25, 1323, 10.1093/glycob/cwv091 · DOI
- Wagih, 2017, Ggseqlogo: a versatile R package for drawing sequence logos, Bioinformatics, 33, 3645, 10.1093/bioinformatics/btx469 · DOI
- West, 2021, Glycomics, Glycoproteomics, and Glycogenomics: an inter-taxa evolutionary perspective, Mol Cell Proteomics, 20, 100024, 10.1074/mcp.R120.002263 · DOI
- Wiater, 2005, Production and use of mutanase from Trichoderma harzianum for effective degradation of streptococcal mutans, Braz J Microbiol, 36, 137, 10.1590/S1517-83822005000200008 · DOI
- Wörheide, 2012, Advances in marine biology, 1
- Xie, 2021, Global profiling of N-glycoproteins and N-Glycans in the diatom Phaeodactylum tricornutum, Front Plant Sci, 12, 10.3389/fpls.2021.779307 · DOI
- Xu, 2019, The allotetraploid origin and asymmetrical genome evolution of the common carp Cyprinus carpio, Nat Commun, 10, 4625, 10.1038/s41467-019-12644-1 · DOI
- Zuber, 2000, Golgi apparatus immunolocalization of endomannosidase suggests post-endoplasmic reticulum glucose trimming: implications for quality control, Mol Biol Cell, 11, 4227, 10.1091/mbc.11.12.4227 · DOI
Metadata
- Authors
- Sobala, Ł. F.
- Affiliations
- Laboratory of Glycobiology, Hirszfeld Institute of Immunology and Experimental Therapy , Weigla 12, 53-114 Wroclaw , Poland
- ORCID
- Sobala, Łukasz F
- Venue
- Glycobiology
- Publisher
- Oxford University Press (OUP)
- Published
- 2023-05-18
- Volume
- 33
- Issue
- 9
- Pages
- 687-699
- ISSN
- 0959-6658 (ISSN-L)
- 1460-2423
- PMC
- PMC11025385
- OpenAlex
- W4377012484
- Cited by
- 5
- References
- 10
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 1
- FWCI
- 0.44
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Glycobiology (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Science Centre of Poland (2020/36/C/NZ8/00081)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Glycosylation and Glycoproteins Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- N-glycosylation, cis-Golgi, whole-genome duplication, paralogs, multicellularity, eukaryotic phylogeny, Golgi apparatus
- MeSH terms
- Animals, Glycosylation, Golgi Apparatus, Mannosidases, Phylogeny, Polysaccharides, Vertebrates, alpha-Mannosidase, Eukaryota
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