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Within-host genetic diversity of SARS-CoV-2 lineages in unvaccinated and vaccinated individuals
Abstract Viral and host factors can shape SARS-CoV-2 evolution. However, little is known about lineage-specific and vaccination-specific mutations that occur within individuals. Here, we analysed deep sequencing data from 2,820 SARS-CoV-2 respiratory samples with different viral lineages to describe the patterns of within-host diversity under different conditions, including vaccine-breakthrough infections. In unvaccinated individuals, variant of Concern (VOC) Alpha, Delta, and Omicron respiratory samples were found to have higher within-host diversity and were under neutral to purifying selection at the full genome level compared to non-VOC SARS-CoV-2. Breakthrough infections in 2-dose or 3-dose Comirnaty and CoronaVac vaccinated individuals did not increase levels of non-synonymous mutations and did not change the direction of selection pressure. Vaccine-induced antibody or T cell responses did not appear to have significant impact on within-host SARS-CoV-2 sequence diversification. Our findings suggest that vaccination does not increase exploration of SARS-CoV-2 protein sequence space and may not facilitate emergence of viral variants.
Introduction The SARS-CoV-2 pandemic continues to spread globally. Despite the vaccination of over 69% of the world population1, the risk of SARS-CoV-2 reinfections and breakthrough infections is increasing due to the emergence of new viral variants2,3. Multiple variants of concern (VOC) have demonstrated the ability to evade naturally-acquired or vaccine-induced immunity4,5,6. Therefore, it is crucial to investigate the impact of vaccination on the mutational and evolutionary processes of SARS-CoV-2.
Genomic surveillance has been used to trace the transmission and evolution of SARS-CoV-2 mutations at local, regional, and global scales throughout the pandemic7,8,9. However, there is still limited knowledge of how these mutations originate and accumulate within hosts. Within-host mutations can arise through replication errors or RNA damage/editing10 and they may be subject to fixation by stochastic (genetic drift) and deterministic (natural selection) processes. We and others have previously found that the SARS-CoV-2 transmission bottleneck between hosts is narrow8,11,12,13,14, suggesting that only few virions are transferred from the host during transmission. Most of the low-frequency mutations are not transmitted between patients, which constrains the use of intrahost single nucleotide variants (iSNVs) for effective contact tracing12,15,16. However, it remains important to investigate the within-host diversity of SARS-CoV-2 to understand host-level evolutionary forces.
Studying SARS-CoV-2 within-host diversity under different conditions may reveal factors that control virus evolution. Host and viral factors can both contribute to within-host diversity. Host factors such as species (animals/humans)17, viral shedding time18, and immune status19 were previously reported to have effects on intrahost SARS-CoV-2 diversity. It was hypothesized that prolonged infections in hosts with distinct immunological backgrounds (e.g., animals or immunocompromised patients) may hasten viral evolution and lead to the emergence of novel variants17,20. However, there is limited knowledge about post-vaccination characteristics of within-host selection pressures, which consistently act on the virus during the entire course of breakthrough infection. Besides, viral factors such as different virus lineages may also affect SARS-CoV-2 replication properties. SARS-CoV-2 VOCs have exhibited varying capacities to evade immunity4,6 and acquire higher transmissibility21,22. However, it is not clear whether different SARS-CoV-2 variants differ in within-host selection pressures.
Here, we analysed 2,820 deep-sequenced SARS-CoV-2 samples collected in Hong Kong (HK) between mid-2020 and 2022. The within-host diversity in SARS-CoV-2 infections from different lineages (VOCs and non-VOCs) and in breakthrough (Delta or Omicron) infections after Comirnaty or CoronaVac vaccination (two or three doses) were studied. Our results provide insights into the variation of within-host diversity, and the mutational patterns and selection pressures acting on viruses.