Associate Laboratory i4HB, Institute for Health and Bioeconomy and UCIBIO, Applied Molecular Biosciences Unit, Department of Life Sciences, NOVA School of Science and Technology, Universidade NOVA de Lisboa, Caparica, Portugal.
UCIBIO-i4HB, Departamento de Ciências da Vida, Faculdade de Ciências e Tecnologia, Universidade Nova de Lisboa, Caparica, Portugal.
Appl Environ Microbiol. 2024 Nov 20;90(11):e0125724. doi: 10.1128/aem.01257-24. Epub 2024 Oct 23.
Distantly related organisms may evolve similar traits when exposed to similar environments or engaging in certain lifestyles. Several members of the Lactobacillaceae [lactic acid bacteria (LAB)] family are frequently isolated from the floral niche, mostly from bees and flowers. In some floral LAB species (henceforth referred to as bee-associated LAB), distinctive genomic (e.g., genome reduction) and phenotypic (e.g., preference for fructose over glucose or fructophily) features were recently documented. These features are found across distantly related species, raising the hypothesis that specific genomic and phenotypic traits evolved convergently during adaptation to the floral environment. To test this hypothesis, we examined representative genomes of 369 species of bee-associated and non-bee-associated LAB. Phylogenomic analysis unveiled seven independent ecological shifts toward the bee environment in LAB. In these species, we observed significant reductions of genome size, gene repertoire, and GC content. Using machine leaning, we could distinguish bee-associated from non-bee-associated species with 94% accuracy, based on the absence of genes involved in metabolism, osmotic stress, or DNA repair. Moreover, we found that the most important genes for the machine learning classifier were seemingly lost, independently, in multiple bee-associated lineages. One of these genes, acetaldehyde-alcohol dehydrogenase (), encodes a bifunctional aldehyde-alcohol dehydrogenase which has been associated with the evolution of fructophily, a rare phenotypic trait that is pervasive across bee-associated LAB species. These results suggest that the independent evolution of distinctive phenotypes in bee-associated LAB has been largely driven by independent losses of the same sets of genes.IMPORTANCESeveral LAB species are intimately associated with bees and exhibit unique biochemical properties with potential for food applications and honeybee health. Using a machine learning-based approach, our study shows that adaptation of LAB to the bee environment was accompanied by a distinctive genomic trajectory deeply shaped by gene loss. Several of these gene losses occurred independently in distantly related species and are linked to some of their unique biotechnologically relevant traits, such as the preference for fructose over glucose (fructophily). This study underscores the potential of machine learning in identifying fingerprints of adaptation and detecting instances of convergent evolution. Furthermore, it sheds light onto the genomic and phenotypic particularities of bee-associated bacteria, thereby deepening the understanding of their positive impact on honeybee health.
亲缘关系较远的生物在暴露于相似环境或从事特定生活方式时，可能会进化出相似的特征。乳杆菌科[乳酸细菌 (LAB)]家族的几个成员经常从花区分离出来，主要来自蜜蜂和花朵。在一些花区 LAB 物种（以下简称与蜜蜂相关的 LAB）中，最近记录了独特的基因组（例如，基因组减少）和表型（例如，对果糖的偏好而不是葡萄糖或果糖）特征。这些特征在亲缘关系较远的物种中都有发现，这提出了一个假设，即特定的基因组和表型特征在适应花环境的过程中趋同进化。为了检验这一假设，我们检查了 369 种与蜜蜂相关和非与蜜蜂相关的 LAB 代表基因组。系统基因组分析揭示了 LAB 中向蜜蜂环境的 7 次独立生态转变。在这些物种中，我们观察到基因组大小、基因库和 GC 含量的显著减少。使用机器学习，我们可以根据参与代谢、渗透胁迫或 DNA 修复的基因不存在，以 94%的准确率将与蜜蜂相关的物种与非与蜜蜂相关的物种区分开来。此外，我们发现，对于机器学习分类器最重要的基因似乎是独立地在多个与蜜蜂相关的谱系中丢失的。这些基因之一，乙醛-乙醇脱氢酶（），编码一种双功能醛-乙醇脱氢酶，它与果糖的进化有关，果糖是一种罕见的表型特征，在与蜜蜂相关的 LAB 物种中普遍存在。这些结果表明，与蜜蜂相关的 LAB 中独特表型的独立进化主要是由相同基因集的独立缺失驱动的。
重要的是，一些 LAB 物种与蜜蜂密切相关，具有独特的生化特性，具有食品应用和蜜蜂健康的潜力。使用基于机器学习的方法，我们的研究表明，LAB 对蜜蜂环境的适应伴随着独特的基因组轨迹，该轨迹深受基因缺失的影响。这些基因缺失中的几个在亲缘关系较远的物种中独立发生，与它们一些独特的生物技术相关特征有关，例如对果糖的偏好而不是葡萄糖（果糖）。这项研究强调了机器学习在识别适应的指纹和检测趋同进化实例方面的潜力。此外，它揭示了与蜜蜂相关的细菌的基因组和表型特征，从而加深了对它们对蜜蜂健康的积极影响的理解。
