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帝王蝶的微生物组分析揭示了发育和饮食的影响。

Microbiome analysis of monarch butterflies reveals effects of development and diet.

作者信息

Sanaei Ehsan, Chavez Joselyne, Harris Erica V, Alcaide Tiffanie Y, Baffour-Addo Keisha, Bugay Mahal J, Adams Kandis L, Zelaya Anna, de Roode Jacobus C, Gerardo Nicole M

机构信息

Department of Biology, Emory University, Atlanta, GA 30322, United States.

Department of Ecology, Evolution, and Organismal Biology, Brown University, Providence, RI 02912, United States.

出版信息

FEMS Microbiol Ecol. 2024 Nov 23;100(12). doi: 10.1093/femsec/fiae143.

DOI:10.1093/femsec/fiae143
PMID:39557647
原文链接:https://pmc.ncbi.nlm.nih.gov/articles/PMC11650861/
Abstract

Diet profoundly influences the composition of an animal's microbiome, especially in holometabolous insects, offering a valuable model to explore the impact of diet on gut microbiome dynamics throughout metamorphosis. Here, we use monarch butterflies (Danaus plexippus), specialist herbivores that feed as larvae on many species of chemically well-defined milkweed plants (Asclepias sp.), to investigate the impacts of development and diet on the composition of the gut microbial community. While a few microbial taxa are conserved across life stages of monarchs, the microbiome appears to be highly dynamic throughout the life cycle. Microbial diversity gradually diminishes throughout the larval instars, ultimately reaching its lowest point during the pupal stage and then recovering again in the adult stage. The microbial composition then undergoes a substantial shift upon the transition from pupa to adult, with female adults having significantly different microbial communities than the eggs that they lay, indicating limited evidence for vertical transmission of gut microbiota. While diet did not significantly impact overall microbial composition, our results suggest that fourth instar larvae exhibit higher microbial diversity when consuming milkweed with high concentrations of toxic cardenolide phytochemicals. This study underscores how diet and developmental stage collectively shape the monarch's gut microbiota.

摘要

饮食对动物微生物组的组成有深远影响,尤其是在全变态昆虫中,这为探索饮食在整个变态过程中对肠道微生物组动态变化的影响提供了一个有价值的模型。在这里,我们以帝王蝶(黑脉金斑蝶)为研究对象,它们是专食性食草动物,幼虫以多种化学成分明确的马利筋属植物(马利筋)为食,以此来研究发育和饮食对肠道微生物群落组成的影响。虽然有一些微生物类群在帝王蝶的各个生命阶段都保持不变,但微生物组在其整个生命周期中似乎具有高度动态性。在幼虫的各个龄期,微生物多样性逐渐降低,最终在蛹期达到最低点,然后在成虫期再次恢复。从蛹到成虫的转变过程中,微生物组成会发生显著变化,雌性成虫的微生物群落与它们所产的卵有明显差异,这表明肠道微生物群垂直传播的证据有限。虽然饮食对整体微生物组成没有显著影响,但我们的结果表明,四龄幼虫在食用含有高浓度有毒强心甾类植物化学物质的马利筋时,表现出更高的微生物多样性。这项研究强调了饮食和发育阶段如何共同塑造帝王蝶的肠道微生物群。

https://cdn.ncbi.nlm.nih.gov/pmc/blobs/871d/11650861/ff496734652e/fiae143fig5.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/871d/11650861/7755a52c0271/fiae143fig1.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/871d/11650861/d2a2168767b6/fiae143fig2.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/871d/11650861/ec933011f2df/fiae143fig3.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/871d/11650861/1402b8872b64/fiae143fig4.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/871d/11650861/ff496734652e/fiae143fig5.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/871d/11650861/7755a52c0271/fiae143fig1.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/871d/11650861/d2a2168767b6/fiae143fig2.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/871d/11650861/ec933011f2df/fiae143fig3.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/871d/11650861/1402b8872b64/fiae143fig4.jpg
https://cdn.ncbi.nlm.nih.gov/pmc/blobs/871d/11650861/ff496734652e/fiae143fig5.jpg

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本文引用的文献

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J Chem Ecol. 2024 Feb;50(1-2):52-62. doi: 10.1007/s10886-023-01461-y. Epub 2023 Nov 6.
2
Composition and diversity of gut microbiota across developmental stages of and its effect on the reproduction.[具体生物]发育阶段肠道微生物群的组成与多样性及其对繁殖的影响。 (注:原文中“of and”中间缺少具体内容)
Front Microbiol. 2023 Sep 18;14:1237684. doi: 10.3389/fmicb.2023.1237684. eCollection 2023.
3
Toward an Integrated Understanding of the Lepidoptera Microbiome.
迈向鳞翅目微生物组的综合理解。
Annu Rev Entomol. 2024 Jan 25;69:117-137. doi: 10.1146/annurev-ento-020723-102548. Epub 2023 Aug 16.
4
Impact of transgenerational host switch on gut bacterial assemblage in generalist pest, (Lepidoptera: Noctuidae).跨代寄主转换对多食性害虫(鳞翅目:夜蛾科)肠道细菌群落的影响
Front Microbiol. 2023 Jul 13;14:1172601. doi: 10.3389/fmicb.2023.1172601. eCollection 2023.
5
Basic Structures of Gut Bacterial Communities in Eusocial Insects.群居昆虫肠道细菌群落的基本结构
Insects. 2023 May 8;14(5):444. doi: 10.3390/insects14050444.
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