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

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，对细菌多样化的程度、速度、模式和驱动因素的认识远远落后于对动物和植物的认识。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，但也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时，这些进化的多样化爆发就会发生，从而使多样化成为许多专门的类型。原生生态系统的独特定殖事件，通常是动植物适应性辐射的原因，在细菌中是极不可能的，因为它们的种群规模大，传播能力强。然而，“关键创新”的进化也可能刺激适应性辐射，这些创新开辟了新的生态机会（例如，允许裂谷湖慈鲷辐射的咽颌的进化）。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使关键创新的进化和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细菌种群的重要驱动因素仍然未知。对于后生动物和细菌来说，最剧烈的环境变化之一是海洋和陆地环境之间的变化。海洋-陆地过渡偶尔发生在细菌分类群中，并伴随着中心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式。我们将从英国康沃尔的一系列陆地和海洋栖息地中取样生态学上通用的粘杆菌，系统地研究细菌的适应性辐射。首先，我们将估计黏菌谱系从海洋生境过渡到陆地生境或反之亦然的频率。为此，我们将在复制的环境样本中对一个标记基因进行测序，以建立一个高分辨率的进化树，在此树上绘制谱系的栖息地偏好。其次，我们假设在新栖息地定居的谱系经历了适应性辐射，与留在祖先栖息地的谱系相比，在系统发育树中留下了分支率增加的印记。第三，我们将通过基于分离体的基因组测序和组装来自宏基因组的基因组来检索基因组，以确定海洋-陆地过渡的关键适应，阐明它们是否是LGT事件的结果，并探索过渡和随后的辐射的基因组后果。研究真核生物的适应性辐射有着悠久的传统。虽然理论和经验数据表明，细菌也可能经历适应性进化的爆发，但这将是第一次大规模的、有目的的对细菌适应性辐射的分析。这个开创性项目产生的结果将为研究通过不同机制在不同环境中定植的其他细菌分类群铺平道路，并更广泛地为产生原核生物多样性的宏观进化模式的详细研究提供动力，这些模式最终成为所有生态系统功能的基础。

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.