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Bacterial Community in Haemaphysalis Ticks of Domesticated Animals

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Bacterial Community in Haemaphysalis Ticks of Domesticated Animals G Model TTBDIS-662; No. of Pages 9 ARTICLE IN PRESS Ticks and Tick-borne Diseases xxx (2016) xxx–xxx Contents lists available at ScienceDirect Ticks and Tick-borne Diseases journal homepage: www.elsevier.com/locate/ttbdis Bacterial community in Haemaphysalis ticks of domesticated animals from the Orang Asli communities in Malaysia a,b a,b b a,b Jing-Jing Khoo , Fezshin Chen , Kai Ling Kho , Azzy Iyzati Ahmad Shanizza , b a,b a,b a,b,∗ Fang-Shiang Lim , Kim-Kee Tan , Li-Yen Chang , Sazaly AbuBakar a Tropical Infectious Diseases Research and Education Centre (TIDREC), Department of Medical Microbiology, Faculty of Medicine, University of Malaya, Kuala Lumpur 50603, Malaysia b Department of Medical Microbiology, Faculty of Medicine, University of Malaya, Kuala Lumpur 50603, Malaysia a r t i c l e i n f o a b s t r a c t Article history: Ticks are vectors in the transmission of many important infectious diseases in human and animals. Ticks Received 20 January 2016 can be readily found in the semi-forested areas such as the settlements of the indigenous people in Received in revised form 8 April 2016 Malaysia, the Orang Asli. There is still minimal information available on the bacterial agents associated Accepted 20 April 2016 with ticks found in Malaysia. We performed a survey of the bacterial communities associated with ticks Available online xxx collected from domestic animals found in two Orang Asli villages in Malaysia. We collected 62 ticks, microscopically and molecularly identified as related to Haemaphysalis wellingtoni, Haemaphysalis hystri- Keywords: cis and Haemaphysalis bispinosa. Bacterial 16s rRNA hypervariable region (V6) amplicon libraries prepared Microbiome from the tick samples were sequenced on the Ion Torrent PGM platform. We detected a total of 392 pos- Coxiella endosymbiont sible bacterial genera after pooling and sequencing 20 samples, indicating a diverse bacterial community Orang asli Malaysia profile. Dominant taxa include the potential tick endosymbiont, Coxiella. Other dominant taxa include the tick-associated pathogen, Rickettsia, and environmental bacteria such as Bacillus, Mycobacterium, Sphingomonas and Pseudomonas. Other known tick-associated bacteria were also detected, including Anaplasma, Ehrlichia, Rickettsiella and Wolbachia, albeit at very low abundance. Specific PCR was per- formed on selected samples to identify Rickettsia and Coxiella. Sequence of Rickettsia felis, which causes spotted fever in human and cats, was identified in one sample. Coxiella endosymbionts were detected in three samples. This study provides the baseline knowledge of the microbiome of ticks in Malaysia, focusing on tick-associated bacteria affecting the Orang Asli communities. The role of the herein found Coxiella and Rickettsia in tick physiology or disease transmission merits further investigation. © 2016 Published by Elsevier GmbH. 1. Introduction hosts life cycles, they are capable of supporting the transmission of pathogens between hosts, in which humans frequently serve as Ticks are excellent vectors for the transmission of zoonotic the accidental host. Multiple pathogenic agents may also be carried infectious agents, including bacteria, viruses and protozoan par- by an individual tick, which could transmit these pathogens to the asites, between human and animals. Ticks are known to harbor a human hosts during a bite (Carmichael and Fuerst, 2006). Ticks are number of medically-important bacterial species within the Rick- also known to harbor endosymbionts or commensal bacteria. How- ettsia, Anaplasma, Bartonella, Coxiella and Ehrlichia genera (Petney, ever, conventional methods for bacteria identification, including 1993; Philippe et al., 2005). As ticks exhibit two-hosts or three- molecular or cultivation-dependent techniques, limits the detec- tion of non-targeted or unexpected bacteria. With the advent of next-generation sequencing (NGS), scientists are now able to investigate the bacterial community carried by ticks, including ∗ Corresponding author at: Tropical Infectious Diseases Research and Education unexpected bacteria that may have been missed using conventional Centre (TIDREC), Department of Medical Microbiology, Faculty of Medicine, Univer- methods (Andreotti et al., 2011; Carpi et al., 2011; Menchaca et al., sity of Malaya, Kuala Lumpur 50603, Malaysia. 2013; Nakao et al., 2013; Vayssier-Taussat et al., 2013; Williams- E-mail addresses: [email protected] (J.-J. Khoo), [email protected] (F. Chen), [email protected] (K.L. Kho), Newkirk et al., 2014). azzy [email protected] (A.I. Ahmad Shanizza), [email protected] Tick-borne illness, such as tick typhus and ehrlichiosis, in (F.-S. Lim), [email protected] (K.-K. Tan), [email protected] (L.-Y. Chang), humans or animals have been documented in Southeast Asian [email protected] (S. AbuBakar). http://dx.doi.org/10.1016/j.ttbdis.2016.04.013 1877-959X/© 2016 Published by Elsevier GmbH. Please cite this article in press as: Khoo, J.-J., et al., Bacterial community in Haemaphysalis ticks of domesticated animals from the Orang Asli communities in Malaysia. Ticks Tick-borne Dis. (2016), http://dx.doi.org/10.1016/j.ttbdis.2016.04.013 G Model TTBDIS-662; No. of Pages 9 ARTICLE IN PRESS 2 J.-J. Khoo et al. / Ticks and Tick-borne Diseases xxx (2016) xxx–xxx countries (Petney, 1993; Sirisanthana et al., 1994; Sagin et al., 2000; inants and also protection of researchers from potential infectious Tay et al., 2000; Irwin and Jefferies, 2004). Most of the findings were pathogens. Tick samples were first pulverized in liquid nitrogen based on serological or microscopic examinations of blood samples using chilled mortar and pestle, using one set for each sample. from humans or animals, such as domestic dogs or cats, presented Before use, all mortars and pestles were soaked in 10% sodium with symptoms of tick-borne illnesses. Molecular approaches such hypochlorite solution for an hour, rinsed with sterile deionized ◦ as polymerase chain reaction (PCR) have also led to the identi- water and baked at 160 C overnight to eliminate contaminat- fication of pathogenic bacteria, including Rickettsia, Ehrlichia and ing materials as much as possible. The resulting fine powder was Anaplasma in ticks sampled from forests or villages in Thailand, resuspended in 500 ␮L of sterile phosphate-buffered saline (PBS). Philippines, Laos and Malaysia (Hirunkanokpun et al., 2003; Parola An aliquot of the suspension (200 ␮L) was used for DNA extrac- et al., 2003a,b; Kernif et al., 2012; Ybanez et al., 2013; Kho et al., tion using the QIAamp DNA Mini Kit (Qiagen, Hilden, Germany) 2015a,b). according to manufacturer’s protocol. DNA was eluted in 100 ␮L In Malaysia, the indigenous people, also known as the Orang Asli, of Ultrapure DNA/RNA-free distilled water (Invitrogen Life Tech- live in remote villages or settlements within or nearing the trop- nologies, MA, USA). Mock extraction was performed in parallel ical rainforests in the Malay peninsula or the Borneo island. The using the same lot of reagents. DNA concentration was determined livelihood of most of these communities is still very much depen- by spectrophotometry using the Implen Nanophotometer (Implen, dent on the hunting and foraging activities within the forests (Khor Munich, Germany). Molecular identification of the tick samples and Zalilah, 2008). The Orang Asli people also live in close contact were performed using previously published primers for the ampli- with domestic animals such as dogs, cats or chickens, which they fication of the mitochondrial 16 rRNA partial sequence (Black and keep as companion animals or as livestock. As the lifestyle of the Piesman, 1994). Orang Asli involves frequent encounters with wildlife or domestic animals, which are common hosts for ticks, the Orang Asli people 2.3. Preparation of the barcoded 16s rRNA V6 amplicon libraries are at higher risk of contracting accidental tick bites and tick- borne illnesses. There has only been one earlier study investigating The presence of bacteria in the tick samples were detected via the seroprevalence of tick-borne rickettsial infections within the nucleic acid amplification using barcode-tagged primers targeting aboriginal communities in Sarawak, Malaysia (Sagin et al., 2000). the V6 hypervariable region of the 16s rRNA gene (nt 872–1052 of Pathogen detection in ticks from Malaysia has only been reported in the complete 16s rRNA sequence of Escherichia coli, NCBI GenBank a handful of studies, which identified the presence of spotted fever Accession: AJ605115) as previously described (Carpi et al., 2011). group rickettsial species and Coxiella from livestock and domes- The V6 region allows for most discrimination between pathogenic tic animals (Tay et al., 2014; Kho et al., 2015a,b; Koh et al., 2015; and non-pathogenic bacteria (Carpi et al., 2011). The forward Watanabe et al., 2015). Hence, more studies are necessary to deter- primers consisted of the A-adaptor sequence (Ion Torrent-specific TM mine the presence and risks of tick-borne diseases in this region, sequence), an Ion Xpress barcode sequence (Life Technologies, especially within the communities of the Orang Asli. MA, USA) and a GAT linker fused to the 5 end of the 16s rRNA In this study, we sampled ticks found feeding on domestic ani- target sequence. Each of the 20 tick samples was assigned to 1 TM mals kept by the Orang Asli from two villages in Malaysia. We of the 20 barcode sequences (Ion Xpress 77–96) used for sam- investigated the bacterial community harbored by these ticks by ple identification and demultiplication during sequence analysis. using the 16s rRNA V6 hypervariable region amplicon sequencing The reverse primer consisted of a CC linker and the Pi-adaptor approach utilizing the Ion Torrent PGM platform technology. sequence (trP1, Ion Torrent-specific sequence) fused to the 5 end of the 16s rRNA target sequence. For the generation of the V6 ampli- con library, DNA amplification was performed in 50 ␮L reaction 2. Material and methods mixture, containing 2 ␮L of extracted DNA, 2.5 units of Dreamtaq DNA polymerase (Thermo Scientific, MA, USA), 0.2 ␮M of dNTPs 2.1.
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