Department of Earth System Science, Stanford University, Stanford, CA, USA.
Department of Geosciences, Princeton University, Princeton, NJ, USA.
ISME J. 2022 Apr;16(4):1140-1152. doi: 10.1038/s41396-021-01167-7. Epub 2021 Dec 6.
The terrestrial subsurface microbiome contains vastly underexplored phylogenetic diversity and metabolic novelty, with critical implications for global biogeochemical cycling. Among the key microbial inhabitants of subsurface soils and sediments are Thaumarchaeota, an archaeal phylum that encompasses ammonia-oxidizing archaea (AOA) as well as non-ammonia-oxidizing basal lineages. Thaumarchaeal ecology in terrestrial systems has been extensively characterized, particularly in the case of AOA. However, there is little knowledge on the diversity and ecophysiology of Thaumarchaeota in deeper soils, as most lineages, particularly basal groups, remain uncultivated and underexplored. Here we use genome-resolved metagenomics to examine the phylogenetic and metabolic diversity of Thaumarchaeota along a 234 cm depth profile of hydrologically variable riparian floodplain sediments in the Wind River Basin near Riverton, Wyoming. Phylogenomic analysis of the metagenome-assembled genomes (MAGs) indicates a shift in AOA population structure from the dominance of the terrestrial Nitrososphaerales lineage in the well-drained top ~100 cm of the profile to the typically marine Nitrosopumilales in deeper, moister, more energy-limited sediment layers. We also describe two deeply rooting non-AOA MAGs with numerous unexpected metabolic features, including the reductive acetyl-CoA (Wood-Ljungdahl) pathway, tetrathionate respiration, a form III RuBisCO, and the potential for extracellular electron transfer. These MAGs also harbor tungsten-containing aldehyde:ferredoxin oxidoreductase, group 4f [NiFe]-hydrogenases and a canonical heme catalase, typically not found in Thaumarchaeota. Our results suggest that hydrological variables, particularly proximity to the water table, impart a strong control on the ecophysiology of Thaumarchaeota in alluvial sediments.
陆地地下微生物组包含大量尚未充分探索的系统发育多样性和代谢新颖性，对全球生物地球化学循环具有重要意义。地下土壤和沉积物中的主要微生物类群包括氨氧化古菌（AOA）以及非氨氧化的基础类群，它们是古菌门的一部分。陆地系统中已经对 Thaumarchaeota 的生态学进行了广泛的描述，特别是在 AOA 的情况下。然而，对于深层土壤中 Thaumarchaeota 的多样性和生态生理学知之甚少，因为大多数类群，特别是基础类群，仍然未被培养和充分研究。在这里，我们使用基因组解析宏基因组学来研究怀俄明州里弗顿附近的风河流域水力变化的河岸洪泛平原沉积物中 234 厘米深度剖面中 Thaumarchaeota 的系统发育和代谢多样性。对宏基因组组装基因组（MAGs）的系统发育分析表明，AOA 种群结构发生了变化，从剖面顶部排水良好的 ~100 厘米深的优势陆地 Nitrososphaerales 谱系转变为深层、更潮湿、能量更有限的沉积物层中典型的海洋 Nitrosopumilales。我们还描述了两个深度扎根的非 AOA MAGs，它们具有许多意想不到的代谢特征，包括还原性乙酰辅酶 A（Wood-Ljungdahl）途径、连四硫酸盐呼吸、形式 III RuBisCO 以及细胞外电子转移的潜力。这些 MAGs还含有钨代醛：铁氧还蛋白氧化还原酶、第 4f 组 [NiFe]-氢化酶和典型的在 Thaumarchaeota 中未发现的完整血红素过氧化氢酶。我们的结果表明，水文变量，特别是与地下水位的接近程度，对冲积沉积物中 Thaumarchaeota 的生理生态学具有很强的控制作用。
