Compartmentalized PGRP expression along the dipteran Bactrocera dorsalis gut forms a zone of protection for symbiotic bacteria

• Published in: Cell reports (Cambridge) Vol. 41; no. 3; p. 111523
• Main Authors: Yao, Zhichao, Cai, Zhaohui, Ma, Qiongke, Bai, Shuai, Wang, Yichen, Zhang, Ping, Guo, Qiongyu, Gu, Jian, Lemaitre, Bruno, Zhang, Hongyu
• Format: Journal Article
• Language: English
• Published: Elsevier Inc 18.10.2022
• Subjects: Bactrocera dorsalis; gut microbiota; Imd pathway; immune genes; PGRPs; CP: Immunology; immune genes; PGRPs; CP: Microbiology; Imd pathway; gut microbiota; Bactrocera dorsalis
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2022.111523

All metazoan guts are subject to opposing pressures wherein the immune system must eliminate pathogens while tolerating the presence of symbiotic microbiota. The Imd pathway is an essential defense against invading pathogens in insect guts, but tolerance mechanisms are less understood. Here, we find PGRP-LB and PGRP-SB express mainly in the anterior and middle midgut in a similar pattern to symbiotic Enterobacteriaceae bacteria along the Bactrocera dorsalis gut. Knockdown of PGRP-LB and PGRP-SB enhances the expression of antimicrobial peptide genes and reduces Enterobacteriaceae numbers while increasing abundance of opportunistic pathogens. Microbiota numbers recover to normal levels after the RNAi effect subsided. In contrast, high expression of PGRP-LC in the foregut allows increased antibacterial peptide production to efficiently filter the entry of pathogens, protecting the symbiotic bacteria. Our study describes a mechanism by which regional expression of PGRPs construct a protective zone for symbiotic microbiota while maintaining the ability to fight pathogens. [Display omitted] •Symbiotic bacteria are mainly located in the anterior midgut of B. dorsalis•Regional expression of PGRP matches the distribution pattern of symbiotic bacteria•PGRP-LB and PGRP-SB establish a protective zone for symbiotic bacteria colonization•PGRP-LC and AMPs in the foregut filter the pathogens to protect symbiotic bacteria Yao et al. find there is a regional expression of PGPR and spatial distribution of symbiotic bacteria along the Bactrocera dorsalis gut. This regional expression of PGPR tightly regulates the Imd pathway to construct a protective zone for symbiotic microbiota while maintaining the ability to fight pathogens.