Candidate Phyla Radiation (CPR) bacteria from hyperalkaline ecosystems provide novel insight into their symbiotic lifestyle and ecological implications.

IF 13.8 1区 生物学 Q1 MICROBIOLOGY
Yu He, Shiyan Zhuo, Meng Li, Jie Pan, Yongguang Jiang, Yidan Hu, Robert A Sanford, Qin Lin, Weimin Sun, Na Wei, Shuming Peng, Zhou Jiang, Shuyi Li, Yongzhe Li, Yiran Dong, Liang Shi
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引用次数: 0

Abstract

Background: Candidate Phyla Radiation (CPR) represents a unique superphylum characterized by ultra-small cell size and symbiotic lifestyle. Although CPR bacteria have been identified in varied environments, their broader distribution, associations with hosts, and ecological roles remain largely unexplored. To address these knowledge gaps, a serpentinite-like environment was selected as a simplified model system to investigate the CPR communities in hyperalkaline environments and their association with hosts in extreme conditions. Additionally, the enzymatic activity, global distribution, and evolution of the CPR-derived genes encoding essential metabolites (e.g., folate or vitamin B9) were analyzed and assessed.

Results: In the highly alkaline serpentinite-like ecosystem (pH = 10.9-12.4), metagenomic analyses of the water and sediment samples revealed that CPR bacteria constituted 1.93-34.8% of the microbial communities. Metabolic reconstruction of 12 high-quality CPR metagenome-assembled genomes (MAGs) affiliated to the novel taxa from orders UBA6257, UBA9973, and Paceibacterales suggests that these bacteria lack the complete biosynthetic pathways for amino acids, lipids, and nucleotides. Notably, the CPR bacteria commonly harbored the genes associated with essential folate cofactor biosynthesis and metabolism, including dihydrofolate reductase (folA), serine hydroxymethyltransferase (glyA), and methylenetetrahydrofolate reductase (folD). Additionally, two presumed auxotrophic hosts, incapable of forming tetrahydrofolate (THF) due to the absence of folA, were identified as potential hosts for some CPR bacteria harboring folA genes. The functionality of these CPR-derived folA genes was experimentally verified by heterologous expression in the folA-deletion mutant Escherichia coli MG1655 ΔfolA. Further assessment of the available CPR genomes (n = 4,581) revealed that the genes encoding the proteins for the synthesis of bioactive folate derivatives (e.g., folA, glyA, and/or folD genes) were present in 90.8% of the genomes examined. It suggests potential widespread metabolic complementarity in folate biosynthesis between CPR and their hosts.

Conclusions: This finding deepens our understanding of the mechanisms of CPR-host symbiosis, providing novel insight into essential cofactor-dependent mutualistic CPR-host interactions. Our observations suggest that CPR bacteria may contribute to auxotrophic organisms and indirectly influence biogeochemical processes. Video Abstract.

来自高碱性生态系统的候选辐射门(CPR)细菌为其共生生活方式和生态意义提供了新的见解。
背景:候选辐射门(CPR)代表了一种独特的超门,其特征是超小细胞大小和共生生活方式。虽然心肺复苏术细菌已经在不同的环境中被发现,但它们更广泛的分布、与宿主的关系以及生态作用在很大程度上仍未被探索。为了解决这些知识空白,研究人员选择了蛇纹岩样环境作为简化模型系统,研究高碱性环境下的CPR群落及其与极端条件下宿主的关系。此外,还分析和评估了编码必需代谢物(如叶酸或维生素B9)的cpr衍生基因的酶活性、全球分布和进化。结果:在高碱性蛇纹岩样生态系统(pH = 10.9 ~ 12.4)中,水体和沉积物样本的宏基因组分析显示,CPR细菌占微生物群落的1.93 ~ 34.8%。对UBA6257、UBA9973和Paceibacterales新分类群的12个高质量CPR宏基因组组装基因组(MAGs)的代谢重建表明,这些细菌缺乏氨基酸、脂质和核苷酸的完整生物合成途径。值得注意的是,CPR细菌通常携带与必需叶酸辅助因子生物合成和代谢相关的基因,包括二氢叶酸还原酶(folA)、丝氨酸羟甲基转移酶(glyA)和亚甲基四氢叶酸还原酶(folD)。此外,两个假定的营养不良宿主,由于缺乏叶酸而不能形成四氢叶酸(THF),被确定为一些含有叶酸基因的CPR细菌的潜在宿主。通过在folA缺失突变型大肠杆菌MG1655 ΔfolA中异源表达,实验证实了这些由心肺复写衍生的folA基因的功能。对现有CPR基因组(n = 4,581)的进一步评估显示,编码合成生物活性叶酸衍生物的蛋白质的基因(例如,folA, glyA和/或folD基因)存在于90.8%的检测基因组中。这表明心肺复苏术与寄主之间叶酸生物合成可能存在广泛的代谢互补。结论:这一发现加深了我们对心肺复苏-宿主共生机制的理解,为心肺复苏-宿主相互作用的基本辅因子依赖提供了新的见解。我们的观察表明,CPR细菌可能有助于营养不良生物,并间接影响生物地球化学过程。视频摘要。
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来源期刊
Microbiome
Microbiome MICROBIOLOGY-
CiteScore
21.90
自引率
2.60%
发文量
198
审稿时长
4 weeks
期刊介绍: Microbiome is a journal that focuses on studies of microbiomes in humans, animals, plants, and the environment. It covers both natural and manipulated microbiomes, such as those in agriculture. The journal is interested in research that uses meta-omics approaches or novel bioinformatics tools and emphasizes the community/host interaction and structure-function relationship within the microbiome. Studies that go beyond descriptive omics surveys and include experimental or theoretical approaches will be considered for publication. The journal also encourages research that establishes cause and effect relationships and supports proposed microbiome functions. However, studies of individual microbial isolates/species without exploring their impact on the host or the complex microbiome structures and functions will not be considered for publication. Microbiome is indexed in BIOSIS, Current Contents, DOAJ, Embase, MEDLINE, PubMed, PubMed Central, and Science Citations Index Expanded.
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