African swine fever virus-like integrated elements in a soft tick genome – an ancient virus vector arms race?

Forth, Jan Hendrik; Forth, Leonie; Lycett, Samantha; Bell‐Sakyi, Lesley; Keil, Guenther; Blome, Sandra; Calvignac‐Spencer, Sébastien; Wissgott, Antje; Krause, Johannes; Hoeper, Dirk; Kampen, Helge; Beer, Martin

doi:10.1101/2020.03.08.978106

Cited by 2 publications

(1 citation statement)

References 82 publications

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“…Several African and exotic Ornithodoros species have been found capable of sustaining replication and transmission of ASFV experimentally, but vector competence appears to be regulated by multiple tick species- and virus strain-specific factors [ 46 , 47 , 48 , 49 , 50 , 51 , 52 , 53 , 54 , 55 , 56 , 57 , 58 , 59 , 60 , 61 , 62 , 63 , 64 , 65 , 66 , 67 , 68 , 69 , 70 , 71 , 72 , 73 ]. Hence, it is important that both ticks and viruses should be identified accurately in assessing and recording vector potential.…”

Section: Discussionmentioning

confidence: 99%

Detection of African Swine Fever Virus in Ornithodoros Tick Species Associated with Indigenous and Extralimital Warthog Populations in South Africa

Craig

Schade-Weskott

Rametse

et al. 2022

Viruses

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We investigated the possibility that sylvatic circulation of African swine fever virus (ASFV) in warthogs and Ornithodoros ticks had extended beyond the historically affected northern part of South Africa that was declared a controlled area in 1935 to prevent the spread of infection to the rest of the country. We recently reported finding antibody to the virus in extralimital warthogs in the south of the country, and now describe the detection of infected ticks outside the controlled area. A total of 5078 ticks was collected at 45 locations in 7/9 provinces during 2019–2021 and assayed as 711 pools for virus content by qPCR, while 221 pools were also analysed for tick phylogenetics. Viral nucleic acid was detected in 50 tick pools representing all four members of the Ornithodoros (Ornithodoros) moubata complex known to occur in South Africa: O. (O.) waterbergensis and O. (O.) phacochoerus species yielded ASFV genotypes XX, XXI, XXII at 4 locations and O. (O.) moubata yielded ASFV genotype I at two locations inside the controlled area. Outside the controlled area, O. (O.) moubata and O. (O.) compactus ticks yielded ASFV genotype I at 7 locations, while genotype III ASFV was identified in O. (O.) compactus ticks at a single location. Two of the three species of the O. (O.) savignyi complex ticks known to be present in the country, O. (O.) kalahariensis and O. (O.) noorsveldensis, were collected at single locations and found negative for virus. The only member of the Pavlovskyella subgenus of Ornithodoros ticks known to occur in South Africa, O. (P.) zumpti, was collected from warthog burrows for the first time, in Addo National Park in the Eastern Cape Province where ASFV had never been recorded, and it tested negative for the viral nucleic acid. While it is confirmed that there is sylvatic circulation of ASFV outside the controlled area in South Africa, there is a need for more extensive surveillance and for vector competence studies with various species of Ornithodoros ticks.

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Section: Discussionmentioning

confidence: 99%

Detection of African Swine Fever Virus in Ornithodoros Tick Species Associated with Indigenous and Extralimital Warthog Populations in South Africa

Craig

Schade-Weskott

Rametse

et al. 2022

Viruses

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Identification of African swine fever virus-like elements in the soft tick genome provides insights into the virus’ evolution

Forth

Lycett

et al. 2020

BMC Biol

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Background African swine fever virus (ASFV) is a most devastating pathogen affecting swine. In 2007, ASFV was introduced into Eastern Europe where it continuously circulates and recently reached Western Europe and Asia, leading to a socio-economic crisis of global proportion. In Africa, where ASFV was first described in 1921, it is transmitted between warthogs and soft ticks of the genus Ornithodoros in a so-called sylvatic cycle. However, analyses into this virus’ evolution are aggravated by the absence of any closely related viruses. Even ancient endogenous viral elements, viral sequences integrated into a host’s genome many thousand years ago that have proven extremely valuable to analyse virus evolution, remain to be identified. Therefore, the evolution of ASFV, the only known DNA virus transmitted by arthropods, remains a mystery. Results For the identification of ASFV-like sequences, we sequenced DNA from different recent Ornithodoros tick species, e.g. O. moubata and O. porcinus, O. moubata tick cells and also 100-year-old O. moubata and O. porcinus ticks using high-throughput sequencing. We used BLAST analyses for the identification of ASFV-like sequences and further analysed the data through phylogenetic reconstruction and molecular clock analyses. In addition, we performed tick infection experiments as well as additional small RNA sequencing of O. moubata and O. porcinus soft ticks. Conclusion Here, we show that soft ticks of the Ornithodoros moubata group, the natural arthropod vector of ASFV, harbour African swine fever virus-like integrated (ASFLI) elements corresponding to up to 10% (over 20 kb) of the ASFV genome. Through orthologous dating and molecular clock analyses, we provide data suggesting that integration could have occurred over 1.47 million years ago. Furthermore, we provide data showing ASFLI-element specific siRNA and piRNA in ticks and tick cells allowing for speculations on a possible role of ASFLI-elements in RNA interference-based protection against ASFV in ticks. We suggest that these elements, shaped through many years of co-evolution, could be part of an evolutionary virus-vector ‘arms race’, a finding that has not only high impact on our understanding of the co-evolution of viruses with their hosts but also provides a glimpse into the evolution of ASFV.

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African swine fever virus-like integrated elements in a soft tick genome – an ancient virus vector arms race?

Cited by 2 publications

References 82 publications

Detection of African Swine Fever Virus in Ornithodoros Tick Species Associated with Indigenous and Extralimital Warthog Populations in South Africa

Detection of African Swine Fever Virus in Ornithodoros Tick Species Associated with Indigenous and Extralimital Warthog Populations in South Africa

Identification of African swine fever virus-like elements in the soft tick genome provides insights into the virus’ evolution

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