[KSCI] Korea Science Citation Index Service

http://dx.doi.org/10.4142/jvs.2021.22.e37

Characterization of microbiota diversity of engorged ticks collected from dogs in China

Wang, Seongjin (Epidemiological Investigation Analysis, Korea Disease Control and Prevention Agency)
Hua, Xiuguo (Shanghai Key Laboratory of Veterinary Biotechnology, Shanghai Jiao Tong University)
Cui, Li (Shanghai Key Laboratory of Veterinary Biotechnology, Shanghai Jiao Tong University)

Publication Information

Journal of Veterinary Science / v.22, no.3, 2021 , pp. 37.1-37.14 More about this Journal

Abstract

Background: Ticks are one of the most common external parasites in dogs, and are associated with the transmission of a number of major zoonoses, which result in serious harm to human health and even death. Also, the increasing number of pet dogs and pet owners in China has caused concern regarding human tick-borne illnesses. Accordingly, studies are needed to gain a complete understanding of the bacterial composition and diversity of the ticks that parasitize dogs. Objectives: To date, there have been relatively few reports on the analysis of the bacterial community structure and diversity in ticks that parasitize dogs. The objective of this study was to investigate the microbial composition and diversity of parasitic ticks of dogs, and assessed the effect of tick sex and geographical region on the bacterial composition in two tick genera collected from dogs in China. Methods: A total of 178 whole ticks were subjected to a 16S ribosomal RNA (rRNA) next generation sequencing analysis. The Illumina MiSeq platform targeting the V3-V4 region of the 16S rRNA gene was used to characterize the bacterial communities of the collected ticks. Sequence analysis and taxonomic assignment were performed using QIIME 2 and the GreenGene database, respectively. After clustering the sequences into taxonomic units, the sequences were quality-filtered and rarefied. Results: After pooling 24 tick samples, we identified a total of 2,081 operational taxonomic units, which were assigned to 23 phyla and 328 genera, revealing a diverse bacterial community profile. The high, moderate and low prevalent taxa include 46, 101, and 182 genera, respectively. Among them, dominant taxa include environmental bacterial genera, such as Psychrobacter and Burkholderia. Additionally, some known tick-associated endosymbionts were also detected, including Coxiella, Rickettsia, and Ricketssiella. Also, the potentially pathogenic genera Staphylococcus and Pseudomonas were detected in the tick pools. Moreover, our preliminary study found that the differences in microbial communities are more dependent on the sampling location than tick sex in the tick specimens collected from dogs. Conclusions: The findings of this study support the need for future research on the microbial population present in ticks collected from dogs in China.

Keywords

Microbiome; China; tick; microbial community; dog;

Citations & Related Records

Reference

1	Greay TL, Gofton AW, Paparini A, Ryan UM, Oskam CL, Irwin PJ. Recent insights into the tick microbiome gained through next-generation sequencing. Parasit Vectors. 2018;11(1):12. DOI
2	Cusco A, Sanchez A, Altet L, Ferrer L, Francino O. Individual signatures define canine skin microbiota composition and variability. Front Vet Sci 2017;4:6. DOI
3	Rodrigues Hoffmann A, Patterson AP, Diesel A, Lawhon SD, Ly HJ, Elkins Stephenson C, et al. The skin microbiome in healthy and allergic dogs. PLoS One. 2014;9(1):e83197. DOI
4	Khoo JJ, Chen F, Kho KL, Ahmad Shanizza AI, Lim FS, Tan KK, et al. Bacterial community in Haemaphysalis ticks of domesticated animals from the Orang Asli communities in Malaysia. Ticks Tick Borne Dis. 2016;7(5):929-937. DOI
5	Poirier S, Rue O, Peguilhan R, Coeuret G, Zagorec M, Champomier-Verges MC, et al. Deciphering intraspecies bacterial diversity of meat and seafood spoilage microbiota using gyrB amplicon sequencing: a comparative analysis with 16S rDNA V3-V4 amplicon sequencing. PLoS One. 2018;13(9):e0204629. DOI
6	Zhang XC, Yang ZN, Lu B, Ma XF, Zhang CX, Xu HJ. The composition and transmission of microbiome in hard tick, Ixodes persulcatus, during blood meal. Ticks Tick Borne Dis. 2014;5(6):864-870. DOI
7	Ravi A, Ereqat S, Al-Jawabreh A, Abdeen Z, Abu Shamma O, Hall H, et al. Metagenomic profiling of ticks: Identification of novel rickettsial genomes and detection of tick-borne canine parvovirus. PLoS Negl Trop Dis. 2019;13(1):e0006805. DOI
8	Vila A, Estrada-Pena A, Altet L, Cusco A, Dandreano S, Francino O, et al. Endosymbionts carried by ticks feeding on dogs in Spain. Ticks Tick Borne Dis. 2019;10(4):848-852. DOI
9	Chermprapai S, Ederveen TH, Broere F, Broens EM, Schlotter YM, van Schalkwijk S, et al. The bacterial and fungal microbiome of the skin of healthy dogs and dogs with atopic dermatitis and the impact of topical antimicrobial therapy, an exploratory study. Vet Microbiol. 2019;229:90-99. DOI
10	Andersson MO, Tolf C, Tamba P, Stefanache M, Radbea G, Frangoulidis D, et al. Molecular survey of neglected bacterial pathogens reveals an abundant diversity of species and genotypes in ticks collected from animal hosts across Romania. Parasit Vectors. 2018;11(1):144. DOI
11	Zhang R, Huang Z, Yu G, Zhang Z. Characterization of microbiota diversity of field-collected Haemaphysalis longicornis (Acari: Ixodidae) with regard to sex and blood meals. J Basic Microbiol. 2019;59(2):215-223. DOI
12	Earl JP, Adappa ND, Krol J, Bhat AS, Balashov S, Ehrlich RL, et al. Species-level bacterial community profiling of the healthy sinonasal microbiome using Pacific biosciences sequencing of full-length 16S rRNA genes. Microbiome. 2018;6(1):190. DOI
13	Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7(5):335-336. DOI
14	Duan D, Cheng T. Determination of the microbial community features of Haemaphysalis flava in different developmental stages by high-throughput sequencing. J Basic Microbiol. 2017;57(4):302-308. DOI
15	DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72(7):5069-5072. DOI
16	R Core Team. R: a Language and Environment for Statistical Computing. Vienna: R Core Team; 2013.
17	Elbir H, Almathen F, Alhumam NA. A glimpse of the bacteriome of Hyalomma dromedarii ticks infesting camels reveals human Helicobacter pylori pathogen. J Infect Dev Ctries. 2019;13(11):1001-1012. DOI
18	Li LH, Zhang Y, Zhu D. Effects of antibiotic treatment on the fecundity of Rhipicephalus haemaphysaloides ticks. Parasit Vectors. 2018;11(1):242. DOI
19	Lalzar I, Harrus S, Mumcuoglu KY, Gottlieb Y. Composition and seasonal variation of Rhipicephalus turanicus and Rhipicephalus sanguineus bacterial communities. Appl Environ Microbiol. 2012;78(12):4110-4116. DOI
20	Chomel B. Tick-borne infections in dogs-an emerging infectious threat. Vet Parasitol. 2011;179(4):294-301. DOI
21	Ruiling Z, Zhendong H, Guangfu Y, Zhong Z. Characterization of the bacterial community in Haemaphysalis longicornis (Acari: Ixodidae) throughout developmental stages. Exp Appl Acarol. 2019;77(2):173-186. DOI
22	Zhang YK, Zhang XY, Liu JZ. Ticks (Acari: Ixodoidea) in China: Geographical distribution, host diversity, and specificity. Arch Insect Biochem Physiol. 2019;102(3):e21544. DOI
23	Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics. 2010;26(19):2460-2461. DOI
24	Dantas-Torres F, Otranto D. Best practices for preventing vector-borne diseases in dogs and humans. Trends Parasitol. 2016;32(1):43-55. DOI
25	Wang S, Zhao T, Yu X, Lin Z, Hua X, Cui L. Characterization of tick viromes collected from dogs in China. Biosaf Health. 2020;2(2):79-88. DOI
26	Zhang J, Liu Q, Wang D, Li W, Beugnet F, Zhou J. Epidemiological survey of ticks and tick-borne pathogens in pet dogs in south-eastern China. Parasite. 2017;24:35. DOI
27	Jones EH, Hinckley AF, Hook SA, Meek JI, Backenson B, Kugeler KJ, et al. Pet ownership increases human risk of encountering ticks. Zoonoses Public Health. 2018;65(1):74-79. DOI
28	Mira A, Moran NA. Estimating population size and transmission bottlenecks in maternally transmitted endosymbiotic bacteria. Microb Ecol. 2002;44(2):137-143. DOI
29	Rene-Martellet M, Minard G, Massot R, Tran Van V, Valiente Moro C, Chabanne L, et al. Bacterial microbiota associated with Rhipicephalus sanguineus (s.l.) ticks from France, Senegal and Arizona. Parasit Vectors. 2017;10(1):416. DOI
30	Smith TA, Driscoll T, Gillespie JJ, Raghavan R. A Coxiella-like endosymbiont is a potential vitamin source for the Lone Star tick. Genome Biol Evol. 2015;7(3):831-838. DOI
31	Gottlieb Y, Lalzar I, Klasson L. Distinctive genome reduction rates revealed by genomic analyses of two coxiella-like endosymbionts in ticks. Genome Biol Evol. 2015;7(6):1779-1796. DOI
32	Kageyama D, Narita S, Watanabe M. Insect sex determination manipulated by their endosymbionts: incidences, mechanisms and implications. Insects. 2012;3(1):161-199. DOI
33	Hunter DJ, Torkelson JL, Bodnar J, Mortazavi B, Laurent T, Deason J, et al. The rickettsia endosymbiont of ixodes pacificus contains all the genes of de novo folate biosynthesis. PLoS One. 2015;10(12):e0144552. DOI
34	He XM, Cheng TY. Tick saliva microbiomes isolated from engorged and partially fed adults of Haemaphysalis flava tick females. J Appl Entomol. 2018;142(1-2):173-180. DOI
35	Bonwitt J, Tran M, Droz A, Gonzalez A, Glover WA. Psychrobacter sanguinis wound infection associated with marine environment exposure, Washington, USA. Emerg Infect Dis. 2018;24(10):1942-1944. DOI
36	Meason-Smith C, Older CE, Ocana R, Dominguez B, Lawhon SD, Wu J, et al. Novel association of Psychrobacter and Pseudomonas with malodour in bloodhound dogs, and the effects of a topical product composed of essential oils and plant-derived essential fatty acids in a randomized, blinded, placebo-controlled study. Vet Dermatol. 2018;29(6):465-e158. DOI
37	Weese JS. The canine and feline skin microbiome in health and disease. Vet Dermatol. 2013;24(1):137-145.e31. DOI
38	Fastres A, Roels E, Vangrinsven E, Taminiau B, Jabri H, Bolen G, et al. Assessment of the lung microbiota in dogs: influence of the type of breed, living conditions and canine idiopathic pulmonary fibrosis. BMC Microbiol. 2020;20(1):84. DOI
39	Muturi EJ, Dunlap C, Ramirez JL, Rooney AP, Kim CH. Host blood-meal source has a strong impact on gut microbiota of Aedes aegypti. FEMS Microbiol Ecol 2019;95(1):1-9.