Abstract
Defensins are the most diverse groups of antimicrobial peptides in invertebrate animals. In ticks, defensins show great potential as targets for tick control, and display future prospect for therapeutic drug development. In the present study, a novel defensin-like gene (Ds-defensin) contributing to the antimicrobial and antioxidant capacity of the tick Dermacentor silvarum was characterized. The full-length of the Ds-defensin gene was 382 bp, which displayed tissue-specific expression and was highly abundant in the salivary glands and carcasses of the adults. It encodes a 71-amino acid defensin-like protein, and the protein precursor is characterized by a 22-amino acid signal peptide and a 34-amino acid mature peptide. The peptide displayed potent activity against most of the tested gram-positive bacteria, including Staphylococcus aureus, S. carnosus and Nocardia asteroides, and one tested gram-negative bacterium, Psychrobacter faecalis. Scanning electron microscopy revealed that the cell wall and surface of treated bacteria became rough and gradually formed pores after a 30-min exposure to the Ds-defensin peptide. Additionally, the peptide also showed significant antioxidant capacity. The above results implied that the defensin-like peptide may play an important role in tick defense and the interaction with microorganisms.
Similar content being viewed by others
References
Bechinger B, Gorr SU (2017) Antimicrobial peptides: mechanisms of action and resistance. J Dent Res 96:254–260. https://doi.org/10.1177/0022034516679973
Becucci L, Valensin D, Innocenti M, Guidelli R (2014) Dermcidin, an anionic antimicrobial peptide: influence of lipid charge, pH and Zn2+ on its interaction with a biomimetic membrane. Soft Matter 10:616–626. https://doi.org/10.1039/c3sm52400k
Bulet P, Hetru C, Dimarcq JL, Hoffmann D (1999) Antimicrobial peptides in insects: structure and function. Dev Comp Immunol 23:329–344. https://doi.org/10.1016/S0145-305X(99)00015-4
Cabezas-Cruz A, Tonk M, Bouchut A, Pierrot C, Pierce RJ, Kotsyfakis M, Rahnamaeian M, Vilcinskas A, Khalife J, Valdés JJ (2016) Antiplasmodial activity is an ancient and conserved feature of tick defensins. Front Microbiol 7:1682. https://doi.org/10.3389/fmicb.2016.01682
Cabezas-Cruz A, Tonk M, Bleackley MR, Valdés JJ, Barrero RA, Hernández-Jarguín A, Moutailler S, Vilcinskas A, Richard-Forget F, Anderson MA, Rodriguez-Valle M (2019) Antibacterial and antifungal activity of defensins from the Australian paralysis tick, Ixodes holocyclus. Ticks Tick-borne Dis 10:101269. https://doi.org/10.1016/j.ttbdis.2019.101269
Ceraul SM, Sonenshine DE, Ratzlaff RE, Hynes WL (2003) An arthropod defensin expressed by the hemocytes of the American dog tick, Dermacentor variabilis (Acari: Ixodidae). Insect Biochem Mol Biol 33:1099–1103. https://doi.org/10.1016/S0965-1748(03)00122-X
Chen M, Fan MY, Bi DZ, Zhang JZ, Huang YP (1998) Detection of Rickettsia sibirica in ticks and small mammals collected in three different regions of China. Acta Virol 142:61–64. https://doi.org/10.1126/science.283.5400.341
Chrudimská T, Čeřovský V, Slaninová J, Rego ROM, Grubhoffer L (2014) Defensin from the ornate sheep tick Dermacentor marginatus and its effect on Lyme borreliosis spirochetes. Dev Comp Immunol 46(2):165–170. https://doi.org/10.1016/j.dci.2014.04.005
Das M, Bjamba B, Splisteser H (1989) Ixodid tick fauna in Mongolia Monatsh. Veterinaermed 44:471–474
Fjell CD, Hiss JA, Hancock REW, Schneider G (2011) Designing antimicrobial peptides: form follows function. Nat Rev Drug Discov 11:37–51. https://doi.org/10.1038/nrd3591
Fogaca AC, Lorenzini DM, Kaku LM, Esteves E, Bulet P, Daffre S (2004) Cysteine-rich antimicrobial peptides of the cattle tick Boophilus microplus: isolation, structural characterization and tissue expression profile. Dev Comp Immunol 28:191–200. https://doi.org/10.1016/j.dci.2003.08.001
Hancock RE, Diamond G (2000) The role of cationic antimicrobial peptides in innate host defences. Trends Microbiol 8:402–410. https://doi.org/10.1016/S0966-842X(00)01823-0
Hynes WL, Ceraul SM, Todd SM, Seguin KC, Sonenshine DE (2010) A defensin-like gene expressed in the black-legged tick, Ixodes scapularis. Med Vet Entomol 19:339–344. https://doi.org/10.1111/j.1365-2915.2005.00579.x
Johns R, Sonenshine DE, Hynes WL (2001) Identification of a defensin from the hemolymph of the American dog tick, Dermacentor variabilis. Insect Biochem Mol Biol 31:857–865. https://doi.org/10.1016/S0965-1748(01)00031-5
Kim J, Yang YL, Jang YS (2019) Human β-defensin 2 is involved in CCR2-mediated Nod2 signal transduction, leading to activation of the innate immune response in macrophages. Immuno Biol 224:502–510. https://doi.org/10.1016/j.imbio.2019. 05.004
Kulik IL, Vinokurova NS (1983) Range of the tick Dermacentor silvarum in the USSR. Med Parazitol (Mosk) 52:23–28
Lai R, Lomas LO, Jonczy J, Turner PC, Ree HH (2004) Two novel non-cationic defensin-like antimicrobial peptides from haemolymph of the female tick, Amblyomma hebraeum. Biochem J 379:681–685. https://doi.org/10.1042/BJ20031429
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. https://doi.org/10.1007/s10493-005-1271-1
Maeda H, Kurisu K, Miyata T, Kusakisako K, Galay RL, Talactac MR, Mochizuki M, Fujisaki K, Tanaka T (2015) Identification of the Babesia responsive leucine-rich repeat domain-containing protein from the hard tick Haemaphysalis longicornis. Parasitol Res 114:1793–1802. https://doi.org/10.1007/s00436-015-4365-7
Nakajima Y, Naters-Yasui AVDGV, Taylor D, Yamakawa M (2001) Two isoforms of a member of the arthropod defensin family from the soft tick, Ornithodoros moubata (Acari: Argasidae). Insect Biochem Mol Biol 31:747–751. https://doi.org/10.1111/j.1365-2915.2007.00682.x
Nakajima Y, Naters-Yasui AVDGV, Taylor D, Yamakawa M (2002) Antibacterial peptide defensin is involved in midgut immunity of the soft tick, Ornithodoros moubata. Insect Mol Biol 11:611–618. https://doi.org/10.1046/j.1365-2583.2002.00372.x
Nakajima Y, Ishibashi J, Yukuhiro F, Asaoka A, Taylor D, Yamakawa M (2003) Antibacterial activity and mechanism of action of tick defensin against Gram-positive bacteria. Biochim Biophys Acta 1624:125–130. https://doi.org/10.1016/j.bbagen.2003.10.004
Sagaram US, Pandurangi R, Kaur J, Smith TJ, Shah DM (2011) Structure-activity determinants in antifungal plant defensins MsDef1 and MtDef4 with different modes of action against Fusarium graminearum. PLoS ONE 6:e18550. https://doi.org/10.1371/journal.pone.0018550
Saito Y, Konnai S, Yamada S, Imamura S, Nishikado H, Ito T, Onuma M, Ohashi K (2009) Identification and characterization of antimicrobial peptide, defensin, in the taiga tick, Ixodes persulcatus. Insect Mol Biol 18:531–539. https://doi.org/10.1111/j.1365-2583.2009.00897.x
Sun T, Pan W, Song Y, Zhang J, Wang J, Dai J (2017) Functional characterization of two defensins, HlDFS1 and HlDFS2, from the hard tick Haemaphysalis longicornis. Parasit Vector 10:455. https://doi.org/10.1186/s13071-017-2397-9
Talactac MR, Yada Y, Yoshii K, Hernandez EP, Kusakisako K, Maeda H, Galay HL, Fujisaki K, Mochizuki M, Tanaka T (2017) Characterization and antiviral activity of a newly identified defensin-like peptide, HEdefensin, in the hard tick Haemaphysalis longicornis. Dev Comp Immunol 68:98–107. https://doi.org/10.1016/j.dci.2016.11.013
Taylor D (2006) Innate immunity in ticks: a review. J Acarol Soc Jpn 15:109–127. https://doi.org/10.2300/acari.15.109
Teng KF, Jiang ZJ (1991) Economic Insect Fauna of China. Fasc 39 Acari: Ixodidae. Science Press, Beijing, pp 295–317 (in Chinese)
Tian ZC, Liu GY, Shen H, Xie JR, Luo J, Tian MY (2012) First report on the occurrence of Rickettsia slovaca and Rickettsia raoultii in Dermacentor silvarum in China. Parasit Vector 5:19. https://doi.org/10.1186/1756-3305-5-19
Todd SM, Sonenshine DE, Hynes WL (2010) Tissue and life-stage distribution of a defensin gene in the Lone Star tick, Amblyomma americanum. Med Vet Entomol 21:141–147. https://doi.org/10.1111/j.1365-2915.2007.00682.x
Tonk M, Cabezas-Cruz A, Valdes JJ, Rego RO, Rudenko N, Golovchenko M, Bell-Sakyi L, de la Fuente J, Grubhoffer L (2014) Identification and partial characterisation of new members of the Ixodes ricinus defensin family. Gene 2:46–52. https://doi.org/10.1016/j.gene.2014.03.002
Tonk M, Knorr E, Cabezas-Cruz A, Valdés JJ, Kollewe C, Vilcinskas A (2015) Tribolium castaneum defensins are primarily active against gram-positive bacteria. J Invert Pathol 132:208–215. https://doi.org/10.1016/j.jip.2015.10.009
Wang J, Bian G, Pan W, Feng T, Dai J (2015) Molecular characterization of a defensin gene from a hard tick,Dermacentor silvarum. Parasit Vector 8:25. https://doi.org/10.1186/s13071-014-0625-0
Wen J, Jiao D, Wang JH, Yao DH, Liu ZX, Zhao G, Ju WD, Cheng C, Li YJ, Sun Y (2014) Rickettsia raoultii, the predominant Rickettsia found in Dermacentor silvarum ticks in China-Russia border areas. Exp Appl Acarol 63:579–585. https://doi.org/10.1007/s10493-014-9792-0
Wimley WC (2015) Describing the mechanism of antimicrobial peptide action with the interfacial activity model. ACS Chem Biol 5:905–917. https://doi.org/10.1021/cb1001558
Xue XF, Han FF, Gao YH, Liu YF, Xia Y, Wang YZ (2012) In vitro detections of antimicrobial and antioxidant activities of porcine β-defensins. J Agric Biotechnol 11:1291–1299
Yada Y, Talactac MR, Kusakisako K, Hernandez EP, Galay RL, Andoh M, Fujisaki K, Tanaka T (2018) Hemolymph defensin from the hard tick Haemaphysalis longicornis attacks Gram-positive bacteria. J Invertebr Pathol 156:14–18. https://doi.org/10.1016/j.jip.2018.07.005
Yamaguchi Y, Ouchi Y (2012) Antimicrobial peptide defensin: identification of novel isoforms and the characterization of their physiological roles and their significance in the pathogenesis of diseases. Proc Jpn Acad Ser B 88:152–166. https://doi.org/10.2183/pjab.88.152
Yang H, Wang X, Liu X, Wu J, Liu C, Gong W, Zhao Z, Hong J, Lin D, Wang Y, Lai R (2009) Antioxidant peptidomics reveals novel skin antioxidant system. Mol Cell Proteomics 8:571–583. https://doi.org/10.1074/mcp.m800297-mcp200
Yao T, Lu J, Ye L, Wang J (2019) Molecular characterization and immune analysis of a defensin from small abalone, Haliotis diversicolor. Comp Biochem Physiol Part B 235:1–5. https://doi.org/10.1016/j.cbpb.2019.05.004
Yu D, Liang J, Yu H, Wu H, Xu C, Liu J, Lai R (2006) A tick B-cell inhibitory protein from salivary glands of the hard tick, Hyalomma asiaticum asiaticum. Biochem Biophys Res Commun 343:585–590. https://doi.org/10.1016/j.bbrc.2006.02.188
Yu Z, Zheng H, Chen Z, Zheng B, Ma H, Liu J (2010) The life cycle and biological characteristics of Dermacentor silvarum Olenev (Acari: Ixodidae) under field conditions. Vet Parasitol 168:323–328. https://doi.org/10.1016/j.vetpar.2009.11.010
Zhang S, Fu L, Wan M, Song J, Gao L, Fang W (2019) Peripheral antimicrobial peptide gomesin induces membrane protrusion, folding, and laceration. Langmuir 35:13233–13242. https://doi.org/10.1021/acs.langmuir.9b02175
Zheng H, Zhou L, Yang X, Wang D, Liu J (2012) Cloning and characterization of a male-specific defensin-like antimicrobial peptide from the tick Haemaphysalis longicornis. Dev Comp Immunol 37:207–211. https://doi.org/10.1016/j.dci.2011.10.004
Zhou Y, Lei Y, Cao Z, Chen X, Sun Y, Xu Y, Guo W, Wang S, Liu C (2019) A β-defensin gene of Trachinotus ovatus might be involved in the antimicrobial and antiviral immune response. Dev Comp Immunol 92:105–115. https://doi.org/10.1016/j.dci.2018.11.011
Acknowledgements
This work was supported by the National Natural Science Foundation of China (31472050, 31071979), the Natural Science Foundation of Hebei Province of China (C2018205054), Hebei Introduction Foundation for the Returned Overseas Scholars (CL201716) and the Foundation of Hebei Educational Committee (ZD2020168).
Author information
Authors and Affiliations
Corresponding authors
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Fengjiao Li and Zhihua Gao have contributed equally to this work.
Rights and permissions
About this article
Cite this article
Li, F., Gao, Z., Wang, K. et al. A novel defensin-like peptide contributing to antimicrobial and antioxidant capacity of the tick Dermacentor silvarum (Acari: Ixodidae). Exp Appl Acarol 83, 271–283 (2021). https://doi.org/10.1007/s10493-020-00584-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10493-020-00584-1