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Sulfur cycling and host-virus interactions in Aquificales-dominated biofilms from Yellowstone’s hottest ecosystems
The ISME Journal ( IF 11.0 ) Pub Date : 2021-10-14 , DOI: 10.1038/s41396-021-01132-4
Luke J McKay 1, 2, 3 , Olivia D Nigro 4 , Mensur Dlakić 5 , Karen M Luttrell 6 , Douglas B Rusch 7 , Matthew W Fields 2, 5 , William P Inskeep 1, 2
Affiliation  

Modern linkages among magmatic, geochemical, and geobiological processes provide clues about the importance of thermophiles in the origin of biogeochemical cycles. The aim of this study was to identify the primary chemoautotrophs and host–virus interactions involved in microbial colonization and biogeochemical cycling at sublacustrine, vapor-dominated vents that represent the hottest measured ecosystems in Yellowstone National Park (~140 °C). Filamentous microbial communities exposed to extreme thermal and geochemical gradients were sampled using a remotely operated vehicle and subjected to random metagenome sequencing and microscopic analyses. Sulfurihydrogenibium (phylum Aquificae) was the predominant lineage (up to 84% relative abundance) detected at vents that discharged high levels of dissolved H2, H2S, and CO2. Metabolic analyses indicated carbon fixation by Sulfurihydrogenibium spp. was powered by the oxidation of reduced sulfur and H2, which provides organic carbon for heterotrophic community members. Highly variable Sulfurihydrogenibium genomes suggested the importance of intra-population diversity under extreme environmental and viral pressures. Numerous lytic viruses (primarily unclassified taxa) were associated with diverse archaea and bacteria in the vent community. Five circular dsDNA uncultivated virus genomes (UViGs) of ~40 kbp length were linked to the Sulfurihydrogenibium metagenome-assembled genome (MAG) by CRISPR spacer matches. Four UViGs contained consistent genome architecture and formed a monophyletic cluster with the recently proposed Pyrovirus genus within the Caudovirales. Sulfurihydrogenibium spp. also contained CRISPR arrays linked to plasmid DNA with genes for a novel type IV filament system and a highly expressed β-barrel porin. A diverse suite of transcribed secretion systems was consistent with direct microscopic analyses, which revealed an extensive extracellular matrix likely critical to community structure and function. We hypothesize these attributes are fundamental to the establishment and survival of microbial communities in highly turbulent, extreme-gradient environments.



中文翻译:

黄石最热生态系统中 Aquificales 主导的生物膜中的硫循环和宿主-病毒相互作用

岩浆、地球化学和地球生物学过程之间的现代联系提供了关于嗜热生物在生物地球化学循环起源中的重要性的线索。本研究的目的是确定在代表黄石国家公园 (~140 °C) 最热测量生态系统的湖下、以蒸汽为主的喷口处微生物定植和生物地球化学循环所涉及的主要化学自养生物和宿主-病毒相互作用。使用远程操作的车辆对暴露于极端温度和地球化学梯度的丝状微生物群落进行采样,并进行随机宏基因组测序和显微分析。Sulfurihydrogenibium(水质) 是在排放高水平溶解 H 2、H 2 S 和 CO 2的喷口检测到的主要谱系(相对丰度高达 84%)。代谢分析表明通过Sulfurihydrogenibium spp. 进行碳固定。由还原硫和 H 2的氧化提供动力,为异养群落成员提供有机碳。高度可变的硫氢化铌基因组表明在极端环境和病毒压力下种群内多样性的重要性。许多裂解病毒(主要是未分类的分类群)与喷口群落中的多种古细菌和细菌有关。五个长度约为 40 kbp 的环状 dsDNA 未培养病毒基因组 (UViGs)通过 CRISPR 间隔子匹配与Sulfurihydrogenibium宏基因组组装基因组 (MAG)相关联。四个 UViGs 包含一致的基因组结构,并与最近提出的有尾病毒目中的Pyrovirus属形成单系群。硫氢铌属 还包含与质粒 DNA 相连的 CRISPR 阵列,质粒 DNA 具有新型 IV 型丝系统和高表达的 β-桶状孔蛋白的基因。一组不同的转录分泌系统与直接显微镜分析一致,这表明广泛的细胞外基质可能对群落结构和功能至关重要。我们假设这些属性是微生物群落在高度动荡、极端梯度环境中建立和生存的基础。

更新日期:2021-10-14
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