Dual oxidase enables insect gut symbiosis by mediating respiratory network formation
Dual oxidase enables insect gut symbiosis by mediating respiratory network formation
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DOI：
10.1073/pnas.2020922118
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发表时间：
2021-03-09
影响因子：
11.1
通讯作者：
Kikuchi, Yoshitomo
中科院分区：
文献类型：
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作者：
Jang, Seonghan;Mergaert, Peter;Kikuchi, Yoshitomo
大多数动物的肠道微生物区系由潜在的致病微生物、共生微生物和互惠共生微生物组成。双氧化酶(DUOX)是一种已知的参与肠道粘膜免疫的酶，它通过产生活性氧(ROS)来对抗昆虫的病原菌并维持肠道的动态平衡。然而，尽管DUOX对微生物具有非特异性的有害活动，但人们对DUOX在维持肠道互惠共生体中的作用知之甚少。在这里，我们表明，在菜豆害虫Riptortus Hadstris中，依赖于DUOX的ROS并不直接促进中肠上皮细胞的免疫，以响应其互惠共生的肠道共生菌Burkholderia Installticola。相反，我们发现DUOX的表达是气管特异的，RNAi下调DUOX的表达会导致气管蛋白基质中双酪氨酸交联链的丢失和呼吸系统的崩溃。我们进一步证明，共生的建立是一个强大的氧汇，触发了覆盖中肠共生器官和其他器官的广泛气管网络的形成，而DUOX RNAi对气管的破坏会破坏肠道共生。低氧反应转录因子SIMA的下调或气管形成的调节因子无分支和无分支会产生类似的表型。因此，除了在免疫和在不同的细胞外基质中形成Dityroine网络方面的已知作用外，DUOX也是气管完整性的关键酶，而气管完整性对于维持互惠共生和肠道内环境稳定至关重要。我们预计这是昆虫的一种保守功能。
Most animals harbor a gut microbiota that consists of potentially pathogenic, commensal, and mutualistic microorganisms. Dual oxidase (Duox) is a well described enzyme involved in gut mucosal immunity by the production of reactive oxygen species (ROS) that antagonizes pathogenic bacteria and maintains gut homeostasis in insects. However, despite its nonspecific harmful activity on microorganisms, little is known about the role of Duox in the maintenance of mutualistic gut symbionts. Here we show that, in the bean bug Riptortus pedestris, Duox-dependent ROS did not directly contribute to epithelial immunity in the midgut in response to its mutualistic gut symbiont, Burkholderia insecticola. Instead, we found that the expression of Duox is tracheaespecific and its down-regulation by RNAi results in the loss of dityrosine cross-links in the tracheal protein matrix and a collapse of the respiratory system. We further demonstrated that the establishment of symbiosis is a strong oxygen sink triggering the formation of an extensive network of tracheae enveloping the midgut symbiotic organ as well as other organs, and that tracheal breakdown by Duox RNAi provokes a disruption of the gut symbiosis. Down-regulation of the hypoxia-responsive transcription factor Sima or the regulators of tracheae formation Trachealess and Branchless produces similar phenotypes. Thus, in addition to known roles in immunity and in the formation of dityrosine networks in diverse extracellular matrices, Duox is also a crucial enzyme for tracheal integrity, which is crucial to sustain mutualistic symbionts and gut homeostasis. We expect that this is a conserved function in insects.