Molecular Epidemiology of Rotavirus A in Calves: Evolutionary Analysis of a Bovine G8P[11] Strain and Spatio-Temporal Dynamics of G6 Lineages in the Americas
Abstract
:1. Introduction
2. Materials and Methods
2.1. Farms, Calves, and Sample Collection
2.2. RVA Reference Strains and Antigen Detection
2.3. RNA Extraction and G/P Genotyping
2.4. Sequencing of VP7 and VP8*
2.5. Sequencing of RVA Gene Segments
2.6. Sequence Analysis, Genotype Assignment, and Percentage Identity
2.7. Substitution Models and Phylogenetic Analyses
2.8. Determination of G8 Lineages
2.9. Phylodynamic and Phylogeographic Analyses of G6 RVA Strains
2.10. GenBank Accession Numbers
2.11. Statistical Analyses
3. Results
3.1. Frequency of RVA Infections
3.2. Genotyping of RVA Field Strains
3.3. Genome Analysis of the G8P[11] RVA Strain
3.4. Phylogenetic Analysis of the G8P[11] RVA Strain
3.5. G8 Lineages and Genetic Distance Analysis
3.6. Phylogenetic Analyses of VP7 and VP8* among G6 and G10 Strains
3.7. Phylogeny of G6 RVA Strains According to Production Systems and Farm Location
3.8. Phylodynamic and Phylogeographic Analyses of G6(III) and G6(IV) Lineages
4. Discussions
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Genotypes and G/P Combinations | Beef (n = 33) | Dairy (n = 34) | Dairy Farm DR * | |||
---|---|---|---|---|---|---|
2009 | 2010 | 2011 | ||||
No. (%) | p-Value FDR & | No. | ||||
G6(III) | 0 (0.0) | 15 (44.1) | <0.0001 | |||
G6(IV) | 30 (90.9) | 4 (11.8) | <0.0001 | |||
G8 | 0 (0.0) | 1 (2.9) | 0.1734 | |||
G10 | 0 (0.0) | 3 (8.8) | 0.0016 | |||
P[5] | 32 (97.0) | 7 (20.6) | <0.0001 | |||
P[11] | 1 (3.0) | 24 (70.6) | <0.0001 | |||
G6(III)P[5] | 0 (0.0) | 1 (2.9) | 0.2033 | |||
G6(IV)P[5] | 30 (90.9) | 3 (8.8) | <0.0001 | 7 | ||
G6(III)P[11] | 0 (0.0) | 14 (41.2) | <0.0001 | 5 | ||
G8P[11] | 0 (0.0) | 1 (2.9) | 0.2049 | |||
G10P[11] | 0 (0.0) | 3 (8.8) | 0.0057 | 2 | ||
GXP[5] | 2 (6.1) | 2 (5.9) | 0.9731 | |||
GXP[11] | 0 (0.0) | 2 (5.9) | 0.0639 | 2 | ||
G6(IV) + G10P[11] | 1 (3.0) | 2 (5.9) | 0.6841 | |||
G6(IV) + G10P[5] | 0 (0.0) | 1 (2.9) | 0.2033 | |||
G6(III) + G10P[11] | 0 (0.0) | 2 (5.9) | 0.0553 | |||
G6(IV) + P[5 + 11] | 0 (0.0) | 1 (2.9) | 0.2049 | |||
G6(IV) + G10P[5 + 11] | 0 (0.0) | 2 (5.9) | 0.0553 | |||
Mixed genotypes (total) | 1 (3.0) | 8 (23.5) | 0.0553 |
Genome Segment (Protein) | Sequenced Fragment † (bp) | Position * | ORF Coverage (%) | Genotype # | Most Similar Strains after Nucleotide BLAST Search | Highest Identity (%) & | Host of Origin | Country |
---|---|---|---|---|---|---|---|---|
1 (VP1) | 3215 | 46-3260 | 98 | R5 | RVA/Cow-wt/ARG/B383/1998/G15P[11] | 98 | Cattle | Argentina |
2 (VP2) | 2643 | 17-2659 | 100 | C2 | RVA/Alpaca-wt/PER/1115/2010/G8P[1] | 96 | Alpaca | Peru |
3 (VP3) | 1518 | 50-1567 | 61 | M2 | RVA/Guanaco-wt/ARG/Chubut/1999/G8P[14] | 91 | Guanaco | Argentina |
4 (VP4) | 2142 | 163-2304 | 92 | P[11] | RVA/Cow-wt/ARG/B1625_B_BA/2001/G10P[11] | 95 | Cattle | Argentina |
5 (NSP1) | 1427 | 83-1509 | 95 | A13 | RVA/Cow-wt/ARG/B383/1998/G15P[11] | 94 | Cattle | Argentina |
6 (VP6) | 1167 | 51-1217 | 98 | I2 | RVA/Cow-wt/URY/LVMS3206/2016/GXP[11] | 93 | Cattle | Uruguay |
7 (VP7) | 898 | 49-946 | 92 | G8 | RVA/Goat-wt/ARG/0040/2011/G8P[1] | 97 | Goat | Argentina |
8 (NSP2) | 954 | 47-1000 | 100 | N2 | RVA/Cow-wt/URY/LVMS3053/2016/G10P[X] | 98 | Cattle | Uruguay |
9 (NSP3) | 933 | 35-967 | 100 | T6 | RVA/Cow-wt/URY/LVMS2625/2016/G10P[11] | 99 | Cattle | Uruguay |
10 (NSP4) | 528 | 42-569 | 100 | E12 | RVA/Cow-wt/ARG/B3700/2008/G6P[5] | 99 | Cattle | Argentina |
11 (NSP5) | 597 | 22-618 | 100 | H3 | RVA/Cow-wt/ARG/B383/1998/G15P[11] | 99 | Cattle | Argentina |
Strains | Genotype Constellation | VP7 (%) * | VP4 (%) | VP6 (%) | VP1 (%) | VP2 (%) | VP3 (%) | NSP1 (%) | NSP2 (%) | NSP3 (%) | NSP4 (%) | NSP5 (%) | Shared Genotypes |
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
RVA/Cow-wt/ARG/4385VT_D_BA/2008/G8P[11] | G8 | P[11] | I2 | R5 | C2 | M2 | A13 | N2 | T6 | E12 | H3 | ||
RVA/Cow-wt/ARG/B383/1998/G15P[11] | Bovine | G15 | P[11] (94/94) | I2 (84/97) | R5 (98/100) | C2 (93/99) | M2 (88/95) | A13 (94/94) | N2 (95/98) | T6 (88/96) | E12 (97/99) | H3 (99/100) | 10 |
RVA/Guanaco-wt/ARG/Rio_Negro/1998/G8P[1] | Artiodactyl bovine-like | G8 (97/99) | P[1] | I2 (91/99) | R5 (96/99) | C2 (85/98) | M2 (84/92) | A11 | N2 (87/95) | T6 (89/97) | E12 (94/97) | H3 (93/94) | 9 |
RVA/Goat-wt/ARG/0040/2011/G8P[1] | Artiodactyl bovine-like | G8 (97/98) | P[1] | I2 (87/97) | R5 (98/99) | C2 (96/100) | M2 (88/94) | A3 | N2 (95/98) | T6 (94/98) | E12 (96/99) | H3 (93/94) | 9 |
RVA/Guanaco-wt/ARG/Chubut/1999/G8P[14] | Artiodactyl bovine-like | G8 (97/97) | P[14] | I2 (91/99) | R5 (93/99) | C2 (85/98) | M2 (91/95) | A3 | N2 (91/97) | T6 (98/99) | E12 (96/100) | H3 (96/97) | 9 |
RVA/Rhesus-tc/USA/PTRV/1990 | Artiodactyl bovine-like | G8 (96/98) | P[1] | I2 (91/99) | R2 | C2 (85/98) | M2 (85/92) | A3 | N2 (94/99) | T6 (95/98) | E2 | H3 (97/99) | 9 |
RVA/Human-tc/KEN/B12/1987/G8P[1] | Human bovine-like | G8 (96/99) | P[1] | I2 (90/99) | R2 | C2 (86/98) | M2 (84/92) | A3 | N2 (88/96) | T6 (97/98) | E2 | H3 (96/98) | 9 |
RVA/Alpaca-wt/PER/562/2010/G8P[14] | Artiodactyl bovine-like | G8 (95/98) | P[14] | I2 (90/99) | R5 (91/98) | C2 (96/100) | M2 (80/88) | A17 | N2 (96/97) | T6 (94/98) | E3 | H3 (97/99) | 8 |
RVA/Cow-wt/BRA/Y136/2017/G8P[11] | Bovine | G8 (87/94) | P[11] (71/71) | I2 (88/98) | R5 (89/99) | C2 (84/96) | M2 (89/93) | A3 | N2 (87/98) | T9 | E2 | H3 (96/98) | 8 |
RVA/Alpaca-wt/PER/1115/2010/G8P[1] | Artiodactyl bovine-like | G8 (88/93) | P[1] | I2 (91/100) | R2 | C2 (96/99) | M2 (84/92) | A17 | N2 (92/98) | T6 (87/96) | E3 | H3 (97/100) | 7 |
RVA/Cow-wt/ZAF/1604/2007/G8P[1] | Bovine | G8 (87/98) | P[1] | I2 (91/99) | R2 | C2 (85/98) | M2 (85/91) | A3 | N2 (94/97) | T6 (89/97) | E2 | H3 (95/97) | 7 |
RVA/Cow–tc/NGA/NGRBg8/1998/G8P[1] | Bovine | G8 (85/96) | P[1] | I2 (87/99) | R2 | C2 (85/98) | M2 (81/91) | A11 | N2 (88/97) | T6 (94/98) | E2 | H3 (95/98) | 7 |
RVA/Cow-tc/THA/A5-10/1988/G8P[1] | Bovine | G8 (85/96) | P[1] | I2 (92/99) | R2 | C2 (84/98) | M2 (82/91) | A11 | N2 (87/96) | T6 (92/98) | E2 | H3 (95/97) | 7 |
RVA/Cow-tc/CHN/DQ-75/2008/G10P[11] | Bovine | G10 | P[11] (72/72) | I2 (91/99) | R2 | C2 (84/98) | M2 (82/90) | A3 | N2 (94/98) | T6 (92/97) | E2 | H3 (95/97) | 7 |
RVA/Human–tc/NGA/HMG035/1999/G8P[1] | Human bovine-like | G8 (85/96) | P[1] | I2 (87/99) | R2 | C2 (85/98) | M2 (81/91) | A11 | N2 (88/97) | T6 (94/98) | E2 | H3 (95/98) | 7 |
RVA/Human-wt/PRY/492SR/2004/G8P[1] | Human bovine-like | G8 (87/94) | P[1] | I2 (87/97) | R2 | C2 (85/98) | M1 | -- | N2 (95/96) | T6 (95/97) | E12 (96/99) | H3 (99/99) | 7 |
RVA/Human-wt/ITA/PR1300/2004/G8P[14] | Human bovine-like | G8 (96/98) | P[14] | I2 (87/99) | R2 | C2 (84/98) | M2 (82/90) | A3 | N2 (88/97) | T6 (90/98) | E2 | H3 (97/100) | 7 |
RVA/Human-wt/HUN/BP1062/2004/G8P[14] | Human bovine-like | G8 (83/95) | P[14] | I2 (91/99) | R2 | C2 (84/97) | M2 (81/91) | A11 | N2 (87/97) | T6 (91/98) | E2 | H3 (95/97) | 7 |
RVA/Sheep-tc/ESP/OVR762/2002/G8P[14] | Artiodactyl bovine-like | G8 (94/98) | P[14] | I2 (90/99) | R2 | C2 (84/98) | M2 (81/90) | A11 | N2 (88/96) | T6 (91/98) | E2 | H3 (97/98) | 7 |
RVA/Vicugna-wt/ARG/C75/2010/G8P[14] | Artiodactyl bovine-like | G8 (97/99) | P[14] | I2 (90/99) | R2 | C2 (85/96) | M2 (92/96) | -- | N2 (92/97) | T6 (97/98) | E3 | -- | 6 |
RVA/Human-wt/GHA/GH018-08/2008/G8P[6] | Human bovine-like | G8 (85/96) | P[6] | I2 (91/99) | R2 | C2 (85/98) | M2 (84/92) | A2 | N2 (89/97) | T2 | E2 | H3 (97/99) | 6 |
RVA/Dog-wt/GER/88977/2013/G8P[1] | Dog bovine-like | G8 (95/98) | P[1] | I2 (92/99) | -- & | C2 (85/99) | -- | A3 | N2 (88/97) | T6 (90/98) | E2 | H3 (97/99) | 6 |
VP7 ORF Sequence Datasets | |||
Parameter | RVA-G6 | RVA-G6(III) | RVA-G6(IV) |
n | 198 | 71 | 127 |
Sampling time interval | 1971–2018 | 1997–2018 | 1971–2016 |
Evolutionary rate (Mean s/s/y) & * | 1.24 × 10−3 (9.97 × 10−4–1.52 × 10−3) | 1.17 × 10−3 (6.49 × 10−4–1.72 × 10−3) | 1.26 × 10−3 (9.44 × 10−4–1.58 × 10−3) |
Mean TMRCA # * for G6 strains | 1853 (1766–1935) | NA | NA |
Mean TMRCA # * for G6(III) lineage | 1981 (1963–1989) | 1982 (1971–1992) | NA |
Mean TMRCA # * for G6(IV) lineage | 1940 (1919–1959) | NA | 1945 (1926–1962) |
Country † (probability) | USA (0.57) ARG (0.23) | ARG (0.99) | USA (0.55) BRA (0.29) |
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Louge Uriarte, E.L.; Badaracco, A.; Spetter, M.J.; Miño, S.; Armendano, J.I.; Zeller, M.; Heylen, E.; Späth, E.; Leunda, M.R.; Moreira, A.R.; et al. Molecular Epidemiology of Rotavirus A in Calves: Evolutionary Analysis of a Bovine G8P[11] Strain and Spatio-Temporal Dynamics of G6 Lineages in the Americas. Viruses 2023, 15, 2115. https://doi.org/10.3390/v15102115
Louge Uriarte EL, Badaracco A, Spetter MJ, Miño S, Armendano JI, Zeller M, Heylen E, Späth E, Leunda MR, Moreira AR, et al. Molecular Epidemiology of Rotavirus A in Calves: Evolutionary Analysis of a Bovine G8P[11] Strain and Spatio-Temporal Dynamics of G6 Lineages in the Americas. Viruses. 2023; 15(10):2115. https://doi.org/10.3390/v15102115
Chicago/Turabian StyleLouge Uriarte, Enrique L., Alejandra Badaracco, Maximiliano J. Spetter, Samuel Miño, Joaquín I. Armendano, Mark Zeller, Elisabeth Heylen, Ernesto Späth, María Rosa Leunda, Ana Rita Moreira, and et al. 2023. "Molecular Epidemiology of Rotavirus A in Calves: Evolutionary Analysis of a Bovine G8P[11] Strain and Spatio-Temporal Dynamics of G6 Lineages in the Americas" Viruses 15, no. 10: 2115. https://doi.org/10.3390/v15102115
APA StyleLouge Uriarte, E. L., Badaracco, A., Spetter, M. J., Miño, S., Armendano, J. I., Zeller, M., Heylen, E., Späth, E., Leunda, M. R., Moreira, A. R., Matthijnssens, J., Parreño, V., & Odeón, A. C. (2023). Molecular Epidemiology of Rotavirus A in Calves: Evolutionary Analysis of a Bovine G8P[11] Strain and Spatio-Temporal Dynamics of G6 Lineages in the Americas. Viruses, 15(10), 2115. https://doi.org/10.3390/v15102115