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Article

New Circulating Variants of SARS-CoV-2 in Asturias During the Period (2022–2024)

by
José María González-Alba
1,2,
Zulema Pérez Martínez
1,2,
Susana Rojo-Alba
1,2,
Cristina Ochoa Varela
1,2,
Juan Gómez de Oña
1,3,
Mercedes Rodríguez Pérez
1,2,
Santiago Melón García
1,2 and
Marta Elena Álvarez-Argüelles
1,2,*
1
Unit of Virology, Microbiology Department, Hospital Universitario Central de Asturias, 33011 Oviedo, Spain
2
Instituto de Investigación Sanitario del Principado de Asturias (ISPA), 33011 Oviedo, Spain
3
Genetic Department, Hospital Universitario Central de Asturias, 33011 Oviedo, Spain
*
Author to whom correspondence should be addressed.
Viruses 2025, 17(12), 1531; https://doi.org/10.3390/v17121531 (registering DOI)
Submission received: 23 October 2025 / Revised: 14 November 2025 / Accepted: 20 November 2025 / Published: 22 November 2025
(This article belongs to the Section Human Virology and Viral Diseases)
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Abstract

The ability of a virus to adapt is key to its survival, and this is achieved through mutation, which allows the virus to change and adapt to new environments. To capture the full extent of SARS-CoV-2 diversity in Asturias, samples obtained from nasopharyngeal swabs were characterised using whole-genome sequencing. Between 2020 and July 2024, a total of 4001 sequences were analysed and 5302 mutations were identified. An increase in the positivity rate was observed between 2022 and 2024 in children under 1 year of age. During this period, 55 new circulating variants belonging to 41 pangolin lineages were detected: 24 originated throughout the world and 31 in Asturias (10 detected only in the region, 8 in the rest of Spain, and 13 around the world). A total of 31 new non-synonymous mutations were fixed in the viral population 250 ± 46 (93–620) days after their appearance. During seasonal SARS-CoV-2 circulation, surveillance systems developed during the pandemic continue to detect new indigenous and imported variants without indicating an increase in severity.

1. Introduction

Since the start of the pandemic, the rate of mutation of SARS-CoV-2 has been decreasing [1]. However, the number of SARS-CoV-2 infections continues to rise, and outbreaks still occur despite the majority of the population being vaccinated. It is fortunate that the current fatality rate due to COVID-19 is lower than it was in the initial phase of the pandemic [1]. This is because the causative agent of COVID-19, SARS-CoV-2, is constantly evolving as it spreads from person to person, with new sub-lineages emerging all the time. Consequently, the genome of the virus should be analysed in order to identify the viral strains in circulation and to investigate their dissemination both geographically and worldwide. Furthermore, the comprehensive sequencing of the entire viral genome associated with infection is a valuable tool with which to elucidate outbreak dynamics [2,3]. Our group started sequencing the whole genome of the SARS-CoV-2 samples to identify the genotypes of the virus circulating in our area and to analyse genomic diversity, the types of mutations, and the emergence of new variants of SARS-CoV-2 by June 2022 [4,5,6]. In June 2022, the Spanish Ministry of Health proposed infection control and surveillance measures that reduced pressure on cases of mild or asymptomatic illness and their contacts [5]. Consequently, all respiratory viral illnesses, including those caused by SARS-CoV-2, must now be considered as posing the same risk. This study monitored and tracked the SARS-CoV-2 epidemic in Asturias during the post-COVID-19 period (July 2022 to July 2024).

2. Materials and Methods

2.1. Sample Collection

From July 2022 to July 2024, 2268 samples (1733 recorded from March 2020 to July 2022) obtained from nasopharyngeal swabs from individuals infected with SARS-CoV-2 were characterised by means of the whole-genome sequencing (WGS) method and were uploaded to GISAID. Data on age, sex, date, and pangolin lineage were collected (Supplementary Table S1).

2.2. WGS

Selected SARS-CoV-2 positive samples were sequenced using the Ion AmpliSeq SARS-CoV-2 research panel (Thermo Fisher Scientific, Waltham, MA, USA) following the instructions set out in the manufacturer’s user guide. Libraries were prepared on the Ion Chef system in accordance with the guidelines outlined in the user’s guide. Subsequently, the amplified samples were subjected to sequencing using Ion 540 chips with the Ion S5 system. This process was carried out in strict accordance with the manufacturer’s user guide.
The obtained sequences were uploaded to the GISAID database (https://www.gisaid.org/).

2.3. Classification/Characterisation

The SARS-CoV-2 genomes were aligned using MAFFT (https://mafft.cbrc.jp/alignment/software/ (accessed on 30 January 2022)) and then manually curated using MEGA 7 (https://www.megasoftware.net/ (accessed on 16 June 2022)). The nucleotide substitution model (GTR + I) was determined using the Akaike information criterion with jModelTest v2.1.10 (https://github.com/ddarriba/jmodeltest2 (accessed on 16 June 2022)). Phylogenetic trees were reconstructed by ML with FastTree (http://www.microbesonline.org/fasttree/ (accessed on 16 June 2022)) for large trees or IQ-TREE (http://www.iqtree.org/ (accessed on 22 February 2022)). Bootstrap values were estimated using the SH test and ultrafast bootstrap. The Wuhan-Hu-1 reference genome (MN908947.3) was used as an outgroup.
The coding regions (ORF1a, RdRp(RNA-dependent RNA polymerase), ORF1ab, S, ORF3a, E, M, ORF6, ORF7a, ORF7b, ORF8, N, and ORF10) were extracted individually from the alignments. Subsequently, the nucleotides in the coding regions were converted to their corresponding encoded amino acid residues (SeaView https://doua.prabi.fr/software/seaview (accessed on 22 February 2013)). The retrieval of SNPs was conducted within the aligned regions, in accordance with the reference genome. Non-synonymous mutations with a frequency of more than 5% (number of strains with a specific mutation/total number of strains) were considered the majority in the population and were used in subsequent analyses. A mutation is considered to have become fixed in the population when it reaches a frequency of 95% (number of strains with a specific mutation/total number of strains in a month) and remains until today.
A dated phylogeny was reconstructed using Bayesian inference via a Markov chain Monte Carlo (MCMC) framework in BEAST v1.10 (https://beast.community/ (accessed on 20 April 2022)). An uncorrelated relaxed clock model was employed to estimate the time to the most recent common ancestor (TMRCA). MCMC chains were run for 100 million steps (sampling every 10,000). Convergence was evaluated using Tracer v1.7.1 (https://beast.community/tracer (accessed on 19 November 2025)).The trees were summarised using TreeAnnotator v1.8.4 after the first 10% were discarded as burn-in and then visualised in FigTree v1.4.4 (http://tree.bio.ed.ac.uk/software/figtree/ (accessed on 15 November 2021)).
A phylogeographic analysis was performed in the BEAST programme. An asymmetric substitution model and an uncorrelated relaxed molecular clock were applied to the Bayesian stochastic search variable selection (BSSVS) method to identify the number of non-zero transition rates between states.
Possible new lineages were defined for study based on SNPs and monophyletic clades with more than five sequences (according to the proposed dynamic nomenclature for SARS-CoV-2 lineages at https://github.com/cov-lineages/pango-designation (accessed on 8 June 2022)). Lineage-specific mutations were obtained by analysing WGS genomes against the Wuhan-Hu-1 reference genome (MN908947.3). The pattern of mutations specific to the possible new lineages was sought in the sequences obtained from GISAID to analyse their global distribution.
The diversity (D = 1 − ∑f2) of the pangolin lineages was analysed, taking into account the frequencies (f) of all types.

3. Results

A total of 4001 sequences were analysed (randomly selected from 533,769 positive SARS-CoV-2 samples with ct < 27) in Asturias (northern Spain) between 2020 and July 2024. The positivity rate of SARS-CoV-2 by age in the pre-Omicron and Omicron periods is shown in Table 1.

3.1. Mutations

During these four years, 5302 amino acid changes were found in the 9769 amino acids that make up the complete genome. Of these, 157 (3% of mutations and 1.6% of the total genome) occurred in more than 5% of the viral population. In the same period, 158 (1.6% of the genome) mutations were found in Spain, and 116 (1.2%) were found worldwide. (Supplementary Table S2, Table 2).
The estimated relative mutation rates for the codon were 1.34 for the third position, 0.81 for the second position, and 0.85 for the first position.
The estimated mean rate was 9.20 × 10−4 (8.07–10.00) replacements per site, per year in the 2022–2024 period, compared to 7.92 × 10−4 (7.30–8.54) replacements per site, per year in the 2020–2022 period.
Between 2022 and 2024, 88 new non-synonymous mutations (0.9% of the genome) occurred in over 5% of the viral population, of which 31 are currently maintained and were fixed 250 ± 46 (93–620) days after their appearance. Between March 2020 and July 2022, 105 (1.1% of the genome) major mutations were identified, of which 51 were fixed after 344 ± 94 (0–1209) days (Supplementary Table S3, Table 3, Figure 1).
In contrast to Asturias, as of June 2024, 50 mutations have been established worldwide: 29 in gene S, 8 in ORF1a, 4 in the N gene, 2 in the M gene, 3 in ORF1ab, and 1 in RdRp, ORF3a, the E gene, and ORF6 (Supplementary Table S2).
The P323L mutation (RdRp gene) and the D614G mutation (S gene) appeared in over 5% of the viral population by day 0. The following mutations were delayed two months: M gene-A63T, M gene-Q19E, ORF1a gene_P3395H, ORF1ab gene_I643V, S gene_N679K, S gene_N764K, S gene_N969K, S gene_Q954H, and S gene_S373P.
Of the 82 mutations fixed, 41 occurred between February and June 2022, and 41 (10 of which appeared in the first period: N_Q229K, ORF1a_A2710T, ORF1a_T4175I, ORF6_D61L, S_A264D, S_E484A, S_G446S, S_L216F, and S_R21T, S_S939F) between January and June 2024 (Figure 2).

3.2. Lineages

From June 2022 to July 2024, 313 pangolin lineages were identified in Asturias, of which BA.5.1 (6.1%), DV.7.1 (5.8%),and BQ.1.1 (5.5%)accounted for over 5% of cases (see Supplementary Table S4, Figure 3). In this period, diversity reached a maximum of 0.980. During the first period (June 2020–2022), diversity was 0.929, and 111 lineages were identified.
From 2020 to 2024, 55 new circulating variants (NCVs) belonging to 41 pangolin lineages were detected (Supplementary Table S5). The distribution of the 91 mutations gained from these NCVs was 21 in NSP3 (ORF1a gene), 17 in S, 9 in ORF3a, 8 in NSP2, and 6 in NSP14 (Supplementary Table S5, Table 4).
Of these 55 NCVs, 24 were circulating throughout the world, with 2 (BF.5 + S_D80E + S_A701V + NSP1_G94C and JN.1.16.1 + NSP3_S1428L + NSP5_K90R + NSP6_L37F + S_F59S) mainly in Asturias, during 59 ± 16 (6–169) days; only variant XBB.1.5.8 + NSP14_V328F in March 2023 belonged to the same transmission clade in the region (Figure 4). The other 31 originated in Asturias: 10 of them were only detected in the region during 92 ± 20 (31–129) days, 8 in the rest of Spain during 107 ± 31 (43–154) days, and 13 around the world during 103 ± 20 (44–184) days (Table 5).
Figure 3C shows the variants circulating in the region, both imported and indigenous, at the time.

3.3. Variants of Interest

Of the 82 non-synonymous mutations fixed in Asturias by 2024, 17 were used to define a variant of interest (Table 6).
Figure 5 shows the number of fixed mutations found in each variant of interest in Asturias and the rest of the world (Supplementary Table S4).

4. Discussion

Viruses constantly change through mutation, and some changes allow the virus to spread more easily or make it resistant to treatments or vaccines. As the virus spreads, it may change and become harder to stop. The mutation rate may not be as high as one might think for the effects to be significant; regardless of the rate at which the environment fluctuates, the highest levels of adaptability occur at intermediate mutation rates [7]. In order to achieve effective surveillance, it is essential to obtain a sufficient amount of sequence data from a representative population. This data must be analysed in order to detect new variants and monitor trends in circulating variants. In 2022, only the impact of the disease on vulnerable people, hospitalisations, and deaths was monitored [8]. Consensus genomic sequences of SARS-CoV-2 variants represent the most frequently observed viral genomes in clinical samples from patients and are widely used to monitor the global spread of the virus [9,10]. However, they do not reflect the full diversity of viral genomes.
Currently, there are growing signs that adaptive evolution of SARS-CoV-2 has stalled, and purifying selection is the dominant evolutionary force acting on non-synonymous mutations in the Omicron lineage [11]. Because mutations at the third nucleotide of a codon often lead to no change in the amino acid sequence, the most frequent change occurs in the third position of the codon [12]. However, despite the fact that SARS-CoV-2 is an RNA virus with a high mutation rate, changes that are maintained only occur in 1% of the viral genome. As you might expect, these changes occur mostly in the S protein. However, mutations in the ORF1a gene, which encodes proteins involved in regulating the host response, are also notable [13,14].
In Asturias, we observed 157 mutations out of 5% of the viral population. This is a similar proportion to that in Spain and slightly higher if all the viral strains circulating in the world are taken into account, where 116 mutations were observed. This is because the number of viral strains is greater, making it more difficult to obtain that 5% viral population for a given mutation.
If we compare the latter period with the start of the pandemic, it is striking that the estimated mutation rate is higher in the post-pandemic era. However, of the non-synonymous mutations that occurred, 31 were fixed in the post-pandemic period, compared to 51 in the first period. This is because, once the initial changes are in place, subsequent changes are more difficult to establish, especially if the first mutations have evolutionary advantages.
In a previous study and as reflected by other authors [3,5,15], mutations can emerge, giving rise to new variants, as the number of infected people increases. This second study provides additional information: it appears that the mutations are fixed within 18 months of the onset period, as illustrated in Figure 2. It will be interesting to see if the pattern of mutation fixation is maintained in 2026 and the number of established mutations continues to decrease due to purifying selection.
High vaccination rates and the widespread use of face masks were considered important factors in preventing the emergence of variants and slowing the spread of the virus. However, the diversity of the virus remains, being greater than during the pandemic. In the post-pandemic era, 313 lineages were identified in Asturias, but only 4 represent more than 5% of the viral population. Furthermore, the gain of 91 mutations led to the classification of 55 new circulating variants according to the criteria for designation of a new Pango lineage (necessary but not sufficient).
As mentioned above, the most frequent mutations are in the S and ORF1a genes. Of the four structural proteins, only the S protein (17 mutations), which serves as the primary antigen targeted by the host immune response, accumulates changes in the new variants. Mutations in viral proteins, particularly the S protein, can significantly affect viral infectivity, virulence, and immunogenicity, so they require continuous monitoring. The RBD (and particularly the RBM) is the core part of the S protein that binds directly to ACE2 in host cells. Some mutations in the RBM (three mutations) can induce significant changes in SARS-CoV-2 phenotypes. Genetic mutations at the V445 site influence membrane fusion and entry into diverse target cells, mutations at the F456 site often result in resistance to class A antibodies, and mutations at the F486 site escape the epitopes of class B antibodies [16,17].P1263L shows a significant increase in fusion [18] compared to P1263Q.Most mutations that generate new variants occur in accessory proteins: ORF7a (3 mutations) can suppress the IFN-I response by inhibiting STAT2, and ORF8 (2 mutations) downregulates the presentation of viral antigens via the class I major histocompatibility complex [19]; the ability to suppress the IFN-I signalling pathway has been exhibited by ORF10 (1 mutation) through its interaction with the mitochondrial antiviral signalling protein [19,20]; ORF3a (9 mutations) modifies crucial cellular processes, such as apoptosis and autophagy [19,21]; inflammatory cytokines have been reported to be induced by both ORF3a and ORF7a through the activation of NF-κB signalling [21]; and Nsp2 (8 mutations) is involved in disruption of signalling in host cells [22]. More surprising are the abundant mutations in NSP3 (21 mutations), which is involved in promoting RNA replication, transcription, and cleavage of proteins involved in the host innate immunity [23,24].
The COVID-19 pandemic has shown a tendency to generate variants in specific geographic areas and cross-border transmission patterns [25,26,27,28]. The introduction and dissemination of the virus across different regions has been facilitated by tourism, transportation routes, and global migration patterns [29]. The increase in incidence may be accompanied by the appearance of new variants originating in the region. New variants circulating around the world continually appear in our region. This makes them the ones that are detected for the longest time, as they are more difficult to control, although none of them generate large outbreaks. In fact, the NCVs from Asturias are the majority. But over time, the absence of new local variants causes a rebound with imported variants. None of the predominant lineages in the epidemic has remained for long, and only two are actively transmitted in the region. This indicates a constant turnover of lineages, each of which predominates for a couple of months at most and without causing any serious problems.
Although most changes have little to no impact on the properties of the virus, this high mutation rate and the continuous appearance of NCVs require genomic surveillance, since some changes can lead to a more aggressive variant that can spread and predominate in the rest of the world. Therefore, lineages may retain mutations that became dominant in the global pandemic over time, which may have positive effects on the fitness of the virus and facilitate the emergence of new variants. The WHO has established a dedicated group to monitor the evolution of the virus. This group has been operational since June 2020 in tracking SARS-CoV-2 variants [30].
The Omicron variant has spread worldwide and is now the predominant variant. In our region, after the arrival of the Omicron variant and the transition to a strategy that reduces pressure on mild or asymptomatic cases and their contacts, there was a decrease in the sampling rate in the age group between 6 and 65 years; an increase in the positivity rate was observed in children under 1 year of age. Compared to previous variants of concern (VOCs), the Omicron variant is characterised by increased infectivity and immune evasion, as well as a substantially larger number of mutations [31]. Mutations originate from the previous variants within the RBD of Omicron; K417N and N501Y (Beta) are largely responsible for these monoclonal antibodies failing to neutralise the Omicron S [32]. Some of these mutations increased affinity for ACE2 (T478K -Delta-, N501Y), while others decreased ACE2 affinity (K417N) [31]. Other mutations fixed from previous variants of interest are as follows. The RdRp_P323L (Alpha)mutation is required for polymerase activity and is predicted to diminish the efficacy of antiviral drugs.The S_D614G (Alpha) mutation increases infectivity [33,34]. S_H655Y (Gamma) may have reduced neutralisation by monoclonal antibody therapies, convalescent sera, and post-vaccination sera [35];it is known to enhance viral growth and S protein cleavage by furin [36], and it also governs entry through endosomes, as suggested by the significant increase in viral infectivity [37]. N protein mutations, including P13L (Lambda), R203K, and G204R/K (Alpha),may increase the transmission of SARS-CoV-2, but they are also associated with reduced disease severity and lower mortality rates than individuals with the wild type [38,39,40]. P13L itself has been identified as the most important epidemiological driver of fitness in the N protein [41]. The S_E484K mutation, present in Beta, has reappeared; it escapes the neutralising effect of several monoclonal antibodies, convalescent plasma, and post-vaccine sera [42]. The ORF1a_T3255I (nsp4_T492I) mutation, present in Lambda, increases the virus’s replication capacity and infectivity and improves its ability to evade host immune responses [43].
The global SARS-CoV-2 pandemic is decreasing, but the populations affected by the virus continue to appear. Geographical epidemiological research clarifies how the virus is spread in the context of the COVID-19 pandemic, explaining how the pathogen propagates within and between populations, which helps to identify and contain chains of transmission [44,45]. Fortunately, all newly detected circulating variants appear to be extinct and do not exhibit signatures suggestive of adaptive or transmission-related changes, but further examination of the spatial patterns and transmission dynamics of COVID-19 at various scales, from local communities to global populations, is necessary to implement localised lockdown measures to contain the spread, the day a really dangerous variant is generated

5. Conclusions

Even as the global pandemic of SARS-CoV-2 recedes, the number of people affected by the virus continues to rise, making it crucial to maintain a strong focus on the issue. Controlling the impact of the virus on a global scale will require continuous efforts to understand and adapt to the ever-changing situation.
This study is going to help us trace the origins and sources of the different versions of the virus that are doing the rounds and compare the emerging variations within Asturias. The next lineage, which may be more transmissible, infectious, and able to evade vaccine-induced or natural host immunity, could be the result of low-frequency lineages and circulating VOCs.
Mutations that increase SARS-CoV-2 transmission and may be associated with less disease severity are those that are becoming established in the virus population.
In addition to direct intervention measures, sustained monitoring of SARS-CoV-2 plays a crucial role in controlling variants. Continuous surveillance facilitates the early identification of variants that undergo substantial changes in their adaptability, which allows rapid adjustments to preventive measures and will contribute to strengthening preparedness for the next pandemic. The discovery of new local variants that can be imported and exported emphasises the importance of local surveillance in informing public health responses relating to diagnostics, vaccination strategies, and health policies at local, regional, and global levels.

Supplementary Materials

The following supporting information can be downloaded at https://www.mdpi.com/article/10.3390/v17121531/s1, Table S1: Asturian sequences uploaded to the GISAID database until July 2024; Table S2: Mutations that occurred in >5% of the sequenced viral population, with fixed mutations indicated as those present in >95% of the world’s population; Table S3: Number of mutations fixed occurring in each gene in the Asturias strains during COVID-19 (March 2020 to June 2022) and the post-COVID-19 period (July 2022 to July 2024);Table S4: Number of pangolin lineages detected in Asturias from June 2022 to July 2024;Table S5: New circulating variants from 2020 to 2024 in Asturias.

Author Contributions

Conceptualisation, J.M.G.-A., Z.P.M., S.R.-A., J.G.d.O., M.E.Á.-A., C.O.V., M.R.P. and S.M.G.; Data curation, J.M.G.-A., Z.P.M., S.R.-A., J.G.d.O., M.E.Á.-A., C.O.V., M.R.P. and S.M.G.; Formal analysis, J.M.G.-A., Z.P.M., S.R.-A., J.G.d.O., M.E.Á.-A., C.O.V., M.R.P. and S.M.G.; Writing—original draft, J.M.G.-A., Z.P.M., S.R.-A., J.G.d.O., M.E.Á.-A., C.O.V., M.R.P. and S.M.G. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

This study was conducted in accordance with the Declaration of Helsinki, as revised in 2013. Approval from a Research Ethics Committee was not required, as Organic Law 3/2018, of 5 December, on the Data Protection and Guarantee of Digital Rights, provides, with respect to the processing of health data, that the health authorities and public institutions with public health monitoring powers may carry out scientific research without the data subject’s consent in situations of exceptional relevance and seriousness for public health.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data availability in GISAID (https:www.gisaid.org/).

Acknowledgments

European Commission/Carlos III Health Institute (Ministry of Science and Innovation), HaDEA RELECOV 2.0 EU4H-2022-DGA-MS-IBA-01-02, and the Ministry of Science, Business, Training, and Employment of the Principality of Asturias (GRUPIN-24-IDE/2024/000719).

Conflicts of Interest

The authors declare no conflicts of interest.

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Viruses 17 01531 g001
Figure 1. Rate of main mutations circulating in Asturias that have been fixed (Viruses 17 01531 i001) and lost (Viruses 17 01531 i002) in the population in each gene during COVID-19 (March 2020 to June 2022) and the post-COVID-19 period (July 2022 to July 2024).
Figure 1. Rate of main mutations circulating in Asturias that have been fixed (Viruses 17 01531 i001) and lost (Viruses 17 01531 i002) in the population in each gene during COVID-19 (March 2020 to June 2022) and the post-COVID-19 period (July 2022 to July 2024).
Viruses 17 01531 g001
Viruses 17 01531 g002
Figure 2. Number of major SARS-CoV-2 mutations (>5% of the viral population) that became fixed in Asturias during COVID-19 (March 2020 to June 2022) and the post-COVID-19 period (July 2022 to July 2024). The figure shows the dates of first detection and fixation.
Figure 2. Number of major SARS-CoV-2 mutations (>5% of the viral population) that became fixed in Asturias during COVID-19 (March 2020 to June 2022) and the post-COVID-19 period (July 2022 to July 2024). The figure shows the dates of first detection and fixation.
Viruses 17 01531 g002
Viruses 17 01531 g003
Figure 3. (A) Number of pangolin lineages (313 colour schemes not included, each colour represents a pangolin lineage) detected in Asturias in the post-COVID-19 period (July 2022 to July 2024). (B) Percentage of pangolin lineages mostly detected over time (>1%) in the post-COVID-19 period (July 2022 to July 2024);only the major lineages are indicated.(C) Number of new circulating variants that originated in Asturias or were imported and incidence of SARS-CoV-2 in the post-COVID-19 period (July 2022 to July 2024).
Figure 3. (A) Number of pangolin lineages (313 colour schemes not included, each colour represents a pangolin lineage) detected in Asturias in the post-COVID-19 period (July 2022 to July 2024). (B) Percentage of pangolin lineages mostly detected over time (>1%) in the post-COVID-19 period (July 2022 to July 2024);only the major lineages are indicated.(C) Number of new circulating variants that originated in Asturias or were imported and incidence of SARS-CoV-2 in the post-COVID-19 period (July 2022 to July 2024).
Viruses 17 01531 g003
Viruses 17 01531 g004
Figure 4. Dated phylogeny of the new circulating variant, XBB.1.5.8 + NSP14_V328F, which was imported and belongs to the same transmission clade in the region (green color in the figure). The days until the date of the most recent sequence were used as the sampling date.
Figure 4. Dated phylogeny of the new circulating variant, XBB.1.5.8 + NSP14_V328F, which was imported and belongs to the same transmission clade in the region (green color in the figure). The days until the date of the most recent sequence were used as the sampling date.
Viruses 17 01531 g004
Viruses 17 01531 g005
Figure 5. The number of major mutations per gene currently fixed and the variants of interest in which they were initially found. (a) In Asturias and in the world, (b) in the world but not in Asturias, (c) in Asturias but not in the world.
Figure 5. The number of major mutations per gene currently fixed and the variants of interest in which they were initially found. (a) In Asturias and in the world, (b) in the world but not in Asturias, (c) in Asturias but not in the world.
Viruses 17 01531 g005
Table 1. Sequences sampled and positivity rate by age in the pre-Omicron period (until November 2021) and in the Omicron period (March 2022 to July 2024).
Table 1. Sequences sampled and positivity rate by age in the pre-Omicron period (until November 2021) and in the Omicron period (March 2022 to July 2024).
Pre-Omicron PeriodOmicron Period
Age (Years)SamplingPositivity (%)SamplingPositivity (%)
<134812.7413612
1–519,6052.910,4942.7
6–2061,0176.512,4994.5
21–65253,6535.536,48919.9
>65100,9204.831,47516.1
Table 2. The number of mutations that occurred in >5% of the viral population sequenced in GISAID in each gene between 2020 and July 2024.
Table 2. The number of mutations that occurred in >5% of the viral population sequenced in GISAID in each gene between 2020 and July 2024.
ORF1a RdRp ORF1abSORF3aEMORF6ORF7aORF7bORF8NORF10Total
GISAID212659225121411 116
SPAIN2947822281224141158
ASTURIAS3138822271224121157
Table 3. Number of mutations fixed occurring in each gene in the Asturias strains during COVID-19 (March 2020 to June 2022) and the post-COVID-19 period (July 2022 to July 2024).Time is the average number of days it took to become fixed with its confidence interval.
Table 3. Number of mutations fixed occurring in each gene in the Asturias strains during COVID-19 (March 2020 to June 2022) and the post-COVID-19 period (July 2022 to July 2024).Time is the average number of days it took to become fixed with its confidence interval.
MutationsORF1a RdRp ORF1abSORF3aEMORF6ORF7aORF7bORF8NORF10Total
2020–2022Occurred2135472151214121105
Fixed813291121 5 51
Days or
Mean± CI		62/124(x4)/217/775,930062
124
124		358 ± 132
(0–1209)		49637262
62		868 124/310
403/713,961		 344 ± 94
(0–1209)
2022–2024Ocsurred203647213 112288
Fixed6 21 3 1 31
Days or
Mean± CI		93/124(x2) 217(x3) 257 ± 53
(124–527)		 248
278
620		 217 250 ± 46
(93–620)
Table 4. Mutations gained by new circulating variants in Asturias.
Table 4. Mutations gained by new circulating variants in Asturias.
ORF_1a RdRp ORF_1ab
NSP1NSP2NSP3NSP4NSP5NSP6NSP8NSP9NSP10NSP12NSP13NSP14NSP15NSP16SORF3aEORF7aORF8NORF10
G94CA357SD112NA128VK90RF235LP10SG38VT115IA4774VV157LA320TD36GK160RA67VD155YT9VL5FD119YP151SI27T
P6SE574DD1764GV13IV35LL37F T21I I4563M I15TP205SP215LA701VD27H Q94LP38S
V121AG265SE119K M5021V N71S A845SL140F T28I
G285SE387D S4621N P203L D253GM260K
L24FI541V Q22H D80EQ185H
N254SM988L V328F F456LQ57H
S591IN1322S F486VS171L
T103IN1680K F59ST270I
P153L G252VV273L
Q167R L249F
R1297G N354K
S126L P1263Q
S1428L Q675H
S454G T547I
T1203I T572I
T424N V1264L
T720I V445P
T970M
V1385I
V1673I
Y1535H
Table 5. Asturian new circulating variants between 2020 and 2024.
Table 5. Asturian new circulating variants between 2020 and 2024.
NCVN (%Total Identified)First Detection DateLast Detection DateTime of Detection (Days)
Frst detected in the world
BA.5.2.1 + NSP3_S454G6 (43)17/09/202222/10/202235
BA.5.2.6 + NSP3_M988L7 (3)22/09/202206/11/202245
BF.5 + S_D80E + S_A701V + NSP1_G94C8 (62)22/09/202208/11/202247
BA.5.1 + NSP12_M5021V5 (7)24/09/202216/11/202253
BF.7 + NSP14_P203L13 (29)19/10/202207/12/202249
BQ.1.1.18 + S_T547I5 (28)16/11/202211/01/202356
XBB.1.5 + NSP3_T1203I12 (6)24/01/202301/05/202397
FL.5 + NSP14_Q22H + NSP3_P153L6 (2)15/02/202324/05/202398
XBB.1.5.8 + NSP14_V328F10 (10)01/03/202329/03/202328
BQ.1.18 + NSP14_I15T20 (17)04/03/202329/06/2023117
XBB.1.5 + NSP2_S591I + NSP3_N1322S12 (1)04/03/202320/08/2023169
XBB.1.5 + NSP5_V35L6 (1)09/03/202307/07/2023120
XBB.1.5.71 + NSP1_P6S + ORF3a_Q57H + NSP12_I4563M5 (4)28/04/202313/06/202346
XBB.1.5.71 + NSP1_P6S + NSP12_I4563M6 (2)12/05/202303/06/202322
EG.5.1 + ORF3a_D27H5 (1)20/06/202324/08/202365
XBB.1.16.11 + NSP2_N254S6 (1)20/07/202316/10/202388
DV.7.1 + NSP3_E119K6 (18)26/07/202308/09/202344
EG.5.1.3 + NSP3_I541V5 (42)05/09/202314/09/20239
JD.1.1 + ORF3a_M260K5 (2)13/10/202328/11/202346
JG.3 + ORF3a_S171L7 (14)27/10/202304/12/202338
JN.1.31 + S_T572I6 (23)29/11/202313/03/2024105
JN.1.16 + S_A67V + S_L249F + S_V445P6 (10)07/05/202426/05/202419
JN.1.32 + S_F456L7 (1)12/05/202406/06/202425
JN.1.16.1 + NSP3_S1428L + NSP5_K90R + NSP6_L37F + S_F59S5 (83)13/05/202419/05/20246
First detected in Asturias
BA.4.6 + NSP2_G265S + NSP3_D112N + ORF7a_Q94L7 (100) **10/06/202217/10/2022129
CH.1.1.28 + NSP16_K160R14 (100) **22/12/202222/03/202390
XBB.1.5 + NSP3_T970M + NSP12_A4774V6 (100) **27/01/202313/04/202376
XBB.1.5.77 + S_G252V + NSP2_E574D + ORF7a_L5F + ORF7a_T28I6 (100) **14/02/202307/04/202352
XBB.1.5.1 + NSP15_D36G + NSP3_S126LL + NSP1_V121A + ORF8_P38S7 (100) **03/04/202304/05/202331
XBB.2.3 + E_T9V + NSP3_N1680K + NSP3_Y1535H + ORF10_I27T5 (100) **16/04/202311/08/2023117
EG.1.4 + NSP12_S4621N + S_A845S6 (100) **09/05/202303/08/202386
DV.7.1 + NSP3_R1297G + ORF3a_Q185H6 (100) **21/05/202331/08/2023102
JG.3 + NSP3_V1385I8 (100) **04/10/202322/01/2024110
JN.1.16.2 + S_A67V + S_V445P + S_L249F8 (100) **24/01/202425/05/2024122
BQ.1.1.15 + NSP3_T1203I6 (55) *26/07/202227/12/2022154
BQ.1.1.66 + NSP3_E387D + NSP9_G38V + NSP10_T115II10 (83) *23/11/202215/03/2023112
XBB.1.5.37 + NSP9_T21I7 (78) *15/12/202223/04/2023129
XBB.2.3.13 + NSP3_Q167R6 (60) *28/02/202331/07/2023153
XBB.2.3.13 + NSP2_A357S + NSP6_F235L + S_A701V13 (93) *12/03/202324/04/202343
XBB.1.5.71 + NSP15_P205S + NSP2_L24F5 (83) *10/05/202327/09/2023140
BA.4.1 + NSP13_V157L7 (88) *09/06/202215/08/202267
BE.1 + ORF3a_T270I + ORF3a_V273L6 (86) *10/07/202208/09/202260
BF.7 + NSP4_A128V + S_Q675H + S_P1263Q10 (19)29/06/202201/12/2022155
CK.2.1.1 + S_V1264L + ORF8_D119Y5 (63)03/10/202221/12/202279
EL.1 + NSP2_T103I + NSP3_T720I35 (90)16/11/202219/05/2023184
EF.1.2 + S_D253G + NSP4_V13I + ORF3a_D155Y10 (67)20/12/202216/03/202386
XBB.2.3.13 + NSP2_A357S12 (16)05/02/202309/06/2023124
EL.1 + NSP14_A320T + NSP2_G265S + NSP3_T970M6 (75)14/02/202319/05/202394
DV.7.1 + NSP14_N71S8 (57)28/04/202302/09/2023127
XBB.1.5 + NSP3_V1673I + ORF3a_L140F13 (81)08/06/202319/09/2023103
EG.6.1 + NSP3_S1428L11 (79)16/06/202302/10/2023108
DV.7.1 + NSP8_P10S + NSP3_D1764G5 (16)23/06/202310/09/202379
EG.5.1.5 + S_N354K + N_P151S12 (46)13/07/202326/08/202344
HV.1 + NSP14_P203L6 (29)05/08/202313/10/202369
JN.1 + S_F486V6 (75)29/10/202325/01/202488
** detected only in Asturias; * detected also in Spain.
Table 6. Mutations fixed in Asturias used to define the genetic characteristics of SARS-CoV-2 variants of interest by the WHO.
Table 6. Mutations fixed in Asturias used to define the genetic characteristics of SARS-CoV-2 variants of interest by the WHO.
VariantAlphaBetaGammaDeltaZetaEtaThetaIotaKappaLambdaMuEpsilonOmicron
Mutation
E_T9I X X X X
M_A63T X
N_G204RX X X X X X
N_P13L X X
N_R203KX X X X X X
ORF1a_T3255I XX X
RdRp_P323LXXXXXXXXXXXXX
S_D614GXXXXXXXXXXXXX
S_E484K XX XXX X
S_H655Y X X
S_K417N X
S_N501Y XX X X
S_N679K X
S_P681R X X
S_Q954H X
S_S373P X
S_T478K X X
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González-Alba, J.M.; Martínez, Z.P.; Rojo-Alba, S.; Varela, C.O.; Oña, J.G.d.; Pérez, M.R.; García, S.M.; Álvarez-Argüelles, M.E. New Circulating Variants of SARS-CoV-2 in Asturias During the Period (2022–2024). Viruses 2025, 17, 1531. https://doi.org/10.3390/v17121531

AMA Style

González-Alba JM, Martínez ZP, Rojo-Alba S, Varela CO, Oña JGd, Pérez MR, García SM, Álvarez-Argüelles ME. New Circulating Variants of SARS-CoV-2 in Asturias During the Period (2022–2024). Viruses. 2025; 17(12):1531. https://doi.org/10.3390/v17121531

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González-Alba, José María, Zulema Pérez Martínez, Susana Rojo-Alba, Cristina Ochoa Varela, Juan Gómez de Oña, Mercedes Rodríguez Pérez, Santiago Melón García, and Marta Elena Álvarez-Argüelles. 2025. "New Circulating Variants of SARS-CoV-2 in Asturias During the Period (2022–2024)" Viruses 17, no. 12: 1531. https://doi.org/10.3390/v17121531

APA Style

González-Alba, J. M., Martínez, Z. P., Rojo-Alba, S., Varela, C. O., Oña, J. G. d., Pérez, M. R., García, S. M., & Álvarez-Argüelles, M. E. (2025). New Circulating Variants of SARS-CoV-2 in Asturias During the Period (2022–2024). Viruses, 17(12), 1531. https://doi.org/10.3390/v17121531

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