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. 2021 Dec 9;13(12):2469.
doi: 10.3390/v13122469.

Evolutionary Dynamics of Type 2 Porcine Reproductive and Respiratory Syndrome Virus by Whole-Genome Analysis

Jiahui Guo  1   2 , Zimin Liu  1   2 , Xue Tong  1   2 , Zixin Wang  1   2 , Shangen Xu  1   2 , Qian Chen  1   2 , Junwei Zhou  1   2 , Liurong Fang  1   2 , Dang Wang  1   2 , Shaobo Xiao  1   2
Affiliations

Evolutionary Dynamics of Type 2 Porcine Reproductive and Respiratory Syndrome Virus by Whole-Genome Analysis

Jiahui Guo et al. Viruses. .

Abstract

Porcine reproductive and respiratory syndrome virus (PRRSV), an important pathogen in the swine industry, is a genetically highly diverse RNA virus. However, the phylogenetic and genomic recombination properties of this virus are not yet fully understood. In this study, we performed an integrated analysis of all available whole-genome sequences of type 2 PRRSV (n = 901) to reveal its evolutionary dynamics. The results showed that there were three distinct phylogenetic lineages of PRRSV in their distribution patterns. We identified that sublineage 2.7 (L2.7), associated with a NADC30 cluster, had the highest substitution rate and higher viral genetic diversity, and inter-lineage recombination is observed more frequently in L2.7 PRRSV compared to other sublineages. Most inter-lineage recombination events detected are observed between L2.7 PRRSVs (as major parents) and L3.4 (a JXA1-R-related cluster)/L3.7 (a WUH3-related cluster) PRRSVs (as minor parents). Moreover, the recombination hotspots are located in the structural protein gene ORF2 and ORF4, or in the non-structural protein gene nsp7. In addition, a GM2-related cluster, L3.2, shows inconsistent recombination modes compared to those of L2.7, suggesting that it may have undergone extensive and unique recombination in their evolutionary history. We also identified several amino acids under positive selection in GP2, GP4 and GP5, the major glycoproteins of PRRSV, showing the driving force behind adaptive evolution. Taken together, our results provide new insights into the evolutionary dynamics of PPRSV that contribute to our understanding of the critical factors involved in its evolution and guide future efforts to develop effective preventive measures against PRRSV.

Keywords: Bayesian evolution; lineages; molecular epidemiology; porcine reproductive and respiratory syndrome virus; recombination.

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Conflict of interest statement

The authors declare no conflict of interest.

Figures

Figure 1
Figure 1
Phylogenetic and sequence distance analyses of the PRRSV (A) Maximum-likelihood phylogenetic tree of PRRSV genome and LDV as an outgroup, colored according to the gene type, type 1 PRRSV are shown in blue, and type 2 PRRSV are shown in pink. (B) Maximum-likelihood phylogenetic tree analyses of type 2 PRRSV, the clade colors indicate lineages and sublineages. Three main genetic lineages were distinguished, lineages 2 and 3 containing further clades 2.1–2.7 and 3.1–3.7, respectively. Other information is displayed next to the phylogenetic tree (Number of the virus, timespan in years, representative strains). The red star indicates two recombination lineages. Of the total L2 and L3, n = 99, n = 31, n = 17, n = 22, n = 117, n = 18 and n = 105 were classified into L2.1 to L2.7 and n = 37, n = 25, n = 45, n = 107, n = 29, n = 49 and n = 103 were classified into L3.1 to L3.7. (C) The nucleotide sequence divergence (p-distance) between Type 2 PRRSV intra-group distance and inter-group distance was used for comparison.
Figure 2
Figure 2
The number and diversity of PRRSV during 2006–2020 The bar chart shows the number of PRRSV sequences obtained by four sublineages during 2006–2020. The line chart shows the diversity of PRRSV sequences obtained by four sublineages during 2006–2020. The number and diversity of samples positive for PRRSV are indicated by different colored lines, respectively.
Figure 3
Figure 3
Bayesian spatiotemporal speculation of sublineages 2.7, 3.3, 3.4, and 3.7 PRRSV (A–D) Bayesian skyline population dynamic analysis. The red line indicates the mean of the size and genetic diversity of the population. The blue line indicates the median of the size and genetic diversity of the population. The dotted line indicates the 95% HPD of the size and genetic diversity of the population.
Figure 4
Figure 4
Schematic representation of PRRSV GP5 and positively selected sites. (A) Schematic diagram of the MEMSAT3 and MEMSATSVM predictions for PRRSV GP2, GP4 and GP5. Topology of unprocessed PRRSV GP2, GP4 and GP5 with signal peptide, ectodomain, a hydrophobic transmembrane stretch and a cytosolic/virus-internal endodomain. Red shows the location of conserved N-glycosylation sites. The lower table shows identified positively selected sites within four lineages. (B) Site conservation of amino acid sequences of PRRSV GP2, GP4 and GP5.
Figure 5
Figure 5
Lineage recombination mode of main sublineages (A–F) Maps of inter-lineage recombination patterns. The horizontal axis shows the 16 sublineages as major parents in Figure 5, the vertical axis shows the 16 sublineages as minor parents in Figure 5. The intensity of the color depends on the number of recombination events and the numbers in the heat map identify the number of recombination events.
Figure 6
Figure 6
Frequency of recombination events in whole-length genome structure, regarding VR-2332, in which the positions and boundaries of the major ORFs and NSPs within ORF1a and ORF1b are shown. The intensity of the color depends on the frequency of recombination events in different ORFs and NSPs. Data are indicated below the whole-length genome structure.
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