Genome-Resolved Metagenomics Extends the Environmental Distribution of the Verrucomicrobia Phylum to the Deep Terrestrial Subsurface

Genome-Resolved Metagenomics Extends the Environmental Distribution of the Verrucomicrobia Phylum to the Deep Terrestrial Subsurface
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DOI:
10.1128/msphere.00613-19
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发表时间:
2019-11-01
期刊:
影响因子:
4.8
通讯作者:
Wrighton, Kelly C.
Wrighton, Kelly C.
中科院分区:
生物学2区
文献类型:
--
作者:
Nixon, Sophie L.;Daly, Rebecca A.;Wrighton, Kelly C.

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疣微菌门的细菌普遍存在,并且在土壤和淡水环境中特别常见。它们的世界性分布和报道的多糖降解能力表明疣微菌属成员是地球生态系统碳循环的重要贡献者。尽管Verrucomicrobia普遍存在,但其在分离物收集和基因组数据库中的代表性不足;因此,它们的生理生态作用可能无法完全实现。在这里,我们扩大基因组抽样的Verrucomicrobia门描述了一个新的属,“马塞利乌斯”,属于该命令Opitutales。Marcellius”是从水力压裂后313天收集的页岩衍生生产流体宏基因组中回收的,这是迄今为止发现的最深的环境。我们发现了可以解释这种生物体栖息在页岩气井中的能力的基因组属性,包括利用水力压裂液中常见的有机聚合物,固氮,适应高盐度以及通过CRISPR-Cas获得的适应性免疫的潜力。为了阐明这些代谢和适应性特征在Verrucomicrobia门中的系统发育和环境分布,我们对31个公开的、几乎完整的Verrucomicrobia基因组进行了比较基因组分析。我们的基因组研究结果将疣微菌的环境分布扩展到陆地地下2.3公里。此外,我们揭示的性状广泛编码的Verrucomicrobia的成员,包括降解半纤维素的能力,以适应物理和生物环境的扰动,从而有助于广泛的栖息地范围报告为这个phylum.IMPORTANCE的Verrucomicrobia门的细菌是广泛存在于许多不同的生态系统,但是,它在微生物群落中的作用仍然知之甚少。疣微菌通常是低丰度的社区成员,但以前的研究表明,它们在有机碳降解中发挥着重要作用。虽然疣微菌在培养物中的代表性仍然很差,但近年来已经从宏基因组数据集重建了许多基因组。对整个门的基因组进行研究可以广泛评估其潜在的生态系统作用。这项工作的意义是(i)在地下2.3公里处恢复一种新的Verrucomicrobia属,能够承受这种环境的极端条件,以及(ii)迄今为止对Verrucomicrobia基因组编码的生理生态特征进行了最广泛的评估。我们表明,这个门的成员是专业的有机聚合物降解剂,可以承受更广泛的环境条件比以前认为的。
Bacteria of the phylum Verrucomicrobia are prevalent and are particularly common in soil and freshwater environments. Their cosmopolitan distribution and reported capacity for polysaccharide degradation suggests members of Verrucomicrobia are important contributors to carbon cycling across Earth's ecosystems. Despite their prevalence, the Verrucomicrobia are underrepresented in isolate collections and genome databases; consequently, their ecophysiological roles may not be fully realized. Here, we expand genomic sampling of the Verrucomicrobia phylum by describing a novel genus, "Candidatus Marcellius," belonging to the order Opitutales. Marcellius" was recovered from a shale-derived produced fluid metagenome collected 313 days after hydraulic fracturing, the deepest environment from which a member of the Verrucomicrobia has been recovered to date. We uncover genomic attributes that may explain the capacity of this organism to inhabit a shale gas well, including the potential for utilization of organic polymers common in hydraulic fracturing fluids, nitrogen fixation, adaptation to high salinities, and adaptive immunity via CRISPR-Cas. To illuminate the phylogenetic and environmental distribution of these metabolic and adaptive traits across the Verrucomicrobia phylum, we performed a comparative genomic analysis of 31 publicly available, nearly complete Verrucomicrobia genomes. Our genomic findings extend the environmental distribution of the Verrucomicrobia 2.3 kilometers into the terrestrial subsurface. Moreover, we reveal traits widely encoded across members of the Verrucomicrobia, including the capacity to degrade hemicellulose and to adapt to physical and biological environmental perturbations, thereby contributing to the expansive habitat range reported for this phylum.IMPORTANCE The Verrucomicrobia phylum of bacteria is widespread in many different ecosystems; however, its role in microbial communities remains poorly understood. Verrucomicrobia are often low-abundance community members, yet previous research suggests they play a major role in organic carbon degradation. While Verrucomicrobia remain poorly represented in culture collections, numerous genomes have been reconstructed from metagenomic data sets in recent years. The study of genomes from across the phylum allows for an extensive assessment of their potential ecosystem roles. The significance of this work is (i) the recovery of a novel genus of Verrucomicrobia from 2.3 km in the subsurface with the ability to withstand the extreme conditions that characterize this environment, and (ii) the most extensive assessment of ecophysiological traits encoded by Verrucomicrobia genomes to date. We show that members of this phylum are specialist organic polymer degraders that can withstand a wider range of environmental conditions than previously thought.