Ingested soil bacteria breach gut epithelia and prime systemic in an insect

• 成果类型: Article
• 署名作者: Jang, Seonghan; Ishigami, Kota; Mergaert, Peter; Kikuchi, Yoshitomo
• 署名单位: National Institute of Advanced Industrial Science & Technology (AIST); Universite Paris Saclay; CEA; Centre National de la Recherche Scientifique (CNRS); Hokkaido University; Korea Research Institute of Bioscience & Biotechnology (KRIBB)
• 刊物名称: PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
• ISSN/ISSBN: 0027-15188
• DOI: 10.1073/pnas.2315540121
• 发表日期: 2024-03-12
• 关键词: drosophila host-defense; antimicrobial peptide; riptortus-pedestris; burkholderia symbiont; infection dynamics; peritrophic matrix; innate immunity; trade-offs; mechanisms; resistance

摘要

Insects lack acquired immunity and were thought to have no immune memory, but recent studies reported a phenomenon called immune priming, wherein sublethal dose of pathogens or nonpathogenic microbes stimulates immunity and prevents subsequential pathogen infection. Although the evidence for insect immune priming is accumulating, the underlying mechanisms are still unclear. The bean bug Riptortus pedestris acquires its gut microbiota from ambient soil and spatially structures them into a multispecies and variable community in the anterior midgut and a specific, monospecies Caballeronia symbiont population in the posterior region. We demonstrate that a particular Burkholderia strain colonizing the anterior midgut stimulates systemic immunity by penetrating gut epithelia and migrating into the hemolymph. The activated immunity, consisting of a humoral and a cellular response, had no negative effect on the host fitness, but on the contrary protected the insect from subsequent infection by pathogenic bacteria. Interruption of contact between the Burkholderia strain and epithelia of the gut weakened the host immunity back to preinfection levels and made the insects more vulnerable to microbial infection, demonstrating that persistent acquisition of environmental bacteria is important to maintain an efficient immunity.