Genetic diversity and genomic epidemiology of SARS-CoV-2 during the first three years of pandemic in Morocco: Comprehensive sequence analysis, including the unique B.1.528 lineage in Morocco

During the three years following the emergence of the COVID-19 pandemic, the African continent, like other regions of the world, was significantly impacted by COVID-19. In Morocco, the COVID-19 pandemic has been marked by the emergence and spread of several SARS-CoV-2 variants, leading to a substantial increase in the incidence of infections and deaths. Nevertheless, there has been a persistent lack of comprehensive understanding regarding the genetic diversity, evolution, and epidemiology of several viral lineages. The aim of this study was to analyze the genetic diversity of SARS-CoV-2 and identify distinct lineages, as well as to assess their evolution during the pandemic in Morocco, using genomic epidemiology approaches. Furthermore, several key mutations in the functional proteins across different viral lineages were highlighted along with an analysis of the genetic relationships amongst these strains to better understand their evolutionary pathways. A total of 2274 genomic sequences of SARS-CoV-2, acquired from Morocco during the period of 2020 to 2023, were extracted from the GISAID EpiCoV database and subjected to analysis. Lineages and clades were classified according to the nomenclature of GISAID, Nextstrain, and Pangolin. The study was conducted and reported in accordance with STROBE (Strengthening the Reporting of Observational Studies in Epidemiology) guidelines. An exhaustive analysis of 2274 genomic sequences led to the identification of 157 PANGO lineages, including notable lineages such as B.1, B.1.1, B.1.528 and B.1.177, as well as variants such as B.1.1.7, B.1.621, B.1.525, B.1.351, B.1.617.1, B.1.617.2 and its notable sub-lineages AY.33, AY.72, AY.112, AY.121 that evolved over time before being supplanted by Omicron in December 2021. Among the 2274 sequences analyzed, Omicron and its sub-variants had a prevalence of 59.5%. The most predominant clades were 21K, 21L, and 22B, which are respectively related phylogenetically to BA.1, BA.2, and BA.5. In June 2022, Morocco rapidly observed a recrudescence of cases of infection, with the emergence and concurrent coexistence of subvariants from clade 22B such as BA.5.2.20, BA.5, BA.5.1, BA.5.2.1, and BF.5, supplanting the subvariants BA.1 (Clade display 21K) and BA.2 (Clade display 21L), which became marginal. However, XBB (clade 22F) and its progeny such XBB.1.5(23A), XBB.1.16(23B), CH.1.1(23C), XBB.1.9(23D), XBB.2.3(23E), EG.5.1(23F), and XBB.1.5.70 (23G) have evolved sporadically. Furthermore, several notable mutations, such as H69del/V70del, G142D, K417N, T478K, E484K, E484A, L452R, F486P, N501Y, Q613H, D614G, and P681H/R, known for their implications in transmissibility by increase infectivity and their ability to escape antibodies, were identified. This study has identified several distinct lineages, various mutations involved in the genetic diversity of Moroccan isolates, and analyzed their evolutionary trends. Furthermore, the lineages identified in Morocco were genetically closely linked to the original lineages, highlighting the importance of maintaining continuous surveillance of COVID-19 and extending vaccination coverage to prevent the emergence of new variants that could potentially be more infectious. These findings also provide a robust basis for better understanding the distinct mutations and their role in transmission, immune evasion, and reinfection.