期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2015
卷号：112
期号：37
页码：E5179-E5188
DOI：10.1073/pnas.1511454112
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：SignificanceIn general, animals have a mouth for feeding, an anus for defecation, and a gut connecting them for digestion and absorption. However, we discovered that the stinkbug's gut is functionally disconnected in the middle by a previously unrecognized organ for symbiont sorting, which blocks food fluid and nonsymbiotic bacteria but selectively allows passing of a specific bacterial symbiont. Though very tiny and inconspicuous, the organ governs the configuration and specificity of stinkbug gut symbiosis, wherein the posterior gut region is devoid of food flow, populated by a specific bacterial symbiont, and transformed into an isolated organ for symbiosis. Mutant analyses showed that the symbiont's flagellar motility is needed for passing the host organ, highlighting intricate host-symbiont interactions underpinning the symbiont sorting process. Symbiosis has significantly contributed to organismal adaptation and diversification. For establishment and maintenance of such host-symbiont associations, host organisms must have evolved mechanisms for selective incorporation, accommodation, and maintenance of their specific microbial partners. Here we report the discovery of a previously unrecognized type of animal organ for symbiont sorting. In the bean bug Riptortus pedestris, the posterior midgut is morphologically differentiated for harboring specific symbiotic bacteria of a beneficial nature. The sorting organ lies in the middle of the intestine as a constricted region, which partitions the midgut into an anterior nonsymbiotic region and a posterior symbiotic region. Oral administration of GFP-labeled Burkholderia symbionts to nymphal stinkbugs showed that the symbionts pass through the constricted region and colonize the posterior midgut. However, administration of food colorings revealed that food fluid enters neither the constricted region nor the posterior midgut, indicating selective symbiont passage at the constricted region and functional isolation of the posterior midgut for symbiosis. Coadministration of the GFP-labeled symbiont and red fluorescent protein-labeled Escherichia coli unveiled selective passage of the symbiont and blockage of E. coli at the constricted region, demonstrating the organ's ability to discriminate the specific bacterial symbiont from nonsymbiotic bacteria. Transposon mutagenesis and screening revealed that symbiont mutants in flagella-related genes fail to pass through the constricted region, highlighting that both host's control and symbiont's motility are involved in the sorting process. The blocking of food flow at the constricted region is conserved among diverse stinkbug groups, suggesting the evolutionary origin of the intestinal organ in their common ancestor.
