The authors have declared that no competing interests exist.
Conceived and designed the experiments: OD CC. Performed the experiments: OD VN JC OM. Analyzed the data: OD CC. Contributed reagents/materials/analysis tools: OD VN KDM MB KSB OM FV LZ EJ PD CA FR JFT ASB JC MDi EL AA MDu EGD GD GKD HA SZ LV CC. Wrote the paper: OD KDM CC.
Q fever is a highly infectious disease with a worldwide distribution. Its causative agent, the intracellular bacterium
How virulent infectious diseases emerge from non-pathogenic organisms is a challenging question. Here, we address this evolutionary issue in the case of Q fever. Its causative agent, the intracellular bacterium
‘Query fever’ (Q fever) is a highly infectious zoonotic disease first identified in 1937 [
The evolutionary origin of Q fever is unclear since the
The
Here, we examine the origin of the Q fever pathogen,
We performed an extensive screening for the presence of
Square size indicates the number of populations sampled per geographic area. Numbers refer to the tick species whereas letters discriminate the different populations screened within a species; this nomenclature is detailed in
Tick species | Sample sites | Tick host species or habitat | n | |||
---|---|---|---|---|---|---|
Argasidae (soft ticks) | ||||||
1 - | 1-A, Porto Velho, Rondonia, Brazil | Bat guano in cave | 4 | 0.00 (0) | 0.00 (0) | |
2 - | 2-A, Chaco, Argentina | Unknown | 3 | 1.00 (3) | 0.00 (0) | |
3 - | 3-A, Lobos de Tierra Island, Peru, 2009 | Peruvian Pelican ( |
5 | 1.00 (5) | 0.00 (0) | |
4 - | 4-A, Sao Francisco de Paula,Brazil | Unknown | 3 | 1.00 (3) | 0.00 (0) | |
5 - | 5-A, Juan de Nova Island, Mozambic Channel, 2011 | Sooty Tern ( |
28 | 1.00 (28) | 0.00 (0) | |
5-B, Réunion Island | Sea bird nests | 3 | 1.00 (3) | 0.00 (0) | ||
6 - | 6-A, Kenitra, Morocco, 2006 | Rodent burrows | 7 | 0.00 (0) | 1.00 (7) | |
6-B, Sidi Akhfennir, Morocco, 2006 | Rodent burrows | 18 | 0.00 (0) | 1.00 (18) | ||
6-C, Boujdour, Morocco, 2006 | Rodent burrows | 2 | 0.00 (0) | 1.00 (2) | ||
6-D, El Argoub, Morocco, 2006 | Rodent burrows | 2 | 0.00 (0) | 1.00 (2) | ||
6-E, Lahmiris, Morocco, 2010 | Rodent burrows | 1 | 0.00 (0) | 1.00 (1) | ||
6-F, Mostaganem, Algeria, 2012 | Rodent burrows | 4 | 0.00 (0) | 1.00 (4) | ||
6-G, Oudhna, Tunisia, 2010 | Rodent burrows | 4 | 0.00 (0) | 1.00 (4) | ||
7 - | 7-H, unknown | Sea bird nests | 1 | 1.00 (1) | 0.00 (0) | |
8 - | 8-A, La Calle, Tunisia, 2009 | Rodent burrows | 1 | 1.00 (1) | 0.00 (0) | |
8-B, Taher, Algeria, 2010 | Rodent burrows | 2 | 1.00 (2) | 0.00 (0) | ||
9 - | 9-A, Kairouan, Tunisia, 2010 | Rodent burrows | 3 | 1.00 (3) | 0.00 (0) | |
10 - | 10-A, Medes Island, Spain, 2009 | Yellow-legged Gull ( |
20 | 1.00 (20) | 0.00 (0) | |
10-B, Zembra Island, Tunisia, 2009 | Yellow-legged Gull ( |
20 | 1.00 (20) | 0.00 (0) | ||
10-C, Carteau, France, 2014 | Yellow-legged Gull ( |
8 | 1.00 (8) | 0.00 (0) | ||
11 - | 11-A, Izemmourèn, Morocco, 2009 | Rodent burrows | 1 | 1.00 (1) | 0.00 (0) | |
11-B, Berkane Oued Kiss, Morocco, 2006 | Rodent burrows | 1 | 1.00 (1) | 0.00 (0) | ||
11-C, Bir-Jdid, Morocco, 2009 | Rodent burrows | 1 | 1.00 (1) | 0.00 (0) | ||
12 - | 12-A, Guelmin, Morocco, 2006 | Rodent burrows | 1 | 0.00 (0) | 1.00 (1) | |
12-B, Sidi Akhfennir, Morocco, 2006 | Rodent burrows | 2 | 0.00 (0) | 1.00 (2) | ||
13 - | 13-A, Laboratory strain derived from field specimens of unknown origin | Unknown | 3 | 0.00 (0) | 0.00 (0) | |
14 - | 14-A, Bizerte, Tunisia, 2010 | Rodent burrows | 1 | 0.00 (0) | 1.00 (1) | |
14-B, Oudhna, Tunisia, 2010 | Rodent burrows | 2 | 0.00 (0) | 1.00 (2) | ||
15 - | 15-A, Fes, Morocco, 2010 | Rodent burrows | 4 | 1.00 (4) | 0.00 (0) | |
15-B, Kenitra, Morocco, 2006 | Rodent burrows | 4 | 1.00 (4) | 0.00 (0) | ||
15-C, Beb-Lerba, Morocco, 2010 | Rodent burrows | 4 | 1.00 (4) | 0.00 (0) | ||
15-D, Oued Choufcherk, Morocco, 2010 | Rodent burrows | 4 | 1.00 (4) | 0.00 (0) | ||
15-E, Bouira, Algeria, 2010 | Rodent burrows | 4 | 1.00 (4) | 0.00 (0) | ||
15-F, Berrouaghia, Algeria, 2010 | Rodent burrows | 4 | 1.00 (4) | 0.00 (0) | ||
15-G, Chlef, Algeria, 2010 | Rodent burrows | 4 | 1.00 (4) | 0.00 (0) | ||
16 - | 16-A, Chile | Common vampire Bat ( |
3 | 1.00 (3) | 0.00 (0) | |
17 - | 17-A, Laboratory strain derived from field specimens collected in Mahitsy, Madagascar, 2008–2010 | Unknown | 3 | 0.00 (0) | 0.00 (0) | |
18 - | 18-A, Salta, Argentina | Environement | 18 | 1.00 (18) | 0.00 (0) | |
18-B, Laboratory strain derived from field specimens collected in Nhecolandi, Pantanal, Brazil | Environement | 4 | 1.00 (4) | 0.00 (0) | ||
19 - | 19-A, Saïda Mt Daïa, Algeria, 2012 | Rodent burrows | 1 | 1.00 (1) | 0.00 (0) | |
19-B, Mostaganem, Algeria, 2012 | Rodent burrows | 2 | 1.00 (2) | 0.00 (0) | ||
20 - | 20-A, Dielmo, Senegal, 2002 | Rodent burrows | 20 | 1.00 (20) | 0.00 (0) | |
20-B, Kanène Khar, Senegal, 2003 | Rodent burrows | 17 | 1.00 (17) | 0.00 (0) | ||
20-C, Richard-Toll, Senegal, 2003 | Rodent burrows | 19 | 1.00 (19) | 0.00 (0) | ||
20-D, Sogoli, Mali, 2007 | Rodent burrows | 10 | 1.00 (10) | 0.00 (0) | ||
20-E, M’Chounèche, Algeria, 2009 | Rodent burrows | 37 | 1.00 (37) | 0.00 (0) | ||
21 - | 21-A, Pan de Azucar, Chile, 2010–2013 | Humboldt penguin ( |
3 | 1.00 (3) | 0.00 (0) | |
22- | 22-A, Boa Vista Island, Cape Verde, 2008 | Cape Verde Shearwater ( |
16 | 1.00 (16) | 0.00 (0) | |
Ixodidae (hard ticks) | ||||||
23 - | 23-A, Laboratory strain derived from field engorged females collected in Oklahoma, USA, 1976–2004 | Unknown | 20 | 1.00 (20) | 0.00 (0) | |
24 - | 24-A, Chapada Gaucha, Brazil, 2013 | Unknown | 3 | 1.00 (3) | 0.00 (0) | |
25 - | 25-A, Petite Ile, La Réunion, 2012 | Wedge-Tailed Shearwater ( |
3 | 1.00 (3) | 0.00 (0) | |
26 - | 26-A, La Réunion | Unknown | 2 | 1.00 (2) | 0.00 (0) | |
27 - | 27-A, Cavaillon, France, 2011 | Vegetation | 1 | 1.00 (1) | 0.00 (0) | |
27-B, Les Plantiers, France, 2013 | Vegetation | 1 | 1.00 (1) | 0.00 (0) | ||
28 - | 28-A, Hopland, Mendocino Co, California, 1985 | Environement | 6 | 0.00 (0) | 0.00 (0) | |
29 - | 29-A, Proveysieux, France, 2011 | Vegetation | 1 | 0.00 (0) | 0.00 (0) | |
30 - | 30-A, Laboratory strain derived from field specimens collected in Xiaowutai National Natural Reserve Area, China | 2 | 1.00 (2) | 0.00 (0) | ||
31 - | 31-A, Queen's biology station, Ontario, Canada, 2013 | Vegetation | 2 | 0.00 (0) | 0.00 (0) | |
32 - | 32-A, East Sussex, England, 2011 | Vegetation | 5 | 1.00 (5) | 0.00 (0) | |
33 - | 33-A, Zimbabwe, 1998 | Zebu ( |
3 | 0.00 (0) | 0.00 (0) | |
34 - | 34-A, Veneguera, Canaries, 2010 | Vegetation | 2 | 0.00 (0) | 0.00 (0) | |
35 - | 35-A, Bretagne, France, 2008 | Eurasian Collared Dove ( |
1 | 0.00 (0) | 0.00 (0) | |
36- | 36-A, Bretagne, France, 2008 | European Red Fox ( |
1 | 1.00 (1) | 0.00 (0) | |
36-B, Beaumont-Monteux, France, 2008 | European Hedgehog ( |
2 | 1.00 (1) | 0.00 (0) | ||
37 - | 37-A, Crozet Archipelago, 2003 | Sea bird nests | 2 | 0.00 (0) | 0.00 (0) | |
38 - | 38-A, Hopland, Mendocino Co, California, 1985 | Environement | 6 | 0.00 (0) | 0.00 (0) | |
39 - | 39-A, Oulu, Finland, 2011 | Vegetation | 3 | 0.00 (0) | 0.00 (0) | |
40 - | 40-A, Lehmäsaari, Finland, 2011 | Vegetation | 20 | 0.00 (0) | 0.00 (0) | |
40-B, Rioja, Spain, 2011 | Vegetation | 20 | 0.00 (0) | 0.00 (0) | ||
40-C, Mafra, Portugal, 2013 | Vegetation | 16 | 0.00 (0) | 0.00 (0) | ||
40-D, Neuchâtel, Switzerland, 2012 | Vegetation | 16 | 0.00 (0) | 0.00 (0) | ||
40-E, Chur, Switzerland, 2012 | Hazel grouse ( |
4 | 0.00 (0) | 0.00 (0) | ||
40-F, Sénart, France, 2010 | European Roe Deer ( |
22 | 0.00 (0) | 0.05 (1) | ||
40-G, Ain, France, 2004 | Vegetation | 2 | 1.00 (1) | 0.00 (0) | ||
41 - | 41-A, Queen's biology station, Ontario, Canada, 2013 | Vegetation | 3 | 0.00 (0) | 0.00 (0) | |
42 - | 42-A, Kilarney Circuit, Coolangubra, Australia, 1982 | Common Wombat (Vo |
2 | 0.00 (0) | 1.00 (2) | |
43 - | 43-A, Ariy Kamen Islet, Kamchatka, Russia, 2008 | Black-legged Kittiwake ( |
4 | 0.00 (0) | 0.00 (0) | |
44 - | 44-A, Possession Island, Crozet Archipelago, 2003 | King Penguin ( |
20 | 0.00 (0) | 0.00 (0) | |
44-B, Hornoeya Island, Norway, 2010 | Brünnich's Guillemot ( |
20 | 0.00 (0) | 0.00 (0) | ||
44-C, Triangle Island, Canada, 2010 | Rhinoceros Auklet ( |
14 | 0.50 (7) | 0.00 (0) | ||
44-D, Pitchie2, Kamchatka, Russia, 2008 | Red-faced Cormorant ( |
20 | 0.00 (0) | 0.00 (0) | ||
44-E, Grimsey, Iceland, 2003 | Atlantic Puffin ( |
25 | 0.00 (0) | 0.20 (5) | ||
45 - | 45-A, Guiglo, Ivory Coast, 1994 | Leopard ( |
12 | 1.00 (12) | 0.00 (0) | |
46 - | 46-A, Guiglo, Ivory Coast, 1994 | Dog ( |
12 | 1.00 (12) | 0.00 (0) | |
47 - | 47-A, Burkina-Faso, 2013 | Zebu ( |
17 | 1.00 (17) | 0.00 (0) | |
47-B, Gogonou, Benin, 2012 | Zebu ( |
5 | 1.00 (5) | 0.00 (0) | ||
48 - | 48-A, CCA Farm, New Caledonia, 2003 | Cattle ( |
12 | 1.00 (12) | 0.00 (0) | |
48-B, BMMMM Farm, New Caledonia, 2003 | Cattle ( |
12 | 1.00 (12) | 0.00 (0) | ||
49 - | 49-A, Italia | Cattle ( |
2 | 1.00 (2) | 0.00 (0) | |
50- | 50-A, Burkina-Faso, 2013 | Zebu ( |
20 | 0.95 (19) | 0.00 (0) | |
50-B, Gogonou, Benin, 2012 | Zebu ( |
9 | 1.00 (9) | 0.00 (0) | ||
50-C, Sandvelt, South Africa, 2011 | Blue Wildebeest (Connochaetes taurinus), Greater Kudu ( |
20 | 1.00 (20) | 0.00 (0) | ||
50-D, Queenstown, South Africa, 2011 | Zebu ( |
17 | 1.00 (17) | 0.00 (0) | ||
50-E, Vaalwater, South Africa, 2010 | Zebu ( |
19 | 1.00 (19) | 0.00 (0) | ||
50-F, Lephalale, South Africa, 2010 | South African Giraffe ( |
9 | 1.00 (9) | 0.00 (0) | ||
50-G, Zimbabwe, 1998 | Impala ( |
11 | 1.00 (11) | 0.00 (0) | ||
51 - | 51-A, Zimbabwe, 1998 | Zebu ( |
8 | 1.00 (8) | 0.00 (0) | |
52 - | 52-A, Burkina-Faso, 2013 | Zebu ( |
18 | 0.94 (17) | 0.00 (0) | |
52-B, Gogonou, Benin, 2012 | Zebu ( |
3 | 1.00 (3) | 0.00 (0) | ||
53 - | 53-A, Kpinnou, Benin, 2012 | Zebu ( |
20 | 1.00 (20) | 0.00 (0) | |
53-B, Ambalanirana, Madagascar, 2013 | Zebu ( |
18 | 1.00 (18) | 0.00 (0) | ||
53-C, Imeritsiatosika, Madagascar, 2013 | Zebu ( |
14 | 1.00 (14) | 0.00 (0) | ||
53-D, Eglinton, South Africa, 2011 | Zebu ( |
20 | 1.00 (20) | 0.00 (0) | ||
53-E, Welverdiemda, South Africa, 2011 | Zebu ( |
11 | 1.00 (11) | 0.00 (0) | ||
53-F, Laboratory strain derived from field engorged females collected in Kpinnou, Benin, 2012 | Girolando (Cattle x Zebu hybrid) | 7 | 1.00 (7) | 0.00 (0) | ||
54 - | 54-A, Gard, France, 2006 | Vegetation | 2 | 1.00 (2) | 0.00 (0) | |
55- | 55-A, Brazil | Dog ( |
1 | 1.00 (1) | 0.00 (0) | |
55-B, Montferrier-sur-Lez, France, 2013 | Dog ( |
1 | 1.00 (1) | 0.00 (0) | ||
56 - | 56-A, Italia | Vegetation | 2 | 1.00 (2) | 0.00 (0) | |
56-B, Kerkyra, Greece, 2012 | Human ( |
3 | 1.00 (3) | 0.00 (0) | ||
57- | 57-A, Guiglo area, Ivory Coast, 1994 | Leopard ( |
3 | 1.00 (3) | 0.00 (0) | |
58- | 58-A, Guiglo, Ivory Coast, 1994 | Dog ( |
2 | 1.00 (2) | 0.00 (0) |
Using this procedure, all the tick-borne bacteria we detected belong to the Legionellales order and can be unambiguously assigned either to
Other Legionellales bacteria of the genus
To characterize
The overall dataset included 33 to 40 alleles per bacterial gene (
Locus | Function | L | Strains | Ni | Pnsi | Na | Ps | Ad | π | D |
---|---|---|---|---|---|---|---|---|---|---|
16S rRNA | Small ribosomal subunit | 1066 | 85 | 93.0–100 | 40 | 262 | 0.985 | 0.038 | 39.960 | |
15 | 99.7–100 | 4 | 4 | 0.552 | 0.001 | 1.224 | ||||
23S rRNA | Large ribosomal subunit | 496 | 82 | 84.2–100 | 34 | 177 | 0.978 | 0.079 | 39.393 | |
15 | 99.4–100 | 2 | 2 | 0.133 | 0.001 | 0.267 | ||||
Chaperone protein GROEL | 550 | 82 | 68.7–100 | 37 | 292 | 0.982 | 0.179 | 98.527 | ||
15 | 99.4–100 | 5 | 5 | 0.562 | 0.002 | 0.895 | ||||
DNA-directed RNA polymerase beta chain | 474 | 85 | 68.7–100 | 38 | 250 | 0.981 | 0.205 | 97.136 | ||
15 | 99.3–100 | 4 | 4 | 0.467 | 0.001 | 0.648 | ||||
Chaperone protein DNAK | 423 | 74 | 69.6–100 | 33 | 227 | 0.979 | 0.177 | 75.789 | ||
15 | 99.8–100 | 3 | 1 | 0.362 | 0.001 | 0.381 | ||||
Full concatenated data set | 3009 | 71 | 81.8–100 | 36 | 1139 | 0.984 | 0.115 | 346.990 | ||
15 | 99.6–100 | 7 | 16 | 0.781 | 0.001 | 2.933 |
Analyses are based on nucleotide sequences of five housekeeping genes, excluding sites with alignment gaps and/or missing data. L, sequence fragment length in base pairs; Ni, Number of examined strains; Pnsi, Pairwise nucleotide sequence identity (%); Na, number of alleles; Ps, number of polymorphic sites; Ad, allelic diversity; π, nucleotide diversity; D, average number of nucleotide differences between sequences.
We constructed a multi-gene phylogeny of the entire
The four
The partitioning of
Further analyses were conducted by examining public repositories of DNA sequencing data generated by the whole genome sequencing (WGS) projects of the cattle tick
(a) Percent identity of 50 genes uniquely attributable to
It should be noted that the
We next compared the metabolic requirements of
Since its original description,
Three complementary lines of argument indicate a much longer evolutionary history for
We identified
Another question remains concerning the degree of vertebrate infection risk by the
The reasons why
The evolutionary transition observed within the
In conclusion, we show that
The examined specimens represent the two main tick families, nine genera, 58 species and 112 populations from around the world (
Tick DNA was individually extracted using the DNeasy Blood & Tissue Kit (QIAGEN) following manufacturer instructions. DNA template quality was systematically verified by PCR amplification of the 18S ribosomal RNA (18S rRNA) or the cytochrome oxydase 1 (
The GBLOCKS program [
Phylogenetic analyses were based on single and concatenated sequences of the five bacterial genes used in the multi-locus typing scheme and on the 50
We first assessed the ability of tick-borne
Nucleotide sequences of PCR-amplified fragments of tick-borne
Genes and primers used in polymerase chain reaction (PCR) assays to detect Coxiella and relatives and to control tick DNA quality. The same primers were used for the
(DOCX)
We are grateful to X. Bailly, A. Barbour, L. Beati, T. Boulinier, J.L. Chapuis, F. Dantas-Torres, A. Estrada-Peña, M. Gauthier-Clerc, L. Gern, D. González Acuña, J. Gonzalez-Solis, U. Guidon, A. Guglielmone, K. Hansford, M. Hipfner, A. Jaeger, D. Jenny, M. Labruna, R. Lane, M.S. Latrofa, C. Lebarbenchon, J. Liu, J. Medlock, S. Nava, A.C. Norte, U.E. Schneppat, D. Spratt, P. Tortosa and M. Vittecoq for help at different stages of this work, and to three anonymous reviewers for helpful comments and suggestions.