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参考文献
1.
Sakai, T., Nishimura, S. I., Naito, T., & Saito, M. (2017). Influenza A virus hemagglutinin
and neuraminidase act as novel motile machinery. Sci Rep 7,
2.
Horimoto, T., & Kawaoka, Y. (2005). Influenza: Lessons from past pandemics, warnings
from current incidents. Nat Rev Microbiol 3, 591–600
3.
Broszeit, F., van Beek, R. J., Unione, L., Bestebroer, T. M., Chapla, D., Yang, J. Y.,
Moremen, K. W., Herfst, S., Fouchier, R. A. M., de Vries, R. P., & Boons, G. J. (2021).
Glycan remodeled erythrocytes facilitate antigenic characterization of recent A/H3N2
influenza viruses. Nat Commun 12,
4.
Suzuki, N., Abe, T., & Natsuka, S. (2022). Structural analysis of N-glycans in chicken
trachea and lung reveals potential receptors of chicken influenza viruses. Sci Rep 12,
5.
Zhao, C., & Pu, J. (2022). Influence of Host Sialic Acid Receptors Structure on the Host
Specificity of Influenza Viruses. Viruses 14,
6.
Kobayashi, D., Hiono, T., Ichii, O., Nishihara, S., Takase-Yoden, S., Yamamoto, K.,
Kawashima, H., Isoda, N., & Sakoda, Y. (2022). Turkeys possess diverse Siaα2-3Gal
glycans that facilitate their dual susceptibility to avian influenza viruses isolated from
ducks and chickens. Virus Res 315,
7.
Yang, J., Cui, H., Teng, Q., Ma, W., Li, X., Wang, B., Yan, D., Chen, H., Liu, Q., & Li, Z.
(2019). Ducks induce rapid and robust antibody responses than chickens at early time
after intravenous infection with H9N2 avian influenza virus. Virol J 16,
8.
Vreman, S., Bergervoet, S. A., Zwart, R., Stockhofe-Zurwieden, N., & Beerens, N. (2022).
Tissue tropism and pathology of highly pathogenic avian influenza H5N6 virus in
chickens and Pekin ducks. Res Vet Sci 146, 1–4
9.
Sid, H., Hartmann, S., Winter, C., & Rautenschlein, S. (2017). Interaction of influenza A
viruses with oviduct explants of different avian species. Front Microbiol 8, 1–11
10.
Pillai, S. P. S., Saif, Y. M., & Lee, C. W. (2010). Detection of Influenza A Viruses in Eggs
Laid by Infected Turkeys. Avian Disease 54, 830–833
11.
Uchida, Y., Takemae, N., Tanikawa, T., Kanehira, K., & Saito, T. (2016). Transmission of
an H5N8-Subtype Highly Pathogenic Avian Influenza Virus from Infected Hens to Laid
Eggs. Avian Dis 60, 450–453
12.
Hiono, T., Okamatsu, M., Nishihara, S., Takase-Yoden, S., Sakoda, Y., & Kida, H. (2014).
A chicken influenza virus recognizes fucosylated α2,3 sialoglycan receptors on the
epithelial cells lining upper respiratory tracts of chickens. Virology 456–457, 131–138
13.
Gambaryan, A., Yamnikova, S., Lvov, D., Tuzikov, A., Chinarev, A., Pazynina, G.,
Webster, R., Matrosovich, M., & Bovin, N. (2005). Receptor specificity of influenza
viruses from birds and mammals: New data on involvement of the inner fragments of the
carbohydrate chain. Virology 334, 276–283
14.
Ichimiya, T., Okamatsu, M., Kinoshita, T., Kobayashi, D., Ichii, O., Yamamoto, N.,
Sakoda, Y., Kida, H., Kawashima, H., Yamamoto, K., Takase-Yoden, S., & Nishihara, S.
(2021). Sulfated glycans containing NeuAcα2-3Gal facilitate the propagation of human
H1N1 influenza A viruses in eggs. Virology 562, 29–39
15.
Ichimiya, T., Nishihara, S., Takase-Yoden, S., Kida, H., & Aoki-Kinoshita, K. (2014).
Frequent glycan structure mining of influenza virus data revealed a sulfated glycan motif
that increased viral infection. Bioinformatics 30, 706–711
16.
Broszeit, F., Tzarum, N., Zhu, X., Nemanichvili, N., Eggink, D., Leenders, T., Li, Z., Liu,
L., Wolfert, M. A., Papanikolaou, A., Martínez-Romero, C., Gagarinov, I. A., Yu, W.,
García-Sastre, A., Wennekes, T., Okamatsu, M., Verheije, M. H., Wilson, I. A., Boons, G.
J., & de Vries, R. P. (2019). N-Glycolylneuraminic Acid as a Receptor for Influenza A
Viruses. Cell Rep 27, 3284-3294.e6
17.
Hincke, M. T., Da Silva, M., Guyot, N., Gautron, J., McKee, M. D., Guabiraba-Brito, R.,
& Réhault-Godbert, S. (2019). Dynamics of Structural Barriers and Innate Immune
Components during Incubation of the Avian Egg: Critical Interplay between Autonomous
Embryonic Development and Maternal Anticipation. J Innate Immun 11, 111–124
18.
Hirose, K., Amano, M., Hashimoto, R., Lee, Y. C., & Nishimura, S. I. (2011). Insight into
glycan diversity and evolutionary lineage based on comparative avio-N-glycomics and
sialic acid analysis of 88 egg whites of galloanserae. Biochemistry 50, 4757–4774
19.
Laskowski, M., Kato, I., Ardelt, W., Cook, J., Denton, A., Empie, M. W., Kohr, W. J.,
Soon, #, Park, J., Parks, K., Schatzley, B. L., Schoenberger, O. L., Tashiro, M., Vichot,
G., Whatley, H. E., Wieczorek, A., & Wieczorek, M. (1987). Ovomucoid Third Domains
from 100 Avian Species: Isolation, Sequences, and Hypervariability of Enzyme-Inhibitor
Contact Residues. Biochemistry 26, 202–221
20.
Laskowski, M., Apostol, I., Ardelt, W., Cook, J., Giletto, A., Kelly, C. A., Lu, W., Park,
S. J., Qasim, M. A., Whatley, H. E., Wieczorek, A., & Wynn, R. (1990). Amino Acid
Sequences of Ovomucoid Third Domain from 25 Additional Species of Birds. J Protein
Chem 9,
21.
Apostol, I., Giletto, A., Komiyama, T., Zhang, W., & Laskowski, M. (1993). Amino Acid
Sequences of Ovomucoid Third Domains from 27 Additional Species of Birds. J Protein
Chem 12,
22.
Sibley, C. G., & Monroe, B. L. (1990). Distribution and Taxonomy of Birds of the World
(Yale University Press, New Haven, CT.)
23.
Sibley, C. G., & Monroe, B. L. (1993). A Supplement to Distribution and Taxonomy of
Birds of the Worlds (Yale University Press, New Haven, CT)
24.
Sanes, J. T., Hinou, H., Lee, Y. C., & Nishimura, S. I. (2019). Glycoblotting of Egg White
Reveals Diverse N-Glycan Expression in Quail Species. J Agric Food Chem 67, 531–540
25.
Gizaw, S. T., Ohashi, T., Tanaka, M., Hinou, H., & Nishimura, S. I. (2016). Glycoblotting
method allows for rapid and efficient glycome profiling of human Alzheimer’s disease
brain, serum and cerebrospinal fluid towards potential biomarker discovery. Biochim
Biophys Acta Gen Subj 1860, 1716–1727
26.
Miura, Y., Shinohara, Y., Furukawa, J. I., Nagahori, N., & Nishimura, S. I. (2007). Rapid
and simple solid-phase esterification of sialic acid residues for quantitative glycomics by
mass spectrometry. Chemistry - A European Journal 13, 4797–4804
27.
Yu, S.-Y., Snovida, S., & Khoo, K.-H. (2020). Permethylation and Microfractionation of
Sulfated Glycans for MS Analysis. Bio Protoc 10, 1–13
28.
Yu, S. Y., Wu, S. W., Hsiao, H. H., & Khoo, K. H. (2009). Enabling techniques and
strategic workflow for sulfoglycomics based on mass spectrometry mapping and
sequencing of permethylated sulfated glycans. Glycobiology 19, 1136–1149
29.
Hinou, H. (2019). Aniline derivative/DHB/alkali metal matrices for reflectron mode
MALDI-TOF and TOF/TOF MS analysis of unmodified sialylated oligosaccharides and
glycopeptides. Int J Mass Spectrom 443, 109–115
30.
Barada, E., & Hinou, H. (2022). BOA/DHB/Na: An Efficient UV-MALDI Matrix for
High-Sensitivity and Auto-Tagging Glycomics. Int J Mol Sci 23, 12510
31.
Chen, J. Y., Huang, H. H., Yu, S. Y., Wu, S. J., Kannagi, R., & Khoo, K. H. (2018).
Concerted mass spectrometry-based glycomic approach for precision mapping of sulfo
sialylated N-glycans on human peripheral blood mononuclear cells and lymphocytes.
Glycobiology 28, 9–20
32.
Kuo, C. W., Guu, S. Y., & Khoo, K. H. (2018). Distinctive and Complementary MS 2
Fragmentation Characteristics for Identification of Sulfated Sialylated N-Glycopeptides
by nanoLC-MS/MS Workflow. J Am Soc Mass Spectrom 29, 1166–1178
33.
Ceroni, A., Maass, K., Geyer, H., Geyer, R., Dell, A., & Haslam, S. M. (2008).
GlycoWorkbench: A tool for the computer-assisted annotation of mass spectra of glycans.
J Proteome Res 7, 1650–1659
34.
Cooper, C. A., Gasteiger, E., & Packer, N. H. (2001). GlycoMod-A software tool for
determining glycosylation compositions from mass spectro-metric data. Proteomics 1,
340–349
35.
Montalban, B. M., & Hinou, H. (2023). Glycoblotting enables seamless and
straightforward workflow for MALDI-TOF/MS-based sulphoglycomics of N- and Oglycans. Proteomics, 1–10
36.
Wille, M., Lisovski, S., Roshier, D., Ferenczi, M., Hoye, B. J., Leen, T., Warner, S.,
Fouchier, R. A. M., Hurt, A. C., Holmes, E. C., & Klaassen, M. (2023). Strong host
phylogenetic and ecological effects on host competency for avian influenza in Australian
wild birds. Proceedings of the Royal Society B: Biological Sciences 290, 1–9
37.
van Dijk, J. G., Verhagen, J. H., Wille, M., & Waldenström, J. (2018). Host and virus
ecology as determinants of influenza A virus transmission in wild birds. Curr Opin Virol
28, 26–36
38.
Garamszegi, L. Z., & Møller, A. P. (2007). Prevalence of avian influenza and host ecology.
Proceedings of the Royal Society B: Biological Sciences 274, 2003–2012
39.
Springer, S. A., & Gagneux, P. (2016). Glycomics: revealing the dynamic ecology and
evolution of sugar molecules. J Proteomics 135, 90–100
40.
Olsen, B., Munster, V. J., Wallensten, A., Waldenström, J., Osterhaus, A. D. M. E., &
Fouchier, R. A. M. (2006). Global Patterns of Influenza A Virus in Wild Birds. Science
(1979) 312, 384–388
41.
Gonzalez, J., Düttmann, H., & Wink, M. (2009). Phylogenetic relationships based on two
mitochondrial genes and hybridization patterns in Anatidae. J Zool 279, 310–318
42.
Donne-Gousse, C., Laudet, V., & Hanni, C. (2002). A molecular phylogeny of
anseriformes based on mitochondrial DNA analysis. Molecular Phylogenetics and
Evolution 23, 339–356
43.
Sun, Z., Pan, T., Hu, C., Sun, L., Ding, H., Wang, H., Zhang, C., Jin, H., Chang, Q., Kan,
X., & Zhang, B. (2017). Rapid and recent diversification patterns in Anseriformes birds:
Inferred from molecular phylogeny and diversification analyses. PLoS One 12, 1–21
44.
Tamura, K., & Nei, M. (1993). Estimation of the Number of Nucleotide Substitutions in
the Control Region of Mitochondrial DNA in Humans and Chimpanzees ’. Mol Biol Evol
10, 512–526
45.
Tamura, K., Stecher, G., & Kumar, S. (2021). MEGA11: Molecular Evolutionary
Genetics Analysis Version 11. Mol Biol Evol 38, 3022–3027
3.6
Supplementary Information
Table S3.1. The list of egg whites from various species of Order Anseriformes (4 families, 27
genera, 66 species) used in this study. Classification was based on Sibley’s DNA-DNA
hybridization[22, 23].
Sample
ID
D1
D2
D3
D4
D5
D6
D7
D8
D9
D10
D11
D12
D13
D14
D15
D16
D17
D18
D19
D20
D21
D22
D23
D24
D25
D26
D27
D28
D29
D30
D31
D32
D33
D34
D35
D36
D37
D38
D39
D40
D41
D42
D43
D44
D45
D46
D47
D48
D49
D50
D51
D52
D53
D54
D55
D56
Scientific name
Aix galericulata
Anas platyrhynchos
Lophodytes cucullatus
Aythya americana
Anas versicolor
Anser anser
Anser indicus
Dendrocygna eytoni
Tadorna radjah
Sarkidiornis melanotos
Anseranas semipalmata
Aix sponsa
Alopochen aegyptiaca
Anas platyrhynchos domesticus
Anser anser domesticus (America)
Anser anser domesticus (France)
Anser anser domesticus (Germany)
Anser canagicus
Anser cygnoides domesticus
Anser cygnoides domesticus
Anser cygnoides domesticus
Anser erythropus
Callonetta leucophrys
Dendrocygna arborea
Lophonetta speculariodes
Netta rufina
Oxyura jamaicensis
Chloephaga picta picta
Branta leucopsis
Branta sandvicensis
Anas gibberifrons
Anas laysanensis
Anas luzonica
Anas rubripes
Anas clypeata
Oxyura vittata
Anas melleri
Oxyura australis
Branta canadensis maxima
Dendrocygna viduata
Anser brachyrhynchus
Chauna torquata
Thalassornis leuconotos
Tadorna tadornoides
Chenonetta jubata
Somateria mollissima
Anser albifrons
Mergus serrator
Aythya affinis
Dendrocygna autumnalis
Clangula hyemalis
Anas discors
Oxyura punctata
Anas strepera
Heteronetta atricapilla
Anas superciliosa
Family
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Dendrocygnidae
Anatidae
Anatidae
Anseranatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Dendrocygnidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Dendrocygnidae
Anatidae
Anhimidae
Dendrocygnidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Dendrocygnidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Sub-Family
Anatinae
Anatinae
Anatinae
Anatinae
Anatinae
Anserinae
Anserinae
Dendrocygninae
Anserinae
Anserinae
Anseranatidae
Anatinae
Anserinae
Anatinae
Anserinae
Anserinae
Anserinae
Anserinae
Anserinae
Anserinae
Anserinae
Anserinae
Anatinae
Dendrocygninae
Anatinae
Anatinae
Oxyurinae
Anserinae
Anserinae
Anserinae
Anatinae
Anatinae
Anatinae
Anatinae
Anatinae
Oxyurinae
Anatinae
Oxyurinae
Anserinae
Dendrocygninae
Anserinae
Anhimidae
Dendrocygninae
Anserinae
Anatinae
Anatinae
Anserinae
Anatinae
Anatinae
Dendrocygninae
Anatinae
Anatinae
Oxyurinae
Anatinae
Anatinae
Anatinae
Common Name
Mandarin Duck
Mallard Duck
Hooded Mergenser
Red head
Silver Teal
Graylag Goose
Bar Headed Goose
Plumed Whistling Duck
White Headed Shelduck
Knob-billed Goose
Magpie Goose
Wood Duck
Egyptian Goose
White Call Duck
Buff Goose
Dewlap Toulouse Goose
Embdens Goose
Emperor Goose
African Goose
White China Goose
Brown China Goose
Lesser white-fronted Goose
Ringed Teal
West Indian Whistling Duck
Crested Duck
Red Crested Pochard
Ruddy duck
Magellan Goose
Barnacle Goose
Hawaiian Goose
Indonesian Teal
Laysan Duck
Philippine Duck
American Black Duck
Northern Shoveler
Lake Duck
Meller's Duck
Blue-billed Duck
Canada Goose
White-faced Whistling Duck
Pink-footed Goose
Southern Screamer
White-backed Duck
Australian Shelduck
Australian Wood Duck
Common Eider
Greater whitefronted Goose
Red-breasted Merganser
Lesser Scaup
Black-bellied whistling Duck
Longtailed Duck
Blue-winged Teal
Gadwall
Black-headed Duck
Pacific black Duck
D57
D58
D59
D60
D61
D62
D63
D64
D65
D66
D67
D68
D69
D70
D71
D72
Anser caerulescens
Aythya fuligula
Aythya ferina
Anas formosa
Dendrocygna bicolor
Anas querquedula
Malacorhynchus membranaceus
Anas hottentota
Anas georgica
Biziura lobata
Cygnus atratus
Aythya australis
Amazonetta brasiliensis
Lophonetta cristata
Anas crecca
Tadorna tadorna
Anatidae
Anatidae
Anatidae
Anatidae
Dendrocygnidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anatidae
Anserinae
Anatinae
Anatinae
Anatinae
Dendrocygninae
Anatinae
Anatinae
Anatinae
Anatinae
Oxyurinae
Cygninae
Anatinae
Anatinae
Anatinae
Anatinae
Anserinae
Snow Goose
Tufted Duck
Common Pochard
Baikal Teal
Fulvous Whistling Duck
Garganey
Pink-eared Duck
Hottentot Teal
Yellow-billed Pintail
Musk Duck
Black swan
Hardhead
Brazilian Teal
Common Teal
Common Shelduck
Table S3.2. List of 89 acidic N-glycans identified from the egg whites of 79 waterfowl species.
Glycan structures were inferred from glycan composition based on the observed monoisotopic
masses.
Glycan
ID
A1
A2
A3
A4
A5
A6
A7
A8
A9
A10
A11
A12
A13
A14
A15
A16
A17
A18
A19
A20
A21
A22
A23
A24
A25
A26
A27
A28
A29
A30
A31
A32
A33
A34
A35
A36
A37
A38
A39
A40
A41
A42
A43
A44
A45
A46
A47
A48
A49
A50
A51
A52
A53
A54
A55
A56
A57
A58
Observed
mass, m/z
[M – H]1094.339
1108.327
1135.373
1149.392
1256.320
1270.431
1295.303
1297.420
1311.445
1338.419
1352.412
1418.430
1432.469
1441.498
1443.485
1459.475
1473.505
1500.497
1514.530
1580.496
1589.525
1594.528
1603.574
1605.533
1621.533
1635.542
1646.558
1662.556
1676.605
1703.584
1717.608
1749.602
1751.599
1764.667
1765.618
1767.620
1783.585
1792.814
1797.610
1806.657
1808.607
1824.608
1838.661
1865.620
1879.661
1888.924
1906.655
1920.682
1945.612
1952.677
1954.866
1959.599
1970.726
1986.667
2000.577
2009.653
2011.663
2027.682
Calculated
Glycoform Mass
[M – BOA]
972.274
972.284
1013.301
1013.310
1134.327
1134.336
1159.368
1175.353
1175.363
1216.380
1216.390
1296.380
1293.389
1305.426
1321.411
1337.406
1337.416
1378.433
1378.442
1458.432
1467.469
1458.442
1467.479
1483.464
1499.459
1499.469
1524.491
1540.486
1540.495
1581.512
1581.522
1613.537
1629.522
1628.502
1629.532
1645.517
1661.512
1670.549
1661.521
1670.558
1686.544
1702.538
1702.548
1743.565
1743.575
1766.543
1784.592
1784.601
1823.565
1816.616
1832.601
1823.574
1848.596
1864.591
1864.601
1873.638
1889.623
1905.618
Mass
Error,
ppm
-10.8
-30.5
-4.2
4.8
-66.7
14.1
-109.5
-7.5
3.7
-28.2
-40.5
-18.9
2.4
-3.3
-1.9
-5.3
8.1
-8.5
7.5
-8.1
-13.1
5.5
11.4
-4.8
-1.7
-2.2
-5.9
-4.1
19.8
-2.8
5.6
-6.8
0.1
50.0
5.3
14.8
-2.1
105.0
6.6
12.5
-7.6
-3.7
19.5
-11.7
4.8
161.1
-7.2
2.3
-15.3
-7.9
96.3
-26.5
26.9
-0.5
-50.2
-30.7
-18.1
-6.1
Monosaccharide composition
Hex3 HexNAc2 Su1
Hex3 HexNAc2 Pho1
Hex2 HexNAc3 Su1
Hex2 HexNAc3 Pho1
Hex4 HexNAc2 Su1
Hex4 HexNAc2 Pho1
Hex2 HexNAc3 dHex1 Pho1
HexNAc1 Su1 + Man3 GlcNAc2
HexNAc1 Pho1 + Man3 GlcNAc2
Hex2 HexNAc4 Su1
Hex2 HexNAc4 Pho1
Hex2 Su1 + Man3 GlcNAc2
Hex2 Pho1 + Man3 GlcNAc2
Unknown structure
HexNAc1 dHex1 Su1 + Man3 GlcNAc2
Hex1 HexNAc1 Su1 + Man3 GlcNAc2
Hex1 HexNAc1 Pho1 + Man3 GlcNAc2
HexNAc2 Su1 + Man3 GlcNAc2
HexNAc2 Pho1 + Man3 GlcNAc2
Hex3 Su1 + Man3 GlcNAc2
HexNAc1 dHex2 Su1 + Man3 GlcNAc2
Hex3 Pho1 + Man3 GlcNAc2
HexNAc1 dHex2 Pho1 + Man3 GlcNAc2
Hex1 HexNAc1 dHex1 Su1 + Man3 GlcNAc2
Hex2 HexNAc1 Su1 + Man3 GlcNAc2
Hex2 HexNAc1 Pho1 + Man3 GlcNAc2
HexNAc2 dHex1 Su1 + Man3 GlcNAc2
Hex1 HexNAc2 Su1 + Man3 GlcNAc2
Hex1 HexNAc2 Pho1 + Man3 GlcNAc2
HexNac3 Su1 + Man3 GlcNAc2
HexNac3 Pho1 + Man3 GlcNAc2
Unknown structure
Hex1 HexNAc1 dHex2 Su1 + Man3 GlcNAc2
Hex1 HexNAc1 NeuAc1 Su1 + Man3 GlcNAc2
Hex1 HexNAc1 dHex2 Pho1 + Man3 GlcNAc2
Hex2 HexNAc1 dHex1 Su1 + Man3 GlcNAc2
Hex3 HexNAc1 Su1 + Man3 GlcNAc2
HexNAc2 dHex2 Su1 + Man3 GlcNAc2
Hex3 HexNAc1 Pho1 + Man3 GlcNAc2
HexNAc2 dHex2 Pho1 + Man3 GlcNAc2
Hex1 HexNAc2 dHex1 Su1 + Man3 GlcNAc2
Hex2 HexNAc2 Su1 + Man3 GlcNAc2
Hex2 HexNAc2 Pho1 + Man3 GlcNAc2
Hex1 HexNAc3 Su1 + Man3 GlcNAc2
Hex1 HexNAc3 Pho1 + Man3 GlcNAc2
Hex4 dHex1 Su1 + Man3 GlcNAc2
HexNAc4 Su1 + Man3 GlcNAc2
HexNAc4 Pho1 + Man3 GlcNAc2
Hex4 HexNAc1 Su1 + Man3 GlcNAc2
HexNAc2 dHex3 Pho1 + Man3 GlcNAc2
Hex1 HexNAc2 dHex2 Su1 + Man3 GlcNAc2
Hex4 HexNAc1 Pho1 + Man3 GlcNAc2
Hex2 HexNAc2 dHex1 Su1 + Man3 GlcNAc2
Hex3 HexNAc2 Su1 + Man3 GlcNAc2
Hex3 HexNAc2 Pho1 + Man3 GlcNAc2
HexNAc3 dHex2 Pho1 + Man3 GlcNAc2
Hex1 HexNAc3 dHex1 Su1 + Man3 GlcNAc2
Hex2 HexNAc3 Su1 + Man3 GlcNAc2
Glyconnect
Database
Links
Glyconnect
Glyconnect
Glyconnect
Glyconnect
Glyconnect
Glyconnect
Glyconnect
Glyconnect
Glyconnect
Glyconnect
Glyconnect
Glyconnect
Glyconnect
Glyconnect
Glyconnect
Glyconnect
Glyconnect
Glyconnect
Glyconnect
Glyconnect
Glyconnect
A59
A60
A61
A62
A63
A64
A65
A66
A67
A68
A69
A70
A71
A72
A73
A74
A75
A76
A77
A78
A79
A80
A81
A82
A83
A84
A85
A86
A87
A88
A89
2041.713
2050.704
2068.719
2082.738
2109.758
2114.753
2129.999
2146.364
2148.660
2158.155
2171.782
2189.759
2203.771
2212.764
2230.794
2244.834
2271.838
2278.900
2287.809
2320.103
2374.818
2392.895
2406.937
2433.956
2449.933
2479.957
2555.030
2569.031
2596.066
2758.164
2920.151
1905.627
1928.596
1946.644
1946.654
1987.671
1978.669
1993.634
2010.659
2026.644
2035.681
2035.690
2067.671
2067.680
2090.649
2108.697
2108.707
2149.724
2156.707
2165.744
2197.734
2252.702
2270.750
2270.760
2311.777
2327.797
2343.801
2432.803
2432.812
2473.829
2635.882
2797.935
4.3
15.2
-1.0
3.3
5.0
3.4
135.3
-173.2
-28.3
184.1
6.9
5.1
6.5
17.2
8.8
22.5
16.2
51.0
-5.2
126.0
16.6
28.3
41.8
42.1
24.4
31.9
58.9
55.4
61.6
74.5
47.7
Hex2 HexNAc3 Pho1 + Man3 GlcNAc2
Hex5 dHex1 Su1 + Man3 GlcNAc2
Hex1 HexNAc4 Su1 + Man3 GlcNAc2
Hex1 HexNAc4 Pho1 + Man3 GlcNAc2
HexNAc5 Su1 + Man3 GlcNAc2
Hex1 HexNAc2 dHex3 Pho1 + Man3 GlcNAc2
Hex2 HexNAc2 NeuAc1 Su1 + Man3 GlcNAc2
Hex3 HexNAc2 dHex1 Pho1 + Man3 GlcNAc2
Hex4 HexNAc2 Su1 + Man3 GlcNAc2
Hex1 HexNAc3 dHex2 Su1 + Man3 GlcNAc2
Hex1 HexNAc3 dHex2 Pho1 + Man3 GlcNAc2
Hex3 HexNAc3 Su1 + Man3 GlcNAc2
Hex3 HexNAc3 Pho1 + Man3 GlcNAc2
Hex6 dHex1 Su1 + Man3 GlcNAc2
Hex2 HexNAc4 Su1 + Man3 GlcNAc2
Hex2 HexNAc4 Pho1 + Man3 GlcNAc2
Hex1 HexNAc5 Su1 + Man3 GlcNAc2
Hex3 HexNAc2 dHex2 Su1 + Man3 GlcNAc2
HexNAc3 dHex4 Su1 + Man3 GlcNAc2
Hex2 HexNAc3 dHex2 Su1 + Man3 GlcNAc2
Hex7 dHex1 Su1 + Man3 GlcNAc2
Hex3 HexNAc4 Su1 + Man3 GlcNAc2
Hex3 HexNAc4 Pho1 + Man3 GlcNAc2
Hex2 HexNAc5 Su1 + Man3 GlcNAc2
Hex1 HexNAc3 dHex4 Su1 + Man3 GlcNAc2
Hex2 HexNAc3 dHex3 Pho1 + Man3 GlcNAc2
Hex4 HexNAc4 Su1 + Man3 GlcNAc2
Hex4 HexNAc4 Pho1 + Man3 GlcNAc2
Hex3 HexNAc5 Su1 + Man3 GlcNAc2
Hex4 HexNAc5 Su1 + Man3 GlcNAc2
Hex5 HexNAc5 Su1 + Man3 GlcNAc2
Glyconnect
Glyconnect
Glyconnect
*Monosaccharide nomenclatures are based on the SNFG: Hexose (Hex), N-acetyl hexosamine (HexNAc),
Mannose (Man), N-acetyl glucosamine (GlcNAc), Fucose (dHex), Sulfate (Su), and Phosphate (Pho). The
number of units corresponding to each monosaccharide are indicated after each abbreviation.
*The links to the Glyconnect database of the Swiss Institute of Bioinformatics are provided for selected
monoisotopic peaks found in the database.
*From the 89 monoisotopic masses, 55 sulfated and 34 phosphorylated N-glycans were identified based on
their glycan composition and MS/MS analysis. Fucosylated acidic N-glycan structures were also found in
trace abundance relative to un-fucosylated acidic N-glycans.
*Glycoform mass is the mass of unlabeled N-glycan structure denoted as [M-BOA], BOA is
benzyloxyamine with a molecular mass of 123.0684 Da.
Table S3.3. Waterfowl classification based on their virus prevalence.
Duck ID
D2
D56
D34
D71
D31
D54
D52
D45
D12
D68
D72
D44
D63
D39
D47
D06
Species
Anas platyrhynchos
Anas superciliosa
Anas rubripes
Anas creeca
Anas gibberifrons
Anas strepera
Anas discors
Chenonetta jubata
Aix sponsa
Aythya australis
Tadorna tadorna
Tadorna tadornoides
M. Membranaceus
Branta canadensis
Anser albifrons
Anser anser
PCA
Group
VP
Values
12.9
5.7
18.1
4.0
5.8
1.5
11.2
2.0
2.2
2.8
6.5
5.0
6.3
0.8
2.2
1.1
VP
Classification
HVP
HVP
HVP
LVP
HVP
LVP
HVP
LVP
LVP
LVP
HVP
LVP
HVP
LVP
LVP
LVP
*Each waterfowl species was classified either as a high virus prevalence (HVP) or low virus prevalence
(LVP). Classification was based on the average virus prevalence (5.5%). LVP < 5.50% < HVP.
*Virus prevalence data of the 16 species shown on the table was taken from the work of Wille, M. et al.
[36] and Olsen, B. et al. [40].
Table S3.4. GenBank accession numbers for various genes of the 72 Anseriformes species
in this study.
Sample
ID
D01
D02
D03
D04
D05
D06
D07
D08
D09
D10
D11
D12
D13
D14
D15
D16
D17
D18
D19
D20
D21
D22
D23
D24
D25
D26
D27
D28
D29
D30
D31
D32
D33
D34
D35
D36
D37
D38
D39
D40
D41
D42
D43
D44
D45
D46
D47
D48
D49
D50
D51
D52
D53
Scientific name
Aix galericulata
Anas platyrhynchos
Lophodytes cucullatus
Aythya americana
Anas versicolor
Anser anser
Anser indicus
Dendrocygna eytoni
Tadorna radjah
Sarkidiornis melanotos
Anseranas semipalmata
Aix sponsa
Alopochen aegyptiaca
Anas platyrhynchos domesticus
Anser anser domesticus (America)
Anser anser domesticus (France)
Anser anser domesticus (Germany)
Anser canagica
Anser cygnoides domesticus
Anser cygnoides domesticus
Anser cygnoides domesticus
Anser erythropus
Callonetta leucophrys
Dendrocygna arborea
Lophonetta speculariodes
Netta rufina
Oxyura jamaicensis
Chloephaga picta
Branta leucopsis
Branta sandvicensis
Anas gibberifrons
Anas laysanensis
Anas luzonica
Anas rubripes
Anas clypeata
Oxyura vittata
Anas melleri
Oxyura australis
Branta canadensis
Dendrocygna viduata
Anser brachyrhynchus
Chauna torquata
Thalassornis leuconotos
Tadorna tadornoides
Chenonetta jubata
Somateria mollissima
Anser albifrons
Mergus serrator
Aythya affinis
Dendrocygna autumnalis
Clangula hyemalis
Anas discors
Oxyura punctata
CO1
Cty b
ND2
JN703260
Mk262361
FJ028237
MN356217
AY666569
Mf580159
EU585604
EU585609
EU585650
NC_000877
AF059094
EU585613
EU585619
EU585647
EU585665
EU585660
NC_005933
EU585605
EU585606
EU585667
EU585672
EU585713
NC_000877
AF059154
EU585676
EU585682
EU585710
EU585728
EU585723
DQ432849
LC145060
EU585615
EU585616
EU585678
EU585679
GU571729
FJ027277
EU161871
EU914157
EU585680
AF059157
JN801488
GQ482234
AY666448
FJ027353
GU571283
JF498832
JQ174015
JF498830
KT151721
AY666211
GU571236
JQ175648
AF059102
EU585657
EU585658
AF515262
EU585630
EU585632
AF059076
AF059078
AF059079
AF059088
AF059062
EU585659
AF059080
AF119167
EU585629
EU585649
EU585614
AY274030
AF059162
EU585720
EU585721
AF515266
EU585693
EU585695
AF059136
AF059138
AF059139
AF059148
AF059122
EU585722
AF059140
AY747867
EU585692
EU585712
EU585677
AY274053
EU585666
AF059100
EU585661
EU585612
EU585655
EU585621
EU585729
AF059160
EU585724
EU585675
EU585718
EU585684
EU585638
EU914146
EU585701
AF059128
DQ434316
FJ027121
GU571243
GU571246
MZ153330
GU571280
FJ027502
GU571244
AY140730
U97738
JN801436
GU571620
DQ433314
GU571482
DQ434308
FJ027495
GU571339
AY666325
Complete
mtDNA
KF437906
MN720361
NC_000877
NC_011196
NC_025654
MN356217
EU585668
EU585669
NC_023832
NC_024922
MW574354
NC_028346
NC_007011
NC_052807
MW849292
NC_004539
MZ365040
MW849278
D54
D55
D56
D57
D58
D59
D60
D61
D62
D63
D64
D65
D66
D68
D67
D69
D70
D71
D72
OG1
OG2
Anas strepera (Mareca strepera)
Heteronetta atricapilla
Anas superciliosa
Anser caerulescens
Aythya fuligula
Aythya ferina
Anas formosa
Dendrocygna bicolor
Anas querquedula
Malacorhynchus membranaceus
Anas hottentota (Anas punctata)
Anas georgica
Biziura lobata
Cygnus atratus
Aythya australis
Amazonetta brasiliensis
Lophonetta cristata
Anas crecca
Tadorna tadorna
Gallus gallus
Struthio camelus
GQ481327
FJ027649
JN801396
DQ434537
JF499099
JF499098
JN703250
GQ481326
FJ027096
NC_012843
MW151626
FJ027059
KC771255
KU140668
LC145063
EU574791
AF059169
AF059092
FJ423758
KU697802
EU585623
AF059073
EU585646
EU585610
EU585651
EU585608
AF059075
EU585627
EU585641
EU585622
AF059054
AF059152
AF059064
AF059113
AF195631
MZ545713
NC_045373
EU585687
EU585686
AF059133
EU585709
EU585673
EU585714
EU585671
AF059135
EU585690
EU585704
EU585685
AF059115
NC_024595
NC_024602
NC_015482
EU585670
AF059173
NC_022452
NC_024750
NC_040902
NC_002785
NC_012843
*Accession numbers of the mitochondrial gene sequences of the cytochrome b (Cty b),
cytochrome oxidase subunit 1 (CO1), NADH dehydrogenase subunit 2 (ND2) and the complete
mitochondrial DNA (mtDNA) was taken from GenBank.
Figure S3.1. The evolutionary history was inferred by using the Maximum Likelihood method and Tamura-Nei model. The tree with the highest log likelihood (11550.63) is shown. Initial tree(s) for the heuristic search were obtained automatically by applying Neighbor-Join and BioNJ algorithms to a matrix of pairwise
distances estimated using the Tamura-Nei model, and then selecting the topology with superior log likelihood value. A discrete Gamma distribution was used to model
evolutionary rate differences among sites (5 categories (+G, parameter = 0.4430)). The rate variation model allowed for some sites to be evolutionarily invariable
([+I], 27.02% sites). The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. This analysis involved 62 nucleotide sequences.
There were a total of 992 positions in the final dataset. Evolutionary analyses were conducted in MEGA11.
Figure S3.2. The evolutionary history was inferred by using the Maximum Likelihood method and Tamura-Nei model. The tree with the highest log likelihood (5786.80) is shown. The percentage of trees in which the associated taxa clustered together is shown below the branches. Initial tree(s) for the heuristic search were
obtained automatically by applying Neighbor-Join and BioNJ algorithms to a matrix of pairwise distances estimated using the Tamura-Nei model, and then selecting
the topology with superior log likelihood value. A discrete Gamma distribution was used to model evolutionary rate differences among sites (5 categories (+G,
parameter = 0.3642)). The tree is drawn to scale, with branch lengths measured in the number of substitutions per site. This analysis involved 18 nucleotide sequences.
There were a total of 1082 positions in the final dataset. Evolutionary analyses were conducted in MEGA11.
Chapter 4
Concluding Remarks
This study addresses the challenges of analyzing sulfated N- and O-glycans in complex
biological samples. We present a comprehensive workflow that integrates the strengths of
Glycoblotting as a complementary purification, enrichment, methylation, and labeling technique
for MALDI-TOF MS-based sulphoglycomics. Glycoblotting demonstrates its efficiency as a
glycan enrichment platform, while the on-bead methyl esterification using MTT successfully
overcomes the obstacles related to trace abundance, sample loss, and the presence of sialic acid.
Notably, the on-bead methyl esterification step of Glycoblotting facilitates the discrimination
between sulfated glycans and sialylated glycans and the differentiation of isomeric glycans
containing sulfate or phosphate groups. This streamlined workflow enables efficient enrichment
and detection of trace sulfated and phosphorylated N-glycans, offering a simplified approach to
MALDI-TOF MS-based sulphoglycomics.
Moreover, employing the Glycoblotting-based sulphoglycomics approach, we uncovered
a diverse array of sulfated and phosphorylated N-glycans in waterfowl egg whites, providing
valuable insights into the differential expressions of acidic N-glycans in egg whites. We observed
distinct variations in the expressions of acidic N-glycans among the four families (Anhimidae,
Anseranatidae, Dendrocygnidae, and Anatinae) within the order Anseriformes. By examining
sulfated trans-Gal(+) and trans-Gal(-) N-glycan structures and phosphorylated N-glycans, we
successfully differentiate waterfowl species. Remarkably, waterfowl species with a high virus
prevalence exhibit elevated phosphorylated hybrid and high-mannose N-glycans expression.
These findings emphasize the significance of phosphorylated and sulfated N-glycans in
comprehending the transmission and evolution of IAV within avian populations.
Further studies can be conducted to expand the application of the Glycoblotting-based
sulphoglycomics workflow to other biological samples and species. In addition, investigations
into the functional roles of specific sulfated and phosphorylated N-glycans ...