The Evolution of Bacterial Mutualism with Eukaryotic Hosts

细菌与真核宿主互惠共生的进化

• 批准号: NE/M018016/1
• 负责人: Lee Henry
• 金额: $ 68.15万
• 依托单位: Queen Mary University of London
• 依托单位国家: 英国
• 项目类别: Fellowship
• 财政年份: 2016
• 资助国家: 英国
• 起止时间: 2016 至 无数据
• 项目状态: 已结题
• 来源: https://gtr.ukri.org/projects?ref=NE%2FM018016%2F1
• 关键词: Evolution; Bacterial; Mutualism; Eukaryotic; Hosts

Bacteria: friend or foe?All plants and animals share some form of intimate relationship with bacteria. Although we often focus on harmful bacteria that cause diseases, recent research has shown that many bacteria that live within animals are actually beneficial. Whether this is the light-producing bacteria that live within fireflies that help them attract mates to the 100 trillion bacterial cells that live within our guts that aid in digestion, beneficial microbes are both ever-present and important to all organisms on the planet. My research explores how animals form beneficial relationships with symbiotic microbes by asking: What are the factors that produce stable mutually beneficial unions between animals and microbes, and what cause these relationships to break down? To answer these questions I focus on a single group of organisms that have evolved fascinating relationships with microbes, insects. Insects are host to a diverse community of symbiotic microbes that have profound effects on their biology. These effects include, protecting insects from natural enemies, such as parasitic wasp and pathogenic fungus, providing insects with protection against heat stress and assist insects in gaining nutrients. A peculiar feature of these helpful microbes is that only certain populations of insects have them, whereas others do not. In addition, only certain bacterial strains provide benefits to their insect hosts whereas others do not. This natural variation presents a perfect opportunity to ask questions such as: why do certain populations of insect hosts contain beneficial microbes whereas others do not? And, why do only some of the symbiotic microbes provide benefits to insects, and how does the loss of beneficial function impact their relationship with their host? To answer these questions I use modern DNA technology that allow me to identity factors that influence beneficial microbial functions at a molecular level, as well as explore the evolution of host-microbe relationships over millions of years. The application of these modern techniques to the intriguing variation in the bacterial symbionts of insects provides a general understanding of the factors that maintain and degrade beneficial relationships with bacteria in all plants and animals. Host-microbe relationships are everywhere in nature, and understanding the factors that maintain and degrade these relationships has important implications in both agriculture and health. My research will not only provide novel insight into the gain and loss of beneficial traits in bacteria, but also has great potential in understanding the gain and loss of harmful traits in bacterial pathogens. Of more immediate application, my research can lead to practical solutions for managing insect pests in agriculture and those that vector major human diseases. Pesticides were common solutions to deal with pests, however there is strong pressure to reduce pesticide use to moderate our reliance on environmental harmful chemicals. Many insect pests have evolved mutualistic relationships with symbiotic bacteria such as, Triatoma bugs that vector Chagas disease, tsetse fly that vector sleeping sickness, cereal weevils that devastates crops around the world, and all sap sucking insects. Research to exploit the relationship between bacteria and insect hosts for the biological control of pests, termed Symbiont-Based Control Strategies, is a preferred strategy to chemical control due to the reduced environmental impact. My research is a critical first step in advancing our understanding of insect-bacteria relationships in many pest species, by revealing both the molecular mechanisms by which bacteria and hosts interact, as well as the conditions that promote stable relationships between bacteria and host. The knowledge from this research can be used to help develop practical solutions for managing pests in agriculture, forestry and those that vector major human diseases.

细菌：朋友或敌人？所有动植物与细菌具有某种形式的亲密关系。尽管我们经常专注于引起疾病的有害细菌，但最近的研究表明，许多生活在动物中的细菌实际上都是有益的。这是否是生活在萤火虫中的产生的细菌，可以帮助它们吸引伴侣与有助于消化的肠道中的100万亿个细菌细胞，对地球上所​​有生物的有益的微生物都始终存在，既有有益的微生物。我的研究探讨了动物如何通过询问与共生微生物建立有益的关系：在动物和微生物之间产生稳定的互惠互利的工会的因素是什么，什么导致这些关系分解？为了回答这些问题，我专注于一组与微生物，昆虫相关关系的生物。昆虫是一个多元化的共生微生物社区，对其生物学产生了深远的影响。这些影响包括保护昆虫免受天然敌人的侵害，例如寄生虫和致病真菌，从而为昆虫提供了防止热应激的保护，并帮助昆虫获得营养。这些有用的微生物的特征是，只有某些昆虫种群才有它们，而其他昆虫则没有。此外，只有某些细菌菌株为其昆虫宿主带来好处，而其他细菌却没有。这种自然变化为提出问题提供了一个绝佳的机会，例如：为什么某些昆虫宿主包含有益的微生物，而其他人则不含有益的微生物？而且，为什么只有一些共生微生物为昆虫提供好处，而丧失有益功能的丧失如何影响其与宿主的关系？为了回答这些问题，我使用了现代DNA技术，使我能够身份影响分子水平上有益微生物功能的身份因素，并探索数百万年来宿主微生物关系的演变。这些现代技术在昆虫的细菌共生体中的有趣变化中的应用提供了对维持和降低所有动植物细菌关系的因素的一般理解。宿主 - 微生物关系在自然界中无处不在，了解维持和降低这些关系的因素在农业和健康中都具有重要意义。我的研究不仅可以为细菌中有益性状的增益和丧失提供新的见解，而且还具有了解细菌病原体中有害特征的增益和丧失的巨大潜力。更直接地应用，我的研究可能会导致解决农业中的害虫和培养主要人类疾病的虫害的实用解决方案。农药是处理害虫的常见解决方案，但是减少农药使用以减少我们对环境有害化学物质的依赖的压力很大。许多害虫与共生细菌相互关系，例如，chagas病的triatoma虫子，tsetse蝇，载体睡眠病，谷物象鼻虫破坏了世界各地的作物，以及所有汁液吮吸昆虫。由于环境影响降低而导致细菌与昆虫宿主之间的关系（称为基于共生体的控制策略）是一种化学控制的首选策略。我的研究是通过揭示细菌和宿主相互作用的分子机制以及促进细菌与宿主之间稳定关系的条件来促进许多害虫物种中昆虫细菌关系的了解的关键第一步。这项研究的知识可用于帮助开发用于管理农业，林业和培养主要人类疾病的害虫的实用解决方案。

项目成果

Convergent evolution of a labile nutritional symbiosis in ants.

蚂蚁不稳定营养共生的趋同进化。

• DOI: 10.1038/s41396-022-01256-1
• 发表时间: 2022-09
• 期刊: ISME JOURNAL
• 影响因子: 11
• 作者: Jackson, Raphaella;Monnin, David;Patapiou, Patapios A.;Golding, Gemma;Helanterae, Heikki;Oettler, Jan;Heinze, Juergen;Wurm, Yannick;Economou, Chloe K.;Chapuisat, Michel;Henry, Lee M.
• 通讯作者: Henry, Lee M.

Distinct genomic routes underlie transitions to specialised symbiotic lifestyles in deep-sea annelid worms.

• DOI: 10.1038/s41467-023-38521-6
• 发表时间: 2023-05-17
• 期刊: NATURE COMMUNICATIONS
• 影响因子: 16.6
• 作者: Moggioli, Giacomo;Panossian, Balig;Sun, Yanan;Thiel, Daniel;Martin-Zamora, Francisco M.;Tran, Martin;Clifford, Alexander M.;Goffredi, Shana K.;Rimskaya-Korsakova, Nadezhda;Jekely, Gaspar;Tresguerres, Martin;Qian, Pei-Yuan;Qiu, Jian-Wen;Rouse, Greg W.;Henry, Lee M.;Martin-Duran, Jose M.
• 通讯作者: Martin-Duran, Jose M.

Symbiont interactions with non-native hosts limit the formation of new symbioses.

• DOI: 10.1186/s12862-018-1143-z
• 发表时间: 2018-03-12
• 期刊: BMC evolutionary biology
• 影响因子: 3.4
• 作者: Niepoth N;Ellers J;Henry LM
• 通讯作者: Henry LM

The evolution of host-symbiont dependence.

• DOI: 10.1038/ncomms15973
• 发表时间: 2017-07-04
• 期刊: Nature communications
• 影响因子: 16.6
• 作者: Fisher RM;Henry LM;Cornwallis CK;Kiers ET;West SA
• 通讯作者: West SA

Evolution: The Legacy of Endosymbiosis in Ants.

进化：蚂蚁内共生的遗产。

• DOI: 10.1016/j.cub.2020.09.023
• 发表时间: 2020
• 期刊: CB
• 作者: Jackson R