Macro-evolution in microorganisms: marine-terrestrial transitions as a case-study for adaptive radiations in bacteria

微生物的宏观进化：海洋-陆地转变作为细菌适应性辐射的案例研究

• 批准号: NE/T008083/1
• 负责人: Michiel Vos
• 金额: $ 70.51万
• 依托单位: UNIVERSITY OF EXETER
• 依托单位国家: 英国
• 项目类别: Research Grant
• 财政年份: 2021
• 资助国家: 英国
• 起止时间: 2021 至 无数据
• 项目状态: 未结题
• 来源: https://gtr.ukri.org/projects?ref=NE%2FT008083%2F1
• 关键词: Macro; evolution; microorganisms; marine; terrestrial

Understanding the ecological and evolutionary drivers of biodiversity is of central importance to biology. However, knowledge on the extent, tempo, mode, and drivers of bacterial diversification greatly lags behind that of animals and plants. This knowledge gap is problematic, as bacteria are fundamental to biogeochemistry and ecosystem functioning, agriculture, industry, and human health, but also because there is great intrinsic value in understanding the evolution of the most ancient and diverse group of organisms on the planet.Adaptive radiations arguably form the best examples of the power of natural selection to generate biodiversity. These evolutionary bursts of diversification occur when a single ancestral type is faced with ecological opportunity enabling diversification into a multitude of specialised types. Unique colonisation events of virgin ecosystems, often the cause of adaptive radiations in animals and plants, are highly improbable in bacteria because of their large population sizes and high dispersal capacity. However, adaptive radiations could also be spurred by the evolution of 'key innovations' that open up new ecological opportunity (e.g. the evolution of the pharyngeal jaw allowing radiation of Rift Lake cichlids). It can be hypothesised that the extraordinary ability of bacteria to acquire novel traits via Lateral Gene Transfer (LGT) could make the evolution of key innovations and thus subsequent adaptive radiations especially prevalent. However, despite having a long history of research in multicellular organisms, it remains unknown whether adaptive radiations are an important driver in natural bacterial populations.One of the most drastic environmental transitions for metazoans and bacteria alike is that between marine and terrestrial environments. Marine-terrestrial transitions occasionally occur in bacterial taxa and are accompanied by significant rewiring of central metabolism. These transitions thus present an excellent model for the exploration of novel adaptive zones through key innovations. We will sample the ecologically versatile Myxobacteria from a range of terrestrial and marine habitats in Cornwall, U.K. to systematically study adaptive radiations in bacteria. First, we will estimate the frequency whereby myxobacterial lineages transition from marine to terrestrial habitats or vice versa. To do so, we will sequence a marker gene in replicated environmental samples to build a high-resolution evolutionary tree on which habitat preferences of lineages are mapped. Second, we hypothesise that lineages that colonise new habitats undergo adaptive radiations, leaving an imprint of increased branching rate in the phylogenetic tree compared to lineages that remain in their ancestral habitat. Third, we will retrieve genomes through isolate-based genome sequencing and by assembling genomes from metagenomes to identify the key adaptation(s) underlying marine-terrestrial transitions, elucidate whether they are the result of LGT events, and to explore the genomic consequences of a transition and subsequent radiation. There is a rich tradition of studying adaptive radiations in eukaryotes. Although theory and empirical data suggest that bacteria could likewise experience bursts of adaptive evolution, this will be the first largescale, purpose-designed analysis of adaptive radiations in bacteria. Results generated in this pioneering project will pave the way for studies in other bacterial taxa colonising different environments through different mechanisms and more generally provide impetus for the detailed study of macro-evolutionary patterns generating prokaryote diversity which ultimately underlies the functioning of all ecosystems.

了解生物多样性的生态和进化驱动因素对生物学至关重要。然而，关于细菌多样化的程度、克里思、模式和驱动因素的知识远远落后于动物和植物。这种知识差距是有问题的，因为细菌是生物地球化学和生态系统功能、农业、工业和人类健康的基础，而且还因为了解地球上最古老和最多样化的生物群体的进化具有巨大的内在价值。适应性辐射可以说是自然选择产生生物多样性的力量的最好例子。当一个单一的祖先类型面临生态机会，使多样化成为众多的专业类型时，这些多样化的进化爆发就会发生。原生生态系统的独特殖民事件，通常是动物和植物适应性辐射的原因，在细菌中是极不可能的，因为它们的人口规模大，传播能力强。然而，适应性辐射也可能受到“关键创新”的进化的刺激，这些创新开辟了新的生态机会（例如，咽颚的进化允许裂谷湖慈鲷的辐射）。可以假设，细菌通过横向基因转移（LGT）获得新特性的非凡能力可能会使关键创新的进化以及随后的适应性辐射特别普遍。然而，尽管对多细胞生物的研究历史悠久，但适应性辐射是否是自然界细菌种群的重要驱动力仍然是未知的。对于后生动物和细菌来说，最剧烈的环境转变之一是海洋和陆地环境之间的转变。海洋-陆地过渡偶尔发生在细菌类群中，并伴随着中央代谢的重大重新布线。因此，这些转变为通过关键创新探索新的适应区提供了一个很好的模型。我们将从英国康沃尔郡的一系列陆地和海洋栖息地采集生态多功能粘细菌样本。系统地研究细菌的适应性辐射。首先，我们将估计粘细菌谱系从海洋到陆地栖息地或反之亦然过渡的频率。为此，我们将在复制的环境样本中对标记基因进行测序，以建立一个高分辨率的进化树，在此基础上绘制谱系的栖息地偏好。其次，我们假设，血统殖民新的栖息地进行适应性辐射，留下的印记，增加分支率的系统发育树相比，血统留在他们的祖先栖息地。第三，我们将通过基于分离物的基因组测序和从宏基因组组装基因组来检索基因组，以确定海洋-陆地转变的关键适应，阐明它们是否是LGT事件的结果，并探索转变和随后辐射的基因组后果。研究真核生物的适应性辐射有着丰富的传统。尽管理论和经验数据表明，细菌也可能经历适应性进化的爆发，但这将是第一次对细菌适应性辐射进行大规模、有目的的分析。在这个开创性的项目中产生的结果将为其他细菌类群通过不同机制在不同环境中定居的研究铺平道路，并更普遍地为宏观进化模式的详细研究提供动力，从而产生原核生物多样性，最终成为所有生态系统功能的基础。

项目成果

Myxococcus xanthus.

黄色粘球菌。

• DOI: 10.1016/j.tim.2021.03.006
• 发表时间: 2021
• 期刊: Trends in microbiology
• 影响因子: 15.9
• 作者: Vos M

Accessory microbiomes.

• DOI: 10.1099/mic.0.001332
• 发表时间: 2023-05
• 期刊: MICROBIOLOGY-SGM
• 影响因子: 2.8
• 作者: Vos, Michiel

A new test suggests hundreds of amino acid polymorphisms in humans are subject to balancing selection.

• DOI: 10.1371/journal.pbio.3001645
• 发表时间: 2022-06
• 期刊: PLOS BIOLOGY
• 影响因子: 9.8
• 作者: Soni, Vivak;Vos, Michiel;Eyre-Walker, Adam
• 通讯作者: Eyre-Walker, Adam

Adaptive radiations in natural populations of prokaryotes: innovation is key.

• DOI: 10.1093/femsec/fiad154
• 发表时间: 2023-11-13
• 期刊: FEMS microbiology ecology
• 影响因子: 4.2

Copper selects for siderophore-mediated virulence in Pseudomonas aeruginosa.

• DOI: 10.1186/s12866-022-02720-w
• 发表时间: 2022-12-13
• 期刊: BMC MICROBIOLOGY
• 影响因子: 4.2
• 作者: Lear, Luke;Hesse, Elze;Buckling, Angus;Vos, Michiel
• 通讯作者: Vos, Michiel