Genetic and Antigenic Evolution of European Swine Influenza A Viruses of HA-1C (Avian-Like) and HA-1B (Human-Like) Lineages in France from 2000 to 2018
Abstract
:1. Introduction
2. Materials and Methods
2.1. Biological Samples, swIAV Detection and Preliminary Molecular Subtyping
2.2. Virus Isolation
2.3. Sequencing
2.4. Phylogenetic Analyses of HA-, NA- and M-Encoding Genes
2.5. Large-Scale Phylogeny of M-Encoding Segment
2.6. Amino Acid Sequence Analyses
2.7. Antigenic Characterization
3. Results
3.1. Relative Proportions of H1avNy and H1huNy swIAVs in France between 2000 and 2018
3.2. Genetic and Antigenic Evolution of HA-1C (H1avNy) swIAVs Isolated in France
3.3. Genetic and Antigenic Evolution of HA-1B (H1huNy) swIAVs Isolated in France
3.4. Genetic Evolution of NA-, M- and other Protein-Encoding Genes from H1av (HA-1C) and H1hu (HA-1B) swIAVs
3.4.1. Evolution of NA-Encoding Segments of N1 and N2 Subtypes
3.4.2. Evolution of M-Encoding Segment
3.4.3. Evolution of Other Internal Protein-Encoding Genomic Segments
3.5. Overview of H1av and H1hu Genotypes Identified in France from 2000 to 2018
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
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Strain (Abbreviated Name) | Subtype | Swine H1 Clade [7] |
---|---|---|
A/Swine/Finistere/2899/82 (Fin2899/82) | H1avN1 | 1C.1 |
A/Swine/Morbihan/0070/05 (Mo0070/05) | H1avN1 | 1C.2.1 |
A/Swine/Cotes d’Armor/0388/09 (CA0388/09) | H1avN1 | 1C.2.1 |
A/Swine/Cotes d’Armor/0186/10 (CA0186/10) | H1avN2 | 1C.2.1 |
A/Swine/France/65-150242/15 (65-150242) | H1avN2 | 1C.2 |
A/Swine/Scotland/410440/94 (Scot/94) | H1huN2 | 1B.1 |
A/Swine/Cotes d’Armor/0214/06 (CA0214/06) | H1huN2 | 1B.1.1 |
A/Swine/Cotes d’Armor/0113/06 (CA0113/06) | H1huN2 | 1B.1.2.3 |
A/Swine/France/22-130212/13 (22-130212) | H1huN2 | 1B.1.2.3 (∆146-147) * |
A/Swine/Cotes d’Armor/0070/10 (CA0070/10) | H1huN1 | 1B.1.2.3 |
A/Swine/Cotes d’Armor/0190/06 (CA0190/06) | H1huN1 | 1B.1.2.3 (∆147) * |
A/Swine/England/117316/86 | clswH1N1 | 1A.1-like |
A/California/04/09 | H1N1pdm | 1A.3.3.2 |
A/Swine/Sarthe/0255/10 | H1N1pdm | 1A.3.3.2 |
Hemagglutination Inhibition Titer to Pig Antiserum Produced against Selected H1av Isolates | ||||||
---|---|---|---|---|---|---|
HA Clade | swIAV Strains (Name or Period of Isolation or Subgroup Within 1C.2.1 Clade of Tested Strains) | A/Sw/Finistere/2899/82 (1C.1-H1avN1) | A/Sw/Morbihan/0070/05 (1C.2.1-H1avN1) | A/Sw/Cotes d’Armor/0388/09 (1C.2.1-H1avN1) | A/Sw/Cotes d’Armor/0186/10 (1C.2.1-H1avN2) | A/Sw/France/65-150242/15 (1C.2-H1avN2) |
1C.1 | A/Sw/Finistere/2899/82 | 2560 | 80 | |||
1C.2.1 | A/Sw/Morbihan/0070/05 | 40 | 640 | |||
A/Sw/Cotes d’Armor/0388/09 | 320 | 640 | ||||
A/Sw/Cotes d’Armor/0186/10 | 320 | 320 | 320 | |||
1C.2 | A/Sw/France/65-150242/15 | 80 | <10 | 2560 | ||
1C.2.1 | 2000–2010 | 215.34 ± 2.85 a | 490.23 ± 1.62 a | 525.01 ± 1.69 a | ||
[40–640] | [160–1280] | [320–1280] | ||||
16 | 26 | 7 | ||||
2011–2014 | 750.18 ± 1.58 b | 879.33 ± 1.83 b | 242.51 ± 1.81 c | |||
[320–1280] | [320–2560] | [<10–640] | ||||
48 | 48 | 30 | ||||
2015–2018 | 336.99 ± 1.96 d | 132.81 ± 1.71 e | 16.59 ± 3.17 f | |||
[40–1280] | [80–320] | [<10–80] | ||||
58 | 58 | 36 | ||||
1C.2 | 2015–2018 | 40 ± 3.32 | 320 ± 18.93 | |||
[10–80] | [<10] | [40–2560] | ||||
3 | 3 | 2 | ||||
1C.2.2 | 2013–2015 | 160 ± 2.67 | 113.14 ± 1.63 | |||
[80–320] | [80–160] | |||||
2 | 2 | |||||
Subgroups within 1C.2.1 2015–2018 | group A | 427.15 ± 1.84 g | 146.72 ± 1.8 ij | 30.07 ± 1.74 k | ||
[160–1280] | [80–320] | [10–80] | ||||
22 | 22 | 15 | ||||
group B | 246.75 ± 1.43 h | 113.14 ± 1.45 i | 9.56 ± 3.66 m | |||
[160–320] | [80–160] | [<10–20] | ||||
6 | 6 | 4 | ||||
group C | 470.32 ± 1.44 g | 201.59 ± 1.63 j | 26.92 ± 1.45 k | |||
[320–640] | [80–320] | [20–40] | ||||
8 | 8 | 6 | ||||
Others (not A, B or C) | 265.52 ± 2.17 h | 110.16 ± 1.57 i | 7.7 ± 4.11 m | |||
[40–1280] | [<10–320] | [<10–40] | ||||
22 | 22 | 11 |
HA Clade | swIAV Strains (Name or Period of Isolation or Subgroup within 1B.1.2.3 Clade of Tested Strains) | Hemagglutination Inhibition Titer to Pig Antiserum Produced Against Selected H1hu Isolates | |||||
---|---|---|---|---|---|---|---|
A/Sw/Scotland/ 410440/94 (1B.1-H1huN2) | A/Sw/Cotes d’Armor/0214/06 (1B.1.1-H1huN2) | A/Sw/Cotes d’Armor/0070/10 (1B.1.2.3-H1huN1) | A/Sw/Cotes d’Armor/0113/06 (1B.1.2.3-D H1huN2) | A/Sw/France/ 22-130212/13 (1B.1.2.3Δ146-147 H1huN2) | A/Sw/Cotes d’Armor/0190/06 (1B.1.2.3Δ147 H1huN1) | ||
1B.1 | A/Sw/Scotland/410440/94 | 2560 | 320 | 160 | 10 | ||
1B.1.1 | A/Sw/Cotes d’Armor/0214/06 | 320 | 1280 | 160 | 10 | ||
1B.1.2.3 | A/Sw/Cotes d’Armor/0070/10 | 1280 | 640 | ||||
A/Sw/Cotes d’Armor/0113/06 | 1280 | 320 | 1280 | 20 | |||
A/Sw/France/ 22-130212/13 | 160 | 320 | 320 | 40 | 1280 | 160 | |
A/Sw/Cotes d’Armor/0190/06 | 40 | 10 | 20 | <10 | 1280 | ||
1B.1.1 | 2000–2010 | 320 ± 2.4 a [80–1280] 6 | 640 ± 1.63 a [320–1280] 5 | 100.79 ± 1.76 f [40–160] 6 | 4.57 ± 4.12 e [<10–20] 5 | ||
1B.1.2.3 | 2000–2010 | 1539.87 ± 1.63 b [640–2560] 15 | 359.19 ± 1.92 a,d [80–640] 12 | 452.55 ± 1.63 [320–640] 2 | 525.01 ± 1.88 d [160–1280] 14 | 40 ± 2.06 b [10–80] 12 | |
2011–2014 | 510.37 ± 3.87 a [40–5120] 49 | 187.44 ± 3.44 d [<10–1280] 38 | 240.8 ± 3.38 d [20–1280] 39 | 61.53 ± 6.27 f [<10–640] 50 | 320 ± 2 a,c [160–1280] 11 | 69.59 ± 3.88 f [<10–1280] 38 | |
2015–2018 | 499.65 ± 4.22 a,d [20–2560] 28 | 160 ± 1.76 [80–320] 4 | 342.97 ± 3.27 d [20–1280] 30 | 77.02 ± 4.81 f [<10–320] 30 | 201.59 ± 2.23 c [40–640] 30 | 134.54 ± 2.39 [40–320] 4 | |
1B.1.2.1 | 2015–2018 | 2031.87 ± 1.49 [1280–2560] 3 | 806.35 ± 1.49 [640–1280] 3 | 253.98 ± 1.49 [160–320] 3 | 126.99 ± 1.49 [80–160] 3 | ||
Subgroups within 1B.1.2.3 2000–2010 | All except groups D | 1741.81 ± 1.65 g [640–2560] 9 | 390.08 ± 2.16 i [80–640] 7 | 452.55 ± 1.9 i [160–1280] 8 | 65.63 ± 1.4 p [40–80] 7 | ||
group D | 1280 ± 1.55 g [640–2560] 6 | 320 ± 1.63 i [160–640] 5 | 640 ± 1.86 g,i [320–1280] 6 | 20 ± 1.63 n [10–40] 5 | |||
Subgroups within 1B.1.2.3 2011–2014 | All except groups D & Δ146-147 | 1612.7 ± 1.66 g [640–5120] 21 | 452.55 ± 1.66 i [160–1280] 16 | 728.82 ± 1.68 j [320–1280] 16 | 181.49 ± 1.94 m [40–640] 22 | 190.27 ± 1.41 [160–320] 4 | 39.45 ± 3.07 p [<10-160] 16 |
group D | 829.98 ± 2.84 g [80–2560] 8 | 12.65 ± 36.19 [<10–160] 2 | 160 ± 6.26 [20–640] 3 | 226.27 ± 2.67 i,m [40–640] 8 | 3.16 ± 5.09 [<10–10] 2 | ||
Δ146-147 | 125.53 ± 1.76 h [40–320] 20 | 121.26 ± 1.99 h [40–320] 20 | 105.56 ± 2.21 h [20–320] 20 | 11.12 ± 5.17 k [<10–40] 20 | 430.69 ± 1.97 j [160–1280] 7 | 149.29 ± 2.1 h [40–1280] 20 | |
Subgroups within 1B.1.2.32015–2018 | All except group Δ146-147 | 1280 ± 1.79 g [320–2560] 18 | 685.94 ± 1.81 j [160–1280] 20 | 190.27 ± 1.72 m [80–320] 20 | 144.2 ± 1.98 m [40–320] 20 | ||
Δ146-147 | 91.9 ± 2.2 h [20–320] 10 | 126.99 ± 1.49 [80–160] 3 | 85.74 ± 2.14 h [20–160] 10 | 12.62 ± 3.92 k [<10–40] 10 | 393.97 ± 1.77 j [160–640] 10 | 201.59 ± 1.49 [160–320] 3 |
SwIAV Proteins | PB2 | PB1 | PB1-F2 | PA | PA-X | NP | M1 | M2 | NS1 | NS2 |
---|---|---|---|---|---|---|---|---|---|---|
Protein length (in amino acid) | 759 | 757 | 90 | 716 | 260 | 498 | 252 | 97 | 230 | 121 |
Nb of conserved residues (%) | 590 (77.7%) | 552 (72.9%) | 8 (8.9%) | 521 (72.8%) | 158 (60.8%) | 406 (81.5%) | 211 (83.7%) | 48 (49.5%) | 98 (42.6%) | 82 (67.8%) |
Mean Entropy | 0.055 | 0.068 | 0.379 | 0.062 | 0.117 | 0.040 | 0.019 | 0.157 | 0.187 | 0.082 |
Max. Entropy | 1.273 | 1.318 | 1.827 | 1.391 | 1.268 | 0.986 | 0.711 | 1.493 | 1.419 | 1.016 |
Entropy st. dev. | 0.159 | 0.176 | 0.364 | 0.168 | 0.236 | 0.123 | 0.065 | 0.307 | 0.274 | 0.178 |
Subtype | Protein-Encoding Genomic Segment | Frequency Nb (%) | Corresponding Genotype Previously Described in [13] * | |||||||
---|---|---|---|---|---|---|---|---|---|---|
HA [7] | NA | PB2 | PB1 | PA | NP | M | NS | |||
H1avN1 | 1C.2.1 | N1-EA | EA | EA | EA | EA | swEA | EA | 34 (21.1) | A |
1C.2.1 | N1-EA | EA | EA | EA | EA | swEU | EA | 55 (34.2) | A | |
1C.2.2 | N1-EA | EA | EA | EA | EA | swEA | EA | 3 (1.9) | A | |
1C.2.3 | N1-EA | EA | EA | EA | EA | swEU | EA | 2 (1.2) | A | |
H1avN2 | 1C.2 | N2-Gent | EA | EA | EA | EA | Dk-like | EA | 2 (1.2) | D |
1C.2 | N2-Gent | pdm | pdm | pdm | pdm | pdm | pdm | 1 (0.6) | T | |
1C.2.1 | N2-Scot | EA | EA | EA | EA | swEA | EA | 3 (1.9) | G | |
1C.2.1 | N2-Scot | EA | EA | EA | EA | swEU | EA | 2 (1.2) | G | |
1C.2.1 | N2hu | EA | EA | EA | EA | swEA | EA | 1 (0.6) | I | |
1C.2.1 | N2hu | EA | EA | EA | EA | pdm | EA | 2 (1.2) | Not described | |
H1huN2 | 1B.1.1 | N2-Scot | EA | EA | EA | EA | swEA | EA | 1 (0.6) | C |
1B.1.2.3 | N2-Scot | EA | EA | EA | EA | swEU | EA | 29 (18.0) | C | |
1B.1.2.3 | N2-Scot | EA | EA | EA | EA | swEA | EA | 9 (5.6) | C | |
1B.1.2.3 (Δ146-147) | N2-Scot | EA | EA | EA | EA | swEA | EA | 5 (3.1) | C | |
1B.1.2.3 (Δ146-147) | N2-Scot | EA | EA | EA | EA | swEU | EA | 4 (2.5) | C | |
1B.1.2.1 | N2-Gent | EA | EA | EA | EA | swEU | EA | 4 (2.5) | E | |
H1huN1 | 1B.1.2.3 | N1-EA | EA | EA | EA | EA | swEU | EA | 4 (2.5) | H |
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Chastagner, A.; Hervé, S.; Quéguiner, S.; Hirchaud, E.; Lucas, P.; Gorin, S.; Béven, V.; Barbier, N.; Deblanc, C.; Blanchard, Y.; et al. Genetic and Antigenic Evolution of European Swine Influenza A Viruses of HA-1C (Avian-Like) and HA-1B (Human-Like) Lineages in France from 2000 to 2018. Viruses 2020, 12, 1304. https://doi.org/10.3390/v12111304
Chastagner A, Hervé S, Quéguiner S, Hirchaud E, Lucas P, Gorin S, Béven V, Barbier N, Deblanc C, Blanchard Y, et al. Genetic and Antigenic Evolution of European Swine Influenza A Viruses of HA-1C (Avian-Like) and HA-1B (Human-Like) Lineages in France from 2000 to 2018. Viruses. 2020; 12(11):1304. https://doi.org/10.3390/v12111304
Chicago/Turabian StyleChastagner, Amélie, Séverine Hervé, Stéphane Quéguiner, Edouard Hirchaud, Pierrick Lucas, Stéphane Gorin, Véronique Béven, Nicolas Barbier, Céline Deblanc, Yannick Blanchard, and et al. 2020. "Genetic and Antigenic Evolution of European Swine Influenza A Viruses of HA-1C (Avian-Like) and HA-1B (Human-Like) Lineages in France from 2000 to 2018" Viruses 12, no. 11: 1304. https://doi.org/10.3390/v12111304