Gut microbiota of the pine weevil degrades conifer diterpenes and increases insect fitness

Gut microbiota of the pine weevil degrades conifer diterpenes and increases insect fitness
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DOI:
10.1111/mec.14186
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发表时间:
2017-08-01
期刊:
影响因子:
4.9
通讯作者:
Schmidt, Axel
Schmidt, Axel
中科院分区:
生物学1区
文献类型:
--
作者:
Berasategui, Aileen;Salem, Hassan;Schmidt, Axel

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松象甲 (Hylobius abietis) 是整个欧洲针叶林的主要害虫,以树皮和形成层为食,这些组织富含萜类树脂,对许多昆虫食草动物有毒。在这里,我们报告了松象甲肠道微生物群降解挪威云杉二萜酸的能力。在通过松象甲肠道时,摄入的树皮中存在的二萜酸水平显着降低。在抗生素治疗后,这种减少明显减少,并且用未经处理的昆虫的肠道悬浮液补充饮食可以恢复降解二萜的能力。此外,从松象甲肠道中分离出的培养细菌被证明可以降解挪威云杉二萜酸。在对昆虫细菌群落的宏基因组调查中,我们能够注释先前描述的二萜降解(dit)基因簇的几个基因。抗生素治疗破坏了松杉肠道的核心细菌群落,并消除了几乎所有与其二萜降解减少一致的dit基因。研究发现,用添加二萜但不含抗生素的人工饲料饲养的松象甲,比用添加抗生素或不含二萜的饲料饲养的松象甲虫产下更多的卵,且孵化率更高。这些结果表明,肠道共生体有助于宿主健康,但不是通过二萜的解毒,因为这些化合物在有或没有抗生素的情况下都不会表现出毒性作用。相反,在富含萜烯的环境中茁壮成长的能力似乎使肠道微生物能够以其他方式使象鼻虫受益,例如增加其饮食的营养特性。
The pine weevil (Hylobius abietis), a major pest of conifer forests throughout Europe, feeds on the bark and cambium, tissues rich in terpenoid resins that are toxic to many insect herbivores. Here, we report the ability of the pine weevil gut microbiota to degrade the diterpene acids of Norway spruce. The diterpene acid levels present in ingested bark were substantially reduced on passage through the pine weevil gut. This reduction was significantly less upon antibiotic treatment, and supplementing the diet with gut suspensions from untreated insects restored the ability to degrade diterpenes. In addition, cultured bacteria isolated from pine weevil guts were shown to degrade a Norway spruce diterpene acid. In a metagenomic survey of the insect's bacterial community, we were able to annotate several genes of a previously described diterpene degradation (dit) gene cluster. Antibiotic treatment disrupted the core bacterial community of H. abietis guts and eliminated nearly all dit genes concordant with its reduction in diterpene degradation. Pine weevils reared on an artificial diet spiked with diterpenes, but without antibiotics, were found to lay more eggs with a higher hatching rate than weevils raised on diets with antibiotics or without diterpenes. These results suggest that gut symbionts contribute towards host fitness, but not by detoxification of diterpenes, as these compounds do not show toxic effects with or without antibiotics. Rather the ability to thrive in a terpene-rich environment appears to allow gut microbes to benefit the weevil in other ways, such as increasing the nutritional properties of their diet.