Skip to main content
Log in

Endosymbiont CLS-HI plays a role in reproduction and development of Haemaphysalis longicornis

  • Published:
Experimental and Applied Acarology Aims and scope Submit manuscript

Abstract

Coxiella-like endosymbiont (CLS-Hl) is a primary endosymbiont of Haemaphysalis longicornis. CLS-Hl infects tick special tissues and its prevalence is 100% in ovaries and Malpighian tubules. Tetracycline was injected into females, which then fed on rabbits also treated with tetracycline. The densities of CLS-Hl were measured by semi-quantitative PCR. CLS-Hl densities in ovaries and Malpighian tubes of H. longicornis had significant effects on engorged weight, feeding time, number of eggs, oviposition period, and hatching period. These findings suggested that CLS-Hl plays a role in the reproduction and development of H. longicornis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Brumin M, Kontsedalov S, Ghanim M (2011) Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype. Insect Sci 18:57–66

    Article  Google Scholar 

  • Camille N, Olivier P, Serra Valentina, Claudia P, Nicola F, Alessandra C, Davide S, Chiara B (2015) Antibiotic treatment of the hard tick Ixodes ricinus: influence on Midichloria mitochondrii load following blood meal. Ticks Tick Borne Dis 6:653–657

    Article  Google Scholar 

  • Chaves S, Neto M, Tenreiro T (2009) Insect-symbiont systems: from complex relationships to biotechnological applications. Biotechnol J 4:1753–1765

    Article  CAS  PubMed  Google Scholar 

  • Chen Z, Yang XJ, Bu FJ, Yang XH, Yang XL, Liu JZ (2010) Ticks (Acari: Ixodoidea: Argasidae, Ixodidae) of China. Exp Appl Acarol 51:393–404

    Article  PubMed  Google Scholar 

  • Dale C, Moran NA (2006) Molecular interactions between bacterial symbionts and their host. Cell 126:453–465

    Article  CAS  PubMed  Google Scholar 

  • Dergousoff SJ, Chilton NB (2010) Detection of a new Arsenophonus-type bacterium in Canadian populations of the Rocky Mountain wood tick, Dermacentor andersoni. Exp Appl Acarol 52:85–91

    Article  CAS  PubMed  Google Scholar 

  • Distel DL, Beaudoin DJ, Morrill W (2002) Coexistence of multiple proteobacterial endosymboionts in the gills of the wood-boring bivalve Lyrodus pedicellatus (Bivalvia: Teredinidae). Appl Environ Microbiol 68:6292–6299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Epis S, Mandrioli M, Genchi M, Montagna M, Sacchi L, Pistone D, Sassera D (2013) Localization of the bacterial symbiont Candidatus Midichloria mitochondtrii within the hard tick Ixodes ricinus by whole-mount FISH staining. Ticks Tick Borne Dis 4:39–45

    Article  PubMed  Google Scholar 

  • Gillespie JJ, Joardar V, Williams KP (2012) A Rickettsia genome overrun by mobile genetic elements provides insight into the acquisition of genes characteristic of an obligate intracellular lifestyle. J Bacteriol 194:376–394

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gosalbes MJ, Latorre A, Lamelas A, Moya A (2010) Genomics of intracellular symbionts in insects. Int J Med Microbiol 300:271–278

    Article  CAS  PubMed  Google Scholar 

  • Guan G, Moreau E, Liu J, Hao X, Ma M, Luo J, Chauvin A, Yin H (2010) Babesia sp. BQ1 (Lintan): molecular evidence of experimental transmission to sheep by Haemaphysalis qinghaiensis and Haemaphysalis longicornis. Parasitol Int 59:265–267

    Article  CAS  PubMed  Google Scholar 

  • Haine ER (2008) Symbiont-mediated protection. Proc Biol Sci 275:353–361

    Article  PubMed  Google Scholar 

  • Hendry TA, Hunter MS, Baltrus DA (2014) The facultative symbiont Rickettsia protects an invasive whitefly against entomopathogenic Pseudomonas syringae strains. Appl Environ Microbiol 80:7161–7168

    Article  PubMed  PubMed Central  Google Scholar 

  • Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE, Tabashnik BE, Chiel E, Duckworth VE, Dennhy TJ, Zchori-Fein E, Hunter MS (2011) Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332:254–256

    Article  CAS  PubMed  Google Scholar 

  • Hoogstraal H, Roberts FH, Kohls GM, Tipton VJ (1968) Review of Haemaphysalis (Kaiseriana) longicornis, Neumann (Resurrected) of Australia, New Zealand, New Caledonia, Fiji, Japan, Korea, and northeastern China and U.S.S.R. and its parthenogenetic and bisexual populations (Ixodoidea, Ixodidae). J Parasitol 54:1197–1213

    Article  CAS  PubMed  Google Scholar 

  • Ivanov IN, Mitkova N, Reye AL, Hübschen JM, Vatcheva-Dobrevska RS, Dobreva EG, Kantardjiev TV, Muller CP (2011) Detection of new Francisella-like tick endosymbionts in Hyalomma spp. and Rhipicephalus spp. (Acari: Ixodidae) from Bulgaria. Appl Environ Microbiol 77:5562–5565

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Klyachko O, Stein BD, Grindle N, Clay K, Fuqua C (2007) Localization and visualization of a Coxiella-type symbiont within the lone star tick, Amblyomma americanum. Appl Environ Microbiol 73:6584–6594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koropatnick TA, Engle JT, Apicella MA, Stabb EV, Goldman WE, McFall-Ngai MJ (2004) Microbial factor-mediated development in a host-bacterial mutualism. Science 306:1186–1188

    Article  CAS  PubMed  Google Scholar 

  • Lee MJ, Chae JS (2010) Molecular detection of Ehrlichia chaffeensis and Anaplasma bovis in the salivary glands from Haemaphysalis longicornis ticks. Vector Borne Zoonotic Dis 10:411–413

    Article  PubMed  Google Scholar 

  • Lee JH, Park HS, Jung KD, Jang WJ, Koh SE, Kang SS, Lee IY, Lee WJ, Kim BJ, Kook YH, Park KH, Lee SH (2003) Identification of the spotted fever group rickettsiae detected from Haemaphysalis longicornis ticks in Korea. Microbiol Immunol 47:301–304

    Article  CAS  PubMed  Google Scholar 

  • Lee JH, Park HS, Jang WJ, Koh SE, Park TK, Kang SS, Kim BJ, Kook YH, Park KH, Lee SH (2004) Identification of the Coxiella sp. detected from Haemaphysalis longicornis ticks in Korea. Microbiol Immunol 48:125–130

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Liu Z, Zhang Y, Yang X, Gao Z (2005) Biology of Dermacentor silvarum (Acari: Ixodidae) under laboratory conditions. Exp Appl Acarol 36:131–138

    Article  PubMed  Google Scholar 

  • Liu LM, Liu JN, Liu Z, Yu ZJ, Xu SQ, Yang XH, Li T, Li SS, Guo LD, Liu JZ (2013) Microbial communities and symbionts in the hard tick Haemaphysalis longicornis (Acari: Ixodidae) from north China. Parasit Vectors 6:310

    Article  PubMed  PubMed Central  Google Scholar 

  • McCutcheon JP, Moran NA (2007) Parallel genomic evolution and metabolic interdependence in an ancient symbiosis. Proc Natl Acad Sci USA 104:19392–19397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moran NA, McCutcheon JP, Nakabachi A (2008) Genomics and evolution of heritable bacterial symbionts. Annu Rev Genet 42:165–190

    Article  CAS  PubMed  Google Scholar 

  • Munderloh UG, Jauron SD, Kurtti TJ (2005) The tick: a different kind of host for human pathogens. In: Goodman JL, Dennis DT, Sonenshine DE (eds) Tick-borne diseases of humans. ASM Press, Washington, pp 37–64

    Google Scholar 

  • Niebylski ML, Schrumpf ME, Burgdorfer W, Fischer ER, Gage KL, Schwan TG (1997) Rickettsia peacockii sp. nov., a new species infecting wood ticks, Demacentor andersoni, in Western Montana. Int J Syst Bacteriol 47:446–452

    Article  CAS  PubMed  Google Scholar 

  • Santos-Garcia D, Vargas-Chavez C, Moya A, Latorre A, Silva FJ (2015) Genome evolution in the primary endosymbiont of whiteflies sheds light on their divergence. Genome Biol Evol 7:873–888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sassera D, Beninati T, Bandi C, Bouman EAP, Sacchi L, Fabbi M, Lo N (2006) Candidatus Midichloria mitochondrii, an endosymbiont of the tick Ixodes ricinus with a unique intramitochondrial lifestyle. Int J Syst Evol Microbiol 56:2535–2540

    Article  CAS  PubMed  Google Scholar 

  • Stouthamer R, Breeuwer JA, Hurst GD (1999) Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol 53:71–102

    Article  CAS  PubMed  Google Scholar 

  • Sun J, Liu Q, Lu L (2008) Coinfection with four genera of bacteria (Borrelia, Bartonella, Anaplasma and Ehrlichia) in Haemaphysalis longicornis and Ixodes sinensis ticks from China. Vector Borne Zoonotic Dis 8:791–795

    Article  PubMed  Google Scholar 

  • Tenquisf JD, Charleston WAG (2001) A revision of the annotated checklist of ectoparasites of terrestrial mammals in New Zealand. J R Soc N Z 31:481–542

    Article  Google Scholar 

  • Tian W, Zhang Z, Moldenhauer S, Guo Y, Yu Q, Wang L, Chen M (1998) Detection of Borrelia burgdorferi from ticks (Acari) in Hebei Province, China. J Med Entomol 35:95–98

    Article  CAS  PubMed  Google Scholar 

  • Todd A, Timothy D, Joseph J, Gillespie Rahul R (2015) A Coxiella-Like endosymbiont is a potential vitamin source for the lone star tick. Genome Biol Evol 7(3):831–838

    Article  Google Scholar 

  • Yu XJ, Liang MF, Zhang SY, Liu Y, Li JD, Sun YL (2011) Fever with thrombocytopenia associated with a novel bunyavirus in China. N Engl J Med 364:1523–1532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu ZJ, Wang H, Wang TH, Sun WY, Yang XL, Liu JZ (2015) Tick-borne pathogens and the vector potential of ticks in China. Parasit Vectors 6:310

    Google Scholar 

  • Zhang X, Norris DE, Rasgon JL (2011) Distribution and molecular characterization of Wolbachia endosymbionts and filarial nematodes in Maryland populations of the lone star tick (Amblyomma americanum). FEMS Microbiol Ecol 77:50–56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhong J, Jasinskas A, Barbour AG (2007) Antibiotic treatment of the tick vector Amblyomma americanum reduced reproductive fitness. PLoS ONE 2(5):e405

    Article  PubMed  PubMed Central  Google Scholar 

  • Zou YX, Jin HT, Wang QY, Fu ZX, Gao HW, Liu PP, Liu Q, Chen LF (2011) Molecular detection of Anaplasma phagocytophilum in Ixodid ticks in Hebei Province, China. Vector Borne Zoonotic Dis 11:1323–1327

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by National Natural Science Foundation of China (Nos. 31672365, 31272372), Key Basic Research Foundation of Hebei Province, China (No. 15966502D).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Jing-Ze Liu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhang, CM., Li, NX., Zhang, TT. et al. Endosymbiont CLS-HI plays a role in reproduction and development of Haemaphysalis longicornis . Exp Appl Acarol 73, 429–438 (2017). https://doi.org/10.1007/s10493-017-0194-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10493-017-0194-y

Keywords

Navigation