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.

KEYWORDS:

• Bird migration
• African-Western Palearctic region
• Hyalomma marginatum s.l.
• Ixodes
• Anaplasma phagocytophilum
• 16s rRNA
• ankA

Acknowledgments

We wish to acknowledge the bird ringers for collecting the bird data and the ticks. Furthermore, we acknowledge Professor Snorre Stuen for his assistance as well as Malin Lager, Lina Löfgren and Laura González Carra for their assistance in the laboratory. This is publication number 26 from the Antikythira Bird Observatory.

Disclosure statement

No potential conflict of interest was reported by the authors.

Correction Statement

This article has been republished with minor changes. These changes do not impact the academic content of the article.

Additional information

Funding

This work was supported by ALF grants from Uppsala University Hospital, the EU Interreg V program ScandTick Innovation, project ID 20200422, reference no 2015-000167, and by the Medical Research Council of Southeast Sweden (FORSS, 657881). Furthermore, TGTJ’s research on ticks and tick-borne pathogens is supported by Carl Tryggers stiftelse, Helge Ax:son Johnsons stiftelse, Längmanska kulturfonden, and Magnus Bergvalls stiftelse, all in Stockholm, Sweden. Antikythira Bird Observatory is run by the Hellenic Ornithological Society/Birdlife Greece and is funded from the A.G. and A.P Leventis Foundation. EU-Interreg North Sea Region project NorthTick ref no: J-No.: 38-2-7-19.

Notes on contributors

Tove Hoffman

Tove Hoffman is a PhD student at the Department of Medical Sciences at Uppsala University, Sweden. Her doctoral studies concern the involvement of northward migratory birds in the dispersal of ticks and tick-borne pathogens.

Peter Wilhelmsson

Peter Wilhelmsson received his PhD in 2014 at Linköping University and is present at Ryhov County Hospital, Jönköping, Sweden.

Christos Barboutis

Christos Barboutis received his PhD in bird migration and stopover ecology at the Department of Biology, University of Crete, Greece. Currently working as the scientific manager of the Antikythira bird observatory, Hellenic Ornithological Society/BirdLife Greece.

Thord Fransson

Thord Fransson is a professor at the Swedish Museum of Natural History. He obtained his PhD in 1997.

Thomas G.T. Jaenson

Thomas G.T. Jaenson is a professor in medical entomology at Uppsala University, Sweden. His research is focused on the vector biology of ticks.

Per-Eric Lindgren

Per-Eric Lindgren received his PhD at the Department of Microbiology, SLU, and since 2010 he is professor and chair of Medical Microbiology, Department of Clinical and Experimental Medicine, Linköping University, Linköping, Sweden.

Friederike D. Von Loewenich

Friederike D. von Loewenich is a medical microbiologist with research interest in epidemiology and phylogeny of Anaplasma phagocytophilum.

Åke Lundkvist

Åke Lundkvist received his PhD at Karolinska Institutet, Stockholm, and is at present professor in virology at the Department of Medical Biochemistry and Microbiology, Uppsala University, Sweden.

Björn Olsen

Björn Olsen received his PhD at Umeå University and is at present professor at the Department of Medical Sciences, Uppsala University, Sweden.

Erik Salaneck

Erik Salaneck is a medical doctor. He obtained his PhD in 2001.