Comparative Usutu and West Nile virus transmission potential by local Culex pipiens mosquitoes in north-western Europe
Jelke J. Fros,
Pascal Miesen,
Chantal B. Vogels,
Paolo Gaibani,
Vittorio Sambri,
Byron E. Martina,
Constantianus J. Koenraadt,
Ronald P. van Rij,
Just M. Vlak,
Willem Takken,
Gorben P. Pijlman
Affiliations
Jelke J. Fros
Laboratory of Virology Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands
Pascal Miesen
Department of Medical Microbiology, Radboud University Medical Center, Radboud Institute for Molecular Life Sciences, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands
Chantal B. Vogels
Laboratory of Entomology, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands
Paolo Gaibani
Regional Reference Centre for Microbiological Emergencies (CRREM), Microbiology Unit, Azienda Ospedaliero-Universitaria di Bologna, Policlinico S. Orsola—Malpighi, Bologna, Italy
Vittorio Sambri
Unit of Microbiology, The Greater Romagna Area Hub Laboratory, Piazza della Liberazione, 60, 47522 Pievesestina, FC, Italy
Byron E. Martina
Department of Viroscience, Erasmus Medical Center, Rotterdam, The Netherlands
Constantianus J. Koenraadt
Laboratory of Entomology, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands
Ronald P. van Rij
Department of Medical Microbiology, Radboud University Medical Center, Radboud Institute for Molecular Life Sciences, P.O. Box 9101, 6500 HB Nijmegen, The Netherlands
Just M. Vlak
Laboratory of Virology Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands
Willem Takken
Laboratory of Entomology, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands
Gorben P. Pijlman
Laboratory of Virology Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands
Originating from Africa, Usutu virus (USUV) first emerged in Europe in 2001. This mosquito-borne flavivirus caused high mortality rates in its bird reservoirs, which strongly resembled the introduction of West Nile virus (WNV) in 1999 in the United States. Mosquitoes infected with USUV incidentally transmit the virus to other vertebrates, including humans, which can result in neuroinvasive disease. USUV and WNV co-circulate in parts of southern Europe, but the distribution of USUV extends into central and northwestern Europe. In the field, both viruses have been detected in the northern house mosquito Culex pipiens, of which the potential for USUV transmission is unknown. To understand the transmission dynamics and assess the potential spread of USUV, we determined the vector competence of C. pipiens for USUV and compared it with the well characterized WNV. We show for the first time that northwestern European mosquitoes are highly effective vectors for USUV, with infection rates of 11% at 18 °C and 53% at 23 °C, which are comparable with values obtained for WNV. Interestingly, at a high temperature of 28 °C, mosquitoes became more effectively infected with USUV (90%) than with WNV (58%), which could be attributed to barriers in the mosquito midgut. Small RNA deep sequencing of infected mosquitoes showed for both viruses a strong bias for 21-nucleotide small interfering (si)RNAs, which map across the entire viral genome both on the sense and antisense strand. No evidence for viral PIWI-associated RNA (piRNA) was found, suggesting that the siRNA pathway is the major small RNA pathway that targets USUV and WNV infection in C. pipiens mosquitoes.
