☆ 4.8 Article

A volatile from the skin microbiota of flavivirus-infected hosts promotes mosquito attractiveness

CELL (2022)

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CELL
卷 185, 期 14, 页码 2510-+

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CELL PRESS
DOI: 10.1016/j.cell.2022.05.016

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Biochemistry & Molecular Biology Cell Biology

资金

  1. National Key Research and Development Plan of China [2021YFC2300200,2020YFC1200100, 2018YFA0507202]
  2. National Natural Science Foundation of China [31825001, 81730063, 32188101, 82102389, 8191101056]
  3. Tsinghua University Spring Breeze Fund [2020Z99CFG017]
  4. Shenzhen Science and Technology Project [JSGG20191129144225464]
  5. Shenzhen San-Ming Project for Prevention and Research on Vector-borne Diseases [SZSM201611064]
  6. Young Elite Scientists Sponsorship Program [2021QNRC001]
  7. Yunnan Cheng Gong expert work-station [202005AF150034]
  8. Provincial innovation team for the prevention and control of highly pathogenic pathogens, Institute of Medical Biology, Chinese Academy of Medical Sciences [202105AE160020]

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Mosquitoes can be attracted to the scent produced by the skin microbiota of hosts infected with flaviviruses. This study found that mosquitoes preferentially seek and feed on mice infected with dengue and Zika viruses. The scent is primarily composed of a volatile compound called acetophenone, which is produced by commensal bacteria on the skin. The expression of an antimicrobial protein called RELMa is suppressed by the flavivirus infection, leading to an expansion of acetophenone-producing bacteria and an increase in acetophenone levels. By administering a vitamin A derivative called isotretinoin, which specifically induces RELMa, the mosquito host-seeking activity is reduced and the flavivirus life cycle is interrupted, offering a strategy for arboviral control.
The host-seeking activity of hematophagous arthropods is essential for arboviral transmission. Here, we demonstrate that mosquito-transmitted flaviviruses can manipulate host skin microbiota to produce a scent that attracts mosquitoes. We observed that Aedes mosquitoes preferred to seek and feed on mice infected by dengue and Zika viruses. Acetophenone, a volatile compound that is predominantly produced by the skin microbiota, was enriched in the volatiles from the infected hosts to potently stimulate mosquito olfaction for attractiveness. Of note, acetophenone emission was higher in dengue patients than in healthy people. Mech-anistically, flaviviruses infection suppressed the expression of RELMa, an essential antimicrobial protein on host skin, thereby leading to the expansion of acetophenone-producing commensal bacteria and, conse-quently, a high acetophenone level. Given that RELMa can be specifically induced by a vitamin A derivative, the dietary administration of isotretinoin to flavivirus-infected animals interrupted flavivirus life cycle by reducing mosquito host-seeking activity, thus providing a strategy of arboviral control.

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