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A spectrum of verticality across genes
PLOS Genetics ( IF 4.0 ) Pub Date : 2020-11-02 , DOI: 10.1371/journal.pgen.1009200
Falk S P Nagies 1 , Julia Brueckner 1 , Fernando D K Tria 1 , William F Martin 1
Affiliation  

Lateral gene transfer (LGT) has impacted prokaryotic genome evolution, yet the extent to which LGT compromises vertical evolution across individual genes and individual phyla is unknown, as are the factors that govern LGT frequency across genes. Estimating LGT frequency from tree comparisons is problematic when thousands of genomes are compared, because LGT becomes difficult to distinguish from phylogenetic artefacts. Here we report quantitative estimates for verticality across all genes and genomes, leveraging a well-known property of phylogenetic inference: phylogeny works best at the tips of trees. From terminal (tip) phylum level relationships, we calculate the verticality for 19,050,992 genes from 101,422 clusters in 5,655 prokaryotic genomes and rank them by their verticality. Among functional classes, translation, followed by nucleotide and cofactor biosynthesis, and DNA replication and repair are the most vertical. The most vertically evolving lineages are those rich in ecological specialists such as Acidithiobacilli, Chlamydiae, Chlorobi and Methanococcales. Lineages most affected by LGT are the α-, β-, γ-, and δ- classes of Proteobacteria and the Firmicutes. The 2,587 eukaryotic clusters in our sample having prokaryotic homologues fail to reject eukaryotic monophyly using the likelihood ratio test. The low verticality of α-proteobacterial and cyanobacterial genomes requires only three partners—an archaeal host, a mitochondrial symbiont, and a plastid ancestor—each with mosaic chromosomes, to directly account for the prokaryotic origin of eukaryotic genes. In terms of phylogeny, the 100 most vertically evolving prokaryotic genes are neither representative nor predictive for the remaining 97% of an average genome. In search of factors that govern LGT frequency, we find a simple but natural principle: Verticality correlates strongly with gene distribution density, LGT being least likely for intruding genes that must replace a preexisting homologue in recipient chromosomes. LGT is most likely for novel genetic material, intruding genes that encounter no competing copy.



中文翻译:


跨基因的垂直度谱



横向基因转移 (LGT) 影响了原核基因组进化,但 LGT 在多大程度上损害了单个基因和单个门的垂直进化,以及控制跨基因 LGT 频率的因素也是未知的。当比较数千个基因组时,通过树比较估计 LGT 频率是有问题的,因为 LGT 变得很难与系统发育人工制品区分开来。在这里,我们报告了所有基因和基因组垂直性的定量估计,利用系统发育推断的众所周知的特性:系统发育在树的尖端最有效。根据末端(顶端)门水平关系,我们计算了 5,655 个原核生物基因组中 101,422 个簇的 19,050,992 个基因的垂直度,并按其垂直度对它们进行排序。在功能类别中,翻译最为垂直,其次是核苷酸和辅因子生物合成,以及DNA复制和修复。最垂直进化的谱系是那些富含生态专家的谱系,例如酸硫杆菌、衣原体、绿球菌和甲烷球菌。受 LGT 影响最大的谱系是变形菌门和厚壁菌门的 α-、β-、γ- 和 δ- 类。我们的样本中具有原核同源物的 2,587 个真核簇未能使用似然比检验拒绝真核单系。 α-变形菌和蓝藻基因组的垂直度较低,只需要三个伙伴——古菌宿主、线粒体共生体和质体祖先——每个伙伴都具有嵌合染色体,就可以直接解释真核基因的原核起源。就系统发育而言,100 个最垂直进化的原核基因既不能代表也不能预测平均基因组的其余 97%。 在寻找控制 LGT 频率的因素时,我们发现了一个简单但自然的原则:垂直度与基因分布密度密切相关,LGT 最不可能出现必须取代受体染色体中预先存在的同源物的入侵基因。 LGT 最有可能是新的遗传物质,即侵入没有遇到竞争副本的基因。

更新日期:2020-11-03
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