A divergent Anaplasma phagocytophilum variant in an Ixodes tick from a migratory bird; Mediterranean basin

Abstract

Anaplasma phagocytophilum (AP) has vast geographical and host ranges and causes disease in humans and domesticated animals. We investigated the role of northward migratory birds in the dispersal of tick-borne AP in the African-Western Palearctic. Ticks were collected from northward migratory birds trapped during spring migration of 2010 at two localities in the central Mediterranean Sea. AP DNA was detected by PCR (gltA and 16S rRNA) and variant determination was performed using ankA sequences. In total, 358 ticks were collected. One of 19 ticks determined as Ixodes was confirmed positive for AP DNA. The tick was collected from a woodchat shrike (Lanius senator senator) trapped in Greece, and molecularly determined to belong to the I. ricinus complex and sharing highest (95%) 16S RNA sequence identity to I. gibbosus. The ankA AP sequence exhibited highest similarity to sequences from rodents and shrews (82%) and ruminants (80%). Phylogenetic analyses placed it convincingly outside other clades, suggesting that it represents a novel AP variant. The divergent Ixodes species harboring a novel AP variant could either indicate an enzootic cycle involving co-evolution with birds, or dissemination from other regions by avian migration. None of the 331 Hyalomma marginatum sensu lato ticks, all immature stages, were positive for AP DNA, lending no evidence for the involvement of Hyalomma ticks transported by birds in the ecology of AP.

Co-Occurrence of Francisella, Spotted Fever Group Rickettsia, and Midichloria in Avian-Associated Hyalomma rufipes

“…Rickettsia species in the SFG are transmitted to humans by multiple tick genera, including Rhipicephalus, Ixodes , and Hyalomma [ 34 ]. Wild birds are frequently parasitized by Ixodes and Hyalomma ticks, and the migratory behavior of the avian hosts aids in the geographical spread of ticks and their associated microorganisms [ 36 , 37 , 38 ]. Because they are intracellular tick-borne bacteria, Francisella , Midichloria , and Rickettsia are difficult to culture, and culture-independent generation of genome sequences is of importance for increasing the knowledge and understanding of these bacteria.…”

The Biological and Ecological Features of Northbound Migratory Birds, Ticks, and Tick-Borne Microorganisms in the African–Western Palearctic

“…Birds have been proposed to have a role as reservoir hosts [ 157 , 158 ], and birds may have a role in the dispersal of ticks infected by the bacterium [ 158 , 159 , 160 , 161 ]. The role of northbound spring migratory birds in the dispersal of tick-borne A. phagocytophilum in the African–Western Palearctic (AWP) region (AWPR) has been addressed [ 162 ]. A. phagocytophilum DNA was detected in an Ixodes species (sp.)…”

“…A. phagocytophilum DNA was detected in an Ixodes species (sp.) tick found feeding on a trans-Saharan migratory bird trapped at a stopover site in the Mediterranean Sea [ 162 ]. The ankA sequence of the detected A. phagocytophilum variant was found to differ from published sequences, raising questions as to whether it represented a novel variant and whether it could reflect a divergent enzootic cycle of A. phagocytophilum with birds as hosts, geographic isolation, or influx from another area by avian migration.…”

“…However, there is no evidence for immature H. marginatum s.l. ticks and birds having a major role in the ecology and northward dispersal of tick-borne A. phagocytophilum in the AWPR [ 162 ].…”

Detection of Pathogens and Ticks on Sedentary and Migratory Birds in Two Corsican Wetlands (France, Mediterranean Area)

“…It has also been detected in the spleen of T. merula from the Netherlands; furthermore, the presence of A. phagocytophilum in North America is often documented in birds and their ticks [59,62,63]. More recently, a different variant was reported from a Greek island in an Ixodes tick infesting a Lanius senator senator [64]. In Corsica, A. phagocytophilum has been mainly reported in I. ricinus, but it has also been detected in the tick species Dermacentor marginatus, Haemaphysalis.…”