C-type lectin-mediated microbial homeostasis is critical for Helicoverpa armigera larval growth and development.-猫眼课题宝

C型凝集素介导的微生物稳态对于棉铃虫幼虫的生长和发育至关重要

DOI：

10.1371/journal.ppat.1008901

发表时间：

2020-09

期刊：

PLoS pathogens

影响因子：

6.7

通讯作者：

中科院分区：

医学1区

文献类型：

作者：

Wang W;Wang G;Zhuo X;Liu Y;Tang L;Liu X;Wang J

来源链接：

https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7549827/

宿主的免疫系统在塑造微生物群的组成方面发挥着至关重要的作用，并且一些微生物参与调节宿主内分泌系统和发育。然而，免疫系统是否通过塑造微生物群的组成来影响内分泌和发育仍不清楚，并且很少有参与这一过程的分子参与者或微生物被识别。在目前的研究中，我们发现棉铃虫Helicoverpa armigera中C型凝集素（HaCTL3）的RNA干扰抑制了蜕皮激素和保幼激素信号传导，从而减小了幼虫体型并延迟了化蛹。 HaCTL3 的消耗还会导致血淋巴中的肠球菌丰度增加，这些细菌可能会从肠道逃逸。此外，HaCTL3 及其控制的抗菌肽（attacin、lebocin 和 gloverin）参与通过吞噬作用或直接杀菌活性从血淋巴中清除 E. mundtii。将 E. mundtii 注射到幼虫血腔中模拟 HaCTL3 耗尽的表型并抑制蜕皮激素和保幼激素信号传导。综上所述，我们得出结论，HaCTL3 通过抑制血淋巴中 E. mundtii 的丰度来维持棉铃虫幼虫的正常生长和发育。我们的研究结果提供了第一个证据，证明免疫系统作用于内分泌系统，通过塑造昆虫血淋巴中的微生物群组成来调节发育。因此，这项研究将加深我们对免疫与发育之间相互作用的理解。考虑到昆虫血淋巴中存在大量的血细胞和多种可溶性效应子，传统上认为健康的昆虫血淋巴对细菌来说是一个不利的环境，因此是无菌的。然而，越来越多的证据反驳了这一观点，尽管血淋巴微生物群与昆虫宿主之间的相互作用机制以及血淋巴微生物群的功能仍不清楚。 C型凝集素（CTL）作为模式识别受体（PRR），在防御多种病原体方面发挥着重要作用。在这里，我们发现多种细菌定植于棉铃虫Helicoverpa armigera 的血淋巴中。我们首先报道了棉铃虫 CTL (HaCTL3) 参与调节幼虫的生长和发育。进一步的研究表明，HaCTL3介导的肠球菌在血淋巴中的稳态对于幼虫的正常生长和发育至关重要。我们的研究表明，这种 PRR 通过塑造血淋巴微生物群来调节昆虫发育，这可能代表了昆虫发育过程中免疫系统调节的一种新机制。

The immune system of a host functions critically in shaping the composition of the microbiota, and some microbes are involved in regulating host endocrine system and development. However, whether the immune system acts on endocrine and development by shaping the composition of the microbiota remains unclear, and few molecular players or microbes involved in this process have been identified. In the current study, we found that RNA interference of a C-type lectin (HaCTL3) in the cotton bollworm Helicoverpa armigera suppresses ecdysone and juvenile hormone signaling, thus reducing larval body size and delaying pupation. Depletion of HaCTL3 also results in an increased abundance of Enterocuccus mundtii in the hemolymph, which may escape from the gut. Furthermore, HaCTL3 and its controlled antimicrobial peptides (attacin, lebocin, and gloverin) are involved in the clearance of E. mundtii from the hemolymph via phagocytosis or direct bactericidal activity. Injection of E. mundtii into larval hemocoel mimics HaCTL3-depleted phenotypes and suppresses ecdysone and juvenile hormone signaling. Taken together, we conclude that HaCTL3 maintains normal larval growth and development of H. armigera via suppressing the abundance of E. mundtii in the hemolymph. Our results provide the first evidence of an immune system acting on an endocrine system to modulate development via shaping the composition of microbiota in insect hemolymph. Thus, this study will deepen our understanding of the interaction between immunity and development. Considering that a large number of hemocytes and multiple soluble effectors are present in insect hemolymph, it is conventionally believed that healthy insect hemolymph is a hostile environment for bacteria and is, therefore, sterile. However, increasing evidences disprove this opinion, although the interactive mechanism between hemolymph microbiota and insect host, as well as the function of hemolymph microbiota, remain unclear. C-type lectin (CTL), as pattern recognition receptor (PRR), plays important roles in defending against various pathogens. Here we found that various bacteria colonized the hemolymph of the cotton bollworm Helicoverpa armigera. We first reported that an H. armigera CTL (HaCTL3) was involved in modulating larval growth and development. Further study indicated that HaCTL3-mediated homeostasis of Enterocuccus mundtii in the hemolymph is critical for normal larval growth and development. Our study demonstrated that this PRR modulated insect development through shaping hemolymph microbiota, which may represent a novel mechanism of immune system regulation during insect development.