Patterns and implications of gene gain and loss in the evolution of Prochlorococcus.
Patterns and implications of gene gain and loss in the evolution of Prochlorococcus.
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DOI：
10.1371/journal.pgen.0030231
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发表时间：
2007-12
期刊：
影响因子：
4.5
通讯作者：
Chisholm SW
中科院分区：
文献类型：
--
作者：
Kettler GC;Martiny AC;Huang K;Zucker J;Coleman ML;Rodrigue S;Chen F;Lapidus A;Ferriera S;Johnson J;Steglich C;Church GM;Richardson P;Chisholm SW
原绿球藻是一种海洋蓝细菌，在数量上占主导地位的中纬度海洋，是最小的已知产氧光合生物。来自世界海洋不同区域的许多分离物已被研究，并显示出生理和遗传上的独特性。到目前为止描述的所有分离株可以被分配到一个紧密聚集的高光（HL）适应的分支，或一个更发散的低光（LL）适应组。整个原绿球藻组的16S rRNA序列最多相差3%，四个最初发表的基因组揭示了遗传分化的模式，有助于解释分离株之间的生理差异。在这里，我们描述了8个新测序的菌株的基因组和联合收割机他们与前四个基因组的核心（共享的所有分离物）和灵活的基因的原绿球藻组的综合分析，以及在进化过程中的灵活的基因的丢失和获得的模式。有1,273个基因代表所有12个基因组共享的核心。根据代谢重建，它们显然足以编码一个功能细胞。我们描述了所有12个菌株的同源性，通过对它们的完整蛋白质组进行三种不同的系统发育分析。对于每个非核心基因，我们使用最大简约法来估计哪个祖先可能首先获得或丢失每个基因。分离物之间的许多遗传差异，特别是涉及外膜合成和营养物质运输的基因，被发现在同一分支内。尽管如此，我们确定了一些基因定义HL和LL生态型，这些广泛的生态型和分支，有助于证明HL和LL适应原绿球藻的基础。此外，我们对基因获得事件的估计使我们能够识别通过简单的成对比较不明显的高度可变的基因组岛。这些结果强调了功能作用，特别是那些与外膜合成和运输有关的功能作用，这些功能作用主导了灵活的基因组，并将其与核心分开。除了确定岛屿并证明它们在原绿球藻历史上的作用外，对过去基因获得和损失的重建表明，大部分变异存在于最密切相关的菌株之间的"树叶"。最后，从这12个基因组比较中识别出的核心和灵活基因与全球海洋宏基因组数据库中发现的原绿球藻基因的相对频率基本一致，进一步缩小了我们在实验室和野生环境中对这些生物的理解之间的差距。 原绿球藻是生活在广阔的海洋中最丰富的光合作用微生物，是全球碳循环的主要贡献者。原绿球藻是由密切相关的，生理上不同的谱系，其差异使该集团作为一个整体，在广泛的环境条件增殖。我们比较了12株原绿球藻代表其主要谱系的基因组，以确定影响不同谱系生态及其进化起源的遗传差异。首先，我们确定了核心基因组：所有菌株共有的1,273个基因。这组核心基因编码功能细胞的基本要素，使其能够利用阳光和二氧化碳制造生命物质。然后，我们创建了一个基因组树，绘制了各个菌株中非核心基因的获得和丢失，显示即使在最密切相关的菌株中，也有大量基因获得或丢失。我们发现丢失和获得的基因通常聚集在称为基因组岛的高度可变区域。非核心基因之间的多样性水平，以及每个新基因组测序后增加的新基因数量，表明有待发现的多样性要多得多。
Prochlorococcus is a marine cyanobacterium that numerically dominates the mid-latitude oceans and is the smallest known oxygenic phototroph. Numerous isolates from diverse areas of the world's oceans have been studied and shown to be physiologically and genetically distinct. All isolates described thus far can be assigned to either a tightly clustered high-light (HL)-adapted clade, or a more divergent low-light (LL)-adapted group. The 16S rRNA sequences of the entire Prochlorococcus group differ by at most 3%, and the four initially published genomes revealed patterns of genetic differentiation that help explain physiological differences among the isolates. Here we describe the genomes of eight newly sequenced isolates and combine them with the first four genomes for a comprehensive analysis of the core (shared by all isolates) and flexible genes of the Prochlorococcus group, and the patterns of loss and gain of the flexible genes over the course of evolution. There are 1,273 genes that represent the core shared by all 12 genomes. They are apparently sufficient, according to metabolic reconstruction, to encode a functional cell. We describe a phylogeny for all 12 isolates by subjecting their complete proteomes to three different phylogenetic analyses. For each non-core gene, we used a maximum parsimony method to estimate which ancestor likely first acquired or lost each gene. Many of the genetic differences among isolates, especially for genes involved in outer membrane synthesis and nutrient transport, are found within the same clade. Nevertheless, we identified some genes defining HL and LL ecotypes, and clades within these broad ecotypes, helping to demonstrate the basis of HL and LL adaptations in Prochlorococcus. Furthermore, our estimates of gene gain events allow us to identify highly variable genomic islands that are not apparent through simple pairwise comparisons. These results emphasize the functional roles, especially those connected to outer membrane synthesis and transport that dominate the flexible genome and set it apart from the core. Besides identifying islands and demonstrating their role throughout the history of Prochlorococcus, reconstruction of past gene gains and losses shows that much of the variability exists at the “leaves of the tree,” between the most closely related strains. Finally, the identification of core and flexible genes from this 12-genome comparison is largely consistent with the relative frequency of Prochlorococcus genes found in global ocean metagenomic databases, further closing the gap between our understanding of these organisms in the lab and the wild. Prochlorococcus—the most abundant photosynthetic microbe living in the vast, nutrient-poor areas of the ocean—is a major contributor to the global carbon cycle. Prochlorococcus is composed of closely related, physiologically distinct lineages whose differences enable the group as a whole to proliferate over a broad range of environmental conditions. We compare the genomes of 12 strains of Prochlorococcus representing its major lineages in order to identify genetic differences affecting the ecology of different lineages and their evolutionary origin. First, we identify the core genome: the 1,273 genes shared among all strains. This core set of genes encodes the essentials of a functional cell, enabling it to make living matter out of sunlight and carbon dioxide. We then create a genomic tree that maps the gain and loss of non-core genes in individual strains, showing that a striking number of genes are gained or lost even among the most closely related strains. We find that lost and gained genes commonly cluster in highly variable regions called genomic islands. The level of diversity among the non-core genes, and the number of new genes added with each new genome sequenced, suggest far more diversity to be discovered.
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