Tick Ecdysteroid Hormone, Global Microbiota/ Signaling in the Ovary Versus Carcass During Vitellogenesis in Part-Fed (Virgin) American Dog Ticks,

Overview

Journal Microorganisms

Specialty Microbiology

Date 2021 Jul 2

PMID 34201013

Citations 2

Authors

Loganathan Ponnusamy

Haley Sutton

Robert D Mitchell 3rd

Daniel E Sonenshine

Charles S Apperson

Richard Michael Roe

Affiliations

Soon will be listed here.

Abstract

The transovarial transmission of tick-borne bacterial pathogens is an important mechanism for their maintenance in natural populations and transmission, causing disease in humans and animals. The mechanism for this transmission and the possible role of tick hormones facilitating this process have never been studied. Injections of physiological levels of the tick hormone, 20-hydroxyecdysone (20E), into part-fed (virgin) adult females of the American dog tick, , attached to the host caused a reduction in density of in the carcass and an increase in the ovaries compared to buffer-injected controls. This injection initiates yolk protein synthesis and uptake by the eggs but has no effect on blood feeding. sp. and were the predominant bacteria based on the proportionality in the carcass and ovary. The total bacteria load increased in the carcass and ovaries, and bacteria in the genus increased in the carcass after the 20E injection. The mechanism of how the species respond to changes in tick hormonal regulation needs further investigation. Multiple possible mechanisms for the proliferation of in the ovaries are proposed.

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References

Mitchell 3rd R, Sonenshine D, Perez de Leon A . Vitellogenin Receptor as a Target for Tick Control: A Mini-Review. Front Physiol. 2019; 10:618. PMC: 6537121. DOI: 10.3389/fphys.2019.00618. View

Negri I . Wolbachia as an "infectious" extrinsic factor manipulating host signaling pathways. Front Endocrinol (Lausanne). 2012; 2:115. PMC: 3356060. DOI: 10.3389/fendo.2011.00115. View

Tufail M, Takeda M . Molecular characteristics of insect vitellogenins. J Insect Physiol. 2008; 54(12):1447-58. DOI: 10.1016/j.jinsphys.2008.08.007. View

Roe R, Donohue K, Khalil S, Sonenshine D . Hormonal regulation of metamorphosis and reproduction in ticks. Front Biosci. 2008; 13:7250-68. DOI: 10.2741/3226. View

Sonenshine D, Hynes W, Ceraul S, Mitchell R, Benzine T . Host blood proteins and peptides in the midgut of the tick Dermacentor variabilis contribute to bacterial control. Exp Appl Acarol. 2005; 36(3):207-23. DOI: 10.1007/s10493-005-2564-0. View

Van Treuren W, Ponnusamy L, Brinkerhoff R, Gonzalez A, Parobek C, Juliano J . Variation in the Microbiota of Ixodes Ticks with Regard to Geography, Species, and Sex. Appl Environ Microbiol. 2015; 81(18):6200-9. PMC: 4542252. DOI: 10.1128/AEM.01562-15. View

Khalil S, Donohue K, Thompson D, Jeffers L, Ananthapadmanaban U, Sonenshine D . Full-length sequence, regulation and developmental studies of a second vitellogenin gene from the American dog tick, Dermacentor variabilis. J Insect Physiol. 2011; 57(3):400-8. DOI: 10.1016/j.jinsphys.2010.12.008. View

Gouin E, Gantelet H, Egile C, Lasa I, Ohayon H, Villiers V . A comparative study of the actin-based motilities of the pathogenic bacteria Listeria monocytogenes, Shigella flexneri and Rickettsia conorii. J Cell Sci. 1999; 112 ( Pt 11):1697-708. DOI: 10.1242/jcs.112.11.1697. View

Pelzer E, Allan J, Theodoropoulos C, Ross T, Beagley K, Knox C . Hormone-dependent bacterial growth, persistence and biofilm formation--a pilot study investigating human follicular fluid collected during IVF cycles. PLoS One. 2012; 7(12):e49965. PMC: 3514270. DOI: 10.1371/journal.pone.0049965. View

10.

Spieth J, Nettleton M, Lea K, Blumenthal T . Vitellogenin motifs conserved in nematodes and vertebrates. J Mol Evol. 1991; 32(5):429-38. DOI: 10.1007/BF02101283. View

11.

Boldbaatar D, Battsetseg B, Matsuo T, Hatta T, Umemiya-Shirafuji R, Xuan X . Tick vitellogenin receptor reveals critical role in oocyte development and transovarial transmission of Babesia parasite. Biochem Cell Biol. 2008; 86(4):331-44. DOI: 10.1139/o08-071. View

12.

Gerhart J, Moses A, Raghavan R . A Francisella-like endosymbiont in the Gulf Coast tick evolved from a mammalian pathogen. Sci Rep. 2016; 6:33670. PMC: 5028885. DOI: 10.1038/srep33670. View

13.

Kumar S, Stecher G, Li M, Knyaz C, Tamura K . MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms. Mol Biol Evol. 2018; 35(6):1547-1549. PMC: 5967553. DOI: 10.1093/molbev/msy096. View

14.

Kimura M . A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980; 16(2):111-20. DOI: 10.1007/BF01731581. View

15.

Herren J, Paredes J, Schupfer F, Lemaitre B . Vertical transmission of a Drosophila endosymbiont via cooption of the yolk transport and internalization machinery. mBio. 2013; 4(2). PMC: 3585447. DOI: 10.1128/mBio.00532-12. View

16.

Huo Y, Liu W, Zhang F, Chen X, Li L, Liu Q . Transovarial transmission of a plant virus is mediated by vitellogenin of its insect vector. PLoS Pathog. 2014; 10(3):e1003949. PMC: 3946389. DOI: 10.1371/journal.ppat.1003949. View

17.

Bressac C, Rousset F . The reproductive incompatibility system in Drosophila simulans: DAPI-staining analysis of the Wolbachia symbionts in sperm cysts. J Invertebr Pathol. 1993; 61(3):226-30. DOI: 10.1006/jipa.1993.1044. View

18.

LARKIN M, Blackshields G, Brown N, Chenna R, McGettigan P, McWilliam H . Clustal W and Clustal X version 2.0. Bioinformatics. 2007; 23(21):2947-8. DOI: 10.1093/bioinformatics/btm404. View

19.

Wahli W . Evolution and expression of vitellogenin genes. Trends Genet. 1988; 4(8):227-32. DOI: 10.1016/0168-9525(88)90155-2. View

20.

Gulia-Nuss M, Nuss A, Meyer J, Sonenshine D, Roe R, Waterhouse R . Genomic insights into the Ixodes scapularis tick vector of Lyme disease. Nat Commun. 2016; 7:10507. PMC: 4748124. DOI: 10.1038/ncomms10507. View