Heterotrophic Thaumarchaea with Small Genomes Are Widespread in the Dark Ocean
Heterotrophic Thaumarchaea with Small Genomes Are Widespread in the Dark Ocean
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DOI：
10.1128/msystems.00415-20
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发表时间：
2020-05-01
期刊：
影响因子：
6.4
通讯作者：
Santoro, Alyson E.
中科院分区：
文献类型：
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作者：
Aylward, Frank O.;Santoro, Alyson E.
Thaumarchaeota是一个多样化的古菌门，包括许多谱系，在全球生物地球化学循环中发挥关键作用，特别是在海洋中。迄今为止，所有基因组特征的海洋thaumarchaea据报道是化能自养氨氧化剂。在这项研究中，我们报告了一组puperium异养海洋thaumarchaea（HMT）的小基因组大小，是全球丰富的中层，显然缺乏氧化氨的能力。我们从宏基因组数据中组装了五个HMT基因组，并表明它们与氨氧化古菌（AOA）形成了一个分支很深的姐妹谱系。我们确定这组在所有主要海洋盆地的中层沃茨的宏基因组中，丰度达到AOA的6%。令人惊讶的是，我们预测HMT具有类似于1 Mbp的小基因组，并且我们的祖先状态重建表明，与其他相关古细菌相比，该谱系经历了大量的基因组减少。HMT的基因组库表明了有氧化能有机异养的多功能代谢，包括一个发散的形式III-a RuBisCO，一个2 M呼吸复合物I，已被假设为增加能量效率，和一个三亚基血红素-铜氧化酶复合物IV，这是从AOA缺席。我们还确定了21个吡咯喹啉醌（PQQ）依赖的脱氢酶，预计提供还原当量的电子传递链，是最高表达的HMT基因，这表明这些酶在这组的生理学中发挥着重要作用。我们的研究结果表明，异养成员的Thaumarchaeota是广泛分布在海洋中，并可能在全球化学transformation.IMPORTANCE发挥关键作用。多年来，人们一直知道，海洋Thaumarchaeota是丰富的组成部分，黑暗的海洋微生物群落，在那里他们的能力，耦合氨氧化和固碳起着至关重要的作用，在营养动态。在这项研究中，我们描述了一个丰富的组puperium异养海洋Thaumarchaeota（HMT）在海洋中的生理不同于他们的氨氧化亲属。HMT缺乏通过3-羟基丙酸/4-羟基丁酸途径氧化氨和固定碳的能力，而是编码一种III-a型RuBisCO和多种PQQ依赖性脱氢酶，这些酶可能用于在黑暗的海洋中保存能量。我们的工作扩大了海洋中Thaumarchaeota已知多样性的范围，并为广泛的海洋谱系提供了重要的见解。
The Thaumarchaeota is a diverse archaeal phylum comprising numerous lineages that play key roles in global biogeochemical cycling, particularly in the ocean. To date, all genomically characterized marine thaumarchaea are reported to be chemolithoautotrophic ammonia oxidizers. In this study, we report a group of putatively heterotrophic marine thaumarchaea (HMT) with small genome sizes that is globally abundant in the mesopelagic, apparently lacking the ability to oxidize ammonia. We assembled five HMT genomes from metagenomic data and show that they form a deeply branching sister lineage to the ammonia-oxidizing archaea (AOA). We identify this group in metagenomes from mesopelagic waters in all major ocean basins, with abundances reaching up to 6% of that of AOA. Surprisingly, we predict the HMT have small genomes of similar to 1 Mbp, and our ancestral state reconstruction indicates this lineage has undergone substantial genome reduction compared to other related archaea. The genomic repertoire of HMT indicates a versatile metabolism for aerobic chemoorganoheterotrophy that includes a divergent form III-a RuBisCO, a 2M respiratory complex I that has been hypothesized to increase energetic efficiency, and a three-subunit heme-copper oxidase complex IV that is absent from AOA. We also identify 21 pyrroloquinoline quinone (PQQ)-dependent dehydrogenases that are predicted to supply reducing equivalents to the electron transport chain and are among the most highly expressed HMT genes, suggesting these enzymes play an important role in the physiology of this group. Our results suggest that heterotrophic members of the Thaumarchaeota are widespread in the ocean and potentially play key roles in global chemical transformations.IMPORTANCE It has been known for many years that marine Thaumarchaeota are abundant constituents of dark ocean microbial communities, where their ability to couple ammonia oxidation and carbon fixation plays a critical role in nutrient dynamics. In this study, we describe an abundant group of putatively heterotrophic marine Thaumarchaeota (HMT) in the ocean with physiology distinct from those of their ammonia-oxidizing relatives. HMT lack the ability to oxidize ammonia and fix carbon via the 3-hydroxypropionate/4-hydroxybutyrate pathway but instead encode a form III-a RuBisCO and diverse PQQ-dependent dehydrogenases that are likely used to conserve energy in the dark ocean. Our work expands the scope of known diversity of Thaumarchaeota in the ocean and provides important insight into a widespread marine lineage.