MALDI-TOF MS identification of ticks of domestic and wild animals in Algeria and molecular detection of associated microorganisms

doi:10.1016/j.cimid.2018.05.002

Comparative Immunology, Microbiology and Infectious Diseases

Volume 57, April 2018, Pages 39-49

https://doi.org/10.1016/j.cimid.2018.05.002 Get rights and content

Highlights

•
This paper assessed MALDI-TOF MS technique to identify ticks sampled on several hosts and investigated tick-borne diseases.
•
Knowledge about tick biodiversity in northeastern Algeria has been updated.
•
93.48% of the tested ticks were correctly identified using MALDI-TOF MS technique.
•
First report of Rickettsia africae and Wolbachia sp. in hard ticks from northeastern Algeria.
•
First molecular detection of Anaplasma phagocytophilum in Argas persicus soft ticks in Algeria.

Abstract

Recent studies have reported the reliability of MALDI-TOF MS for arthropod identification, including fresh or alcohol-preserved ticks based on leg-derived mass spectra. The aim of this study was to evaluate the performance of MALDI-TOF MS for the identification of alcohol-preserved Algerian ticks collected from different domestic and wild hosts. Secondly, we conducted a molecular survey to detect the presence of bacterial DNA in all ticks that were previously subjected to MALDI-TOF MS. A total of 2635 ixodid and 1401 argasid ticks belonging to 9 distinct species were collected in nine different regions of northeastern Algeria. The legs of 230 specimens were subjected to MALDI-TOF MS assays. Spectral analysis revealed intra-species similarity and inter-species specificity for the MS spectra, which was consistent with the morphological identification. Blind tests against the in-lab database revealed that 93.48% of the tested specimens were correctly identified. The accuracy of the morphological and MALDI-TOF MS identifications was validated by sequencing the 12S ribosomal RNA gene (rRNA) for 33 specimens and all the ticks were correctly identified. The quantitative PCR screening showed that for 219 tested ticks, 15 were positive for Rickettsia spp., 8 for Borrelia spp. and 17 for Anaplasmataceae. The PCR tests were negative for Coxiella burnetii and Bartonella spp. This study supports MALDI-TOF MS being a reliable tool for the identification of arthropods and brings new data that sheds light on tick species diversity and tick-borne diseases in Algeria.

Introduction

Ticks (Acari: Ixodidae and Argasidae) are currently recognized as efficient vectors of a wide panel of pathogens, including bacteria, protozoa, viruses and helminths [[1], [2], [3], [4], [5]]. Identified as the second vector of human diseases after mosquitoes [3,6], their medical and veterinary importance cannot be overlooked.

More than 896 tick species are currently identified worldwide [7]. The first surveys on ticks and their geographical distribution in Algeria were conducted during the period 1922–1924 by Senevet [[8], [9], [10]]. This work, when associated with other later work, [11,12] provided the initial primary data on tick species and their distribution.

In recent years, several studies have focused on tick-borne diseases in Algeria, particularly rickettsioses [1,[13], [14], [15], [16]] but also Crimean-Congo hemorrhagic fever virus (CCHFV) [17].

All the previous data on tick species were gathered with identification of ticks by the morphotaxonomy methods based on specific phenotypic criteria for each species [18]. This process is considered a skill challenge especially when taxonomic keys are not available.

Recently, the matrix-assisted laser desorption/ionization time-of-flight mass spectrometry (MALDI-TOF) technique has been presented as an alternative tool for arthropod identification [19,20]. Particularly, the efficiency and accuracy of MALDI-TOF MS technique to identify tick species using the protein extract of the legs has been emphasized through several studies [[21], [22], [23], [24]]. However, to validate the tick identification using this MS technique, the generated spectra have to be queried against a preconceived database.

Our goals were to gather information on tick biodiversity in northeastern Algeria, to assess the discriminatory power of the MALDI-TOF MS technique to identify ticks, and to investigate by molecular tools the presence of zoonotic bacteria associated with these arthropods.

Section snippets

Study areas and period of collection

The study was conducted from June 2015 to September 2016 in nine (9) different regions of the extreme northeast of Algeria: El Tarf (36°51′21.5″N, 8°19′34.5″E); Annaba (36°54′15″N, 7°45′7″E); Guelma (36°28′0″N, 7°26′0″E); Souk Ahras (36°17′14.84″N, 7°57′14.77″E); Skikda (36°52′0″N, 6°54′0″E); Mila (36°27′0″N, 6°16′0″E); Sétif (36°9′0″N, 5°26′0″E); M’Sila (35° 42′6.9″N, 4°32′49.08″E) and Jijel (36°47′04.7″N 5°54′32.0″E). These regions belong to different bioclimatic stages which can range from

Tick collection and morphological identification

A total of 2635 (1028 males and 1607 females) Ixodid adult ticks and 1401 Argasid (535 males and 866 females) ticks were collected from more than 207 infested animals in nine regions of the extreme northeast of Algeria. The outputs of the morphological identification were confirmed by both laboratories (Algeria and France).

For the Ixodid ticks, eight different species belonging to four genera were identified. The most frequent tick was Rh. (Bo.) annulatus with 1898 (72.03%) specimens collected

Discussion

In recent years, the identification of bacteria in clinical bacteriological laboratories has considerably progressed thanks to the introduction of MALDI-TOF MS as a standard profiling tool [24,29,30]. It is known that this technique is fast to implement, that it is precise, and that the linear data generated are relatively simple to interpret and inexpensive to obtain contrary to the usual tools.

The spectra generated by MALDI-TOF MS devices are very informative and are considered to be a unique

Conclusion

The results of the blind test against the updated database were consistent with those of molecular and morphological identification. These results proved the accuracy of the Algerian MS spectra database and confirm once again the reliability of MALDI-TOF for tick identification. Future applications of the MALDI-TOF MS technique may include tests on different developmental stages of ticks and concomitant identification of a vector and its infectious agents from a unique spectrum. Particular

Author contributions

MB contributed to arthropod collections, performed MALDI-TOF MS analysis, DNA extractions, PCRs, sequencing and prepared the first draft of the paper. ML helped with the experiments, contributed to the manuscript, analyzed the data and coordinated the study. AA helped with ticks sampling. LD helped with authorization papers to collect ticks from hedgehogs. AB contributed to conceiving, designing and coordinating the study. DR Contributed reagents/materials/analysis tools. PP^* conceived,

Competing interests

The authors declared that they have no competing interests.

Acknowledgment

The project leading to this publication has received funding from Excellence Initiative of Aix-Marseille University - A*MIDEX, a French “Investissements d’Avenir” program” ANR-10-IAHU-03.

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MALDI-TOF MS identification of ticks of domestic and wild animals in Algeria and molecular detection of associated microorganisms

Highlights

Abstract

Introduction

Section snippets

Study areas and period of collection

Tick collection and morphological identification

Discussion

Conclusion

Author contributions

Competing interests

Acknowledgment

Microbiol. Infect. Dis.

Microbiol. Infect. Dis.

Ticks Tick-borne Dis.

Microbes Infect.

Ticks Tick-borne Dis.

Trans. R. Soc. Trop. Med. Hyg.

Ticks Tick-borne Dis.

Comp. Immunol. Microbiol. Infect. Dis.

Ticks Tick-borne Dis.

Ticks Tick-borne Dis.

Vet. Parasitol.

Clin. Microbiol. Infect.

Clin. Microbiol. Infect.

Ticks Tick-borne Dis.

Ticks Tick-borne Dis.

Ticks Tick-borne Dis.

Vet. Microbiol.

Vet. Microbiol.

Mol. Phylogenet. Evol.

Infect. Genet. Evol.

Ticks Tick-borne Dis.

Update on tick-borne rickettsioses around the world: a geographic approach

Clin. Microbiol. Rev.

Tick-pathogen interactions and vector competence: identification of molecular drivers for tick-Borne diseases

Front. Cell. Infect. Microbiol.

Ticks and tickborne bacterial diseases in humans: an emerging infectious threat

Clin. Infect. Dis.

Tick-borne infectious diseases in Australia

Med. J. Aust.

Tick paralysis in Australia caused by Ixodes holocyclus Neumann

Ann. Trop. Med. Parasitol.

The global importance of ticks

Parasitology

The Argasidae, Ixodidae and Nuttalliellidae (Acari: Ixodida) of the world: a list of valid species names

Zootaxa

Contribution à l’étude des Ixodidés (IX° note) - Espèces trouvées en Algérie sur les bovins pendant les mois d’été, Archives de l’Institut Pasteur

Afrique du Nord. T2 (Fasc 4)

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Archives de l’Institut Pasteur, Afrique du Nord. T2(Fasc 3)

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Archives de l’Institut Pasteur d’Algérie, Alger. T2(2)

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Les tiques du monde (Acarida, Ixodida): nomenclature, stades décrits, hôtes, répartition (espèces décrites avant le 1/01/96) = The ticks of the world (Acarida, Ixodida): nomenclature, described stages, hosts, distribution (Including New Species Described before 1/01/96)

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