{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,3,7]],"date-time":"2026-03-07T16:42:12Z","timestamp":1772901732026,"version":"3.50.1"},"update-to":[{"DOI":"10.1371\/journal.pntd.0013139","type":"new_version","label":"New version","source":"publisher","updated":{"date-parts":[[2025,6,17]],"date-time":"2025-06-17T00:00:00Z","timestamp":1750118400000}}],"reference-count":79,"publisher":"Public Library of Science (PLoS)","issue":"6","license":[{"start":{"date-parts":[[2025,6,5]],"date-time":"2025-06-05T00:00:00Z","timestamp":1749081600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Key Technologies Research and Development Program of People's Republic of China","award":["2022YFC2305001"],"award-info":[{"award-number":["2022YFC2305001"]}]},{"name":"National Science and Technology Fundamental Resource Investigation Program of People\u2019s Republic of China","award":["2022FY100900"],"award-info":[{"award-number":["2022FY100900"]}]}],"content-domain":{"domain":["www.plosntds.org"],"crossmark-restriction":false},"short-container-title":["PLoS Negl Trop Dis"],"abstract":"<jats:sec id=\"sec001\">\n<jats:title>Objects<\/jats:title>\n<jats:p>Vector ticks\u2019 perception of characteristic odors emitted by infected hosts is key to understand tick\u2019s foraging behavior for infected host and design odor-based control strategies for tick-borne diseases.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec002\">\n<jats:title>Methods<\/jats:title>\n<jats:p>Laboratory mice knocked out for type I interferon (IFN) receptors (Ifnar<jats:sup>-\/-<\/jats:sup>) were used to develop a simulated host by intraperitoneal infection with <jats:italic>Bandavirus dabieense<\/jats:italic> (SFTSV). Urine and fecal samples were collected 4 days post-infection and analyzed to detect differential volatile metabolites (DVMs) during infection. Next, the two salient odor cues among the SFTSV-induced host DVMs, indole and 3-methylindole, were used to test the olfactory response of <jats:italic>Haemaphysalis. longicornis<\/jats:italic> by electroantennographic detection (EAD) and Y-tube olfactometry, respectively. To gain insight into the potential olfactory mechanism, two olfactory-associated proteins, Niemann-Pick type C2 (NPC2) and Odor Binding Protein-like (OBPL) proteins were annotated from the transcriptomic data derived from <jats:italic>H. longicornis<\/jats:italic> forelegs. Online tools were used to predict the ligand binding properties of the two proteins to the two indole candidates. Simultaneously, quantitative RT-PCR using \u03b2-actin as an internal reference gene was used to monitor the relative transcript levels of NPC2 and OBPL proteins under the stimulation of two indole candidates. The significantly regulated proteins were cloned and expressed with the vector plasmid pET-28b <jats:italic>in vitro<\/jats:italic>. The purified proteins were tested for the binding properties to the two indole candidates.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec003\">\n<jats:title>Results<\/jats:title>\n<jats:p>SFTSV-infected Ifnar<jats:sup>-\/-<\/jats:sup> mice upregulated 11 DVMs in fecal samples, mostly indoles and phenols, along with indole biosynthesis and related metabolic processes. In the urine samples, 29 DVMs were downregulated in the infected host, with eucalyptol and phenylalanine acid being the most altered. We test the olfactory responses of <jats:italic>H. longicornis<\/jats:italic> to indole and 3-methylindole, which influence tick foraging behavior. The olfactometers showed that the tick preferred both indole and 3-methylindole. EAD tests showed that stimulation of the olfactory receptor neuron in Haller\u2019s organ produced significant active potential in response to indoles. Two olfactory proteins, NPC2 and OBPL, were successfully annotated from <jats:italic>H. longicornis<\/jats:italic> foreleg transcriptomic data. NPC2 has a \u03b2-barrel structure that binds signal chemicals, while OBPL is a classical OBP with a hydrophobic binding cavity. When monitoring the transcript levels of NPC2 and OBPL in the tick forelegs, the increased transcript level (1.2-1.4 folds change) of OBPL was observed following indoles stimulation, compared to the downregulated level (0.6-0.8 folds change) of NPC2 under the same circumstances. The <jats:italic>OBPL<\/jats:italic> and <jats:italic>NPC2<\/jats:italic> gene from <jats:italic>H. longicornis<\/jats:italic> were successfully cloned and expressed as inclusion proteins respectively. The purified OBPL (20.28 kDa) showed higher affinity for both indole (Ki 2.256\u03bcM) and 3-methylindole (Ki 4.191\u03bcM) than NPC2 in the competitive fluorescence binding assays with 1-NPN as a competitor.<\/jats:p>\n<\/jats:sec>\n<jats:sec id=\"sec004\">\n<jats:title>Conclusions<\/jats:title>\n<jats:p>Facilitated by the olfactory OBPL protein in Haller\u2019s organ, <jats:italic>H. longicornis<\/jats:italic> smells and is attracted to the characteristic indolic scents of hosts induced by SFTSV infection. Olfactory associations between infected hosts and vector arthropods could provide a new perspective to understand host foraging behavior and design novel control strategies for tick-borne diseases based on pathogen-induced scent according to chemical ecology theory.<\/jats:p>\n<\/jats:sec>","DOI":"10.1371\/journal.pntd.0013139","type":"journal-article","created":{"date-parts":[[2025,6,5]],"date-time":"2025-06-05T17:55:14Z","timestamp":1749146114000},"page":"e0013139","update-policy":"https:\/\/doi.org\/10.1371\/journal.pntd.corrections_policy","source":"Crossref","is-referenced-by-count":1,"title":["Smelly communication between haemaphysalis longicornis and infected hosts with indolic odorants: A case from severe fever with thrombocytopenia syndrome virus"],"prefix":"10.1371","volume":"19","author":[{"given":"Zhitong","family":"Liu","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hao","family":"Feng","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Xiaohe","family":"Liu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Bin","family":"Wu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Hong","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6871-6975","authenticated-orcid":true,"given":"Yi","family":"Sun","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jiahong","family":"Wu","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Chunxiao","family":"Li","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jiafu","family":"Jiang","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"340","published-online":{"date-parts":[[2025,6,5]]},"reference":[{"issue":"5","key":"pntd.0013139.ref001","doi-asserted-by":"crossref","first-page":"230084","DOI":"10.1098\/rsos.230084","article-title":"Synergistic attraction of Western black-legged ticks, Ixodes pacificus, to CO2 and odorant emissions from deer-associated microbes","volume":"10","author":"J Long","year":"2023","journal-title":"R Soc Open Sci"},{"issue":"5","key":"pntd.0013139.ref002","doi-asserted-by":"crossref","first-page":"605","DOI":"10.1093\/aesa\/55.5.605","article-title":"Carbon Dioxide as an Attractant for Certain Ticks (Acarina: Argasidae and Ixodidae)","volume":"55","author":"R Garcia","year":"1962","journal-title":"Annals of the Entomological Society of America"},{"key":"pntd.0013139.ref003","article-title":"Pheromones and other semiochemicals of ticks and their use in tick control","author":"DE Sonenshine","year":"2004","journal-title":"Parasitology"},{"issue":"1","key":"pntd.0013139.ref004","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1603\/0022-2585-38.1.114","article-title":"Interdigital gland substances of white-tailed deer and the response of host-seeking ticks (Acari: Ixodidae)","volume":"38","author":"JF Carroll","year":"2001","journal-title":"J Med Entomol"},{"issue":"8","key":"pntd.0013139.ref005","article-title":"Ticks home in on body heat: A new understanding of Haller\u2019s organ and repellent action","volume":"14","author":"AL Carr","year":"2019","journal-title":"PLoS One"},{"issue":"5","key":"pntd.0013139.ref006","doi-asserted-by":"crossref","first-page":"764","DOI":"10.1016\/j.ttbdis.2017.06.001","article-title":"Infrared light detection by the haller\u2019s organ of adult american dog ticks, Dermacentor variabilis (Ixodida: Ixodidae)","volume":"8","author":"RD Mitchell","year":"2017","journal-title":"Ticks Tick Borne Dis"},{"issue":"1","key":"pntd.0013139.ref007","doi-asserted-by":"crossref","first-page":"39","DOI":"10.1111\/j.1708-8305.2007.00176.x","article-title":"What makes ticks tick? 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