Department of Land Resources & Environmental Sciences, Montana State University, Bozeman, MT, 59717, USA.
Thermal Biology Institute, Montana State University, Bozeman, MT, 59717, USA.
ISME J. 2022 Mar;16(3):842-855. doi: 10.1038/s41396-021-01132-4. Epub 2021 Oct 14.
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 H, HS, and CO. Metabolic analyses indicated carbon fixation by Sulfurihydrogenibium spp. was powered by the oxidation of reduced sulfur and H, 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.
现代岩浆、地球化学和地球生物学过程之间的联系为嗜热菌在生物地球化学循环起源中的重要性提供了线索。本研究的目的是确定参与微生物定殖和生物地球化学循环的主要化能自养生物和宿主-病毒相互作用，这些微生物定殖和生物地球化学循环发生在亚湖底、蒸汽主导的喷口，这些喷口代表黄石国家公园（~140°C）中测量到的最热生态系统。使用远程操作车辆对暴露在极端热和地球化学梯度下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镜分析。在排放高浓度溶解 H、HS 和 CO 的喷口处，检测到硫氢杆菌（Aquificae 门）是主要的谱系（相对丰度高达 84%）。代谢分析表明，硫氢杆菌属 spp 的碳固定是由还原硫和 H 的氧化驱动的，这为异养群落成员提供了有机碳。高度可变的硫氢杆菌属基因组表明，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）与喷口群落中的各种古菌和细菌相关。五个约 40 kbp 长的圆形 dsDNA 未培养病毒基因组（UViGs）通过 CRISPR 间隔匹配与硫氢杆菌宏基因组组装基因组（MAG）相关联。四个 UViGs 具有一致的基因组结构，并与最近提出的 Caudovirales 中的 Pyrovirus 属形成单系聚类。硫氢杆菌属还包含与质粒 DNA 相关的 CRISPR 阵列，该质粒 DNA 具有用于新型 IV 型丝系统和高度表达的β桶孔蛋白的基因。转录分泌系统的多样性与直接显微镜分析一致，这揭示了广泛的细胞外基质，这可能对群落结构和功能至关重要。我们假设这些特征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。
