Table_5_A Large-Scale Genome-Based Survey of Acidophilic Bacteria Suggests That Genome Streamlining Is an Adaption for Life at Low pH.XLSX

The genome streamlining theory suggests that reduction of microbial genome size optimizes energy utilization in stressful environments. Although this hypothesis has been explored in several cases of low-nutrient (oligotrophic) and high-temperature environments, little work has been carried out on microorganisms from low-pH environments, and what has been reported is inconclusive. In this study, we performed a large-scale comparative genomics investigation of more than 260 bacterial high-quality genome sequences of acidophiles, together with genomes of their closest phylogenetic relatives that live at circum-neutral pH. A statistically supported correlation is reported between reduction of genome size and decreasing pH that we demonstrate is due to gene loss and reduced gene sizes. This trend is independent from other genome size constraints such as temperature and G + C content. Genome streamlining in the evolution of acidophilic bacteria is thus supported by our results. The analyses of predicted Clusters of Orthologous Genes (COG) categories and subcellular location predictions indicate that acidophiles have a lower representation of genes encoding extracellular proteins, signal transduction mechanisms, and proteins with unknown function but are enriched in inner membrane proteins, chaperones, basic metabolism, and core cellular functions. Contrary to other reports for genome streamlining, there was no significant change in paralog frequencies across pH. However, a detailed analysis of COG categories revealed a higher proportion of genes in acidophiles in the following categories: “replication and repair,” “amino acid transport,” and “intracellular trafficking”. This study brings increasing clarity regarding the genomic adaptations of acidophiles to life at low pH while putting elements, such as the reduction of average gene size, under the spotlight of streamlining theory.

基因组精简理论（genome streamlining theory）指出，在胁迫环境下，微生物基因组尺寸的缩减能够优化能量利用效率。尽管该假说已在多项寡营养（oligotrophic）环境与高温环境研究中得到验证，但针对低pH环境微生物的相关研究仍较为匮乏，且已有的报道结论并不一致。本研究对260余株高质量嗜酸菌（acidophiles）细菌基因组序列，以及其亲缘关系最近的栖息于近中性pH环境的系统发育近亲的基因组进行了大规模比较基因组学分析。研究发现，基因组尺寸缩减与pH值降低之间存在统计学上的显著相关性，且该相关性可归因于基因丢失与基因尺寸缩小。该趋势不受温度、G+C含量等其他基因组尺寸限制因素的影响。因此，本研究结果支持嗜酸菌进化过程中存在基因组精简现象。对预测的同源基因簇（Clusters of Orthologous Genes, COG）功能分类以及亚细胞定位的分析结果显示，嗜酸菌中编码胞外蛋白、信号转导机制以及功能未知蛋白的基因占比更低，但在内膜蛋白、分子伴侣、基础代谢与核心细胞功能相关蛋白的编码基因上呈现富集态势。与其他基因组精简相关报道不同的是，不同pH环境下旁系同源基因（paralog）的频率未出现显著变化。然而，对COG功能分类的详细分析显示，嗜酸菌中以下几类基因的占比更高："复制与修复"、"氨基酸转运"以及"细胞内运输"。本研究进一步明确了嗜酸菌适应低pH环境的基因组适应特征，同时将平均基因尺寸缩减等现象置于基因组精简理论的研究焦点之下。