Department of Earth and Planetary Science, The University of Tokyo, Bunkyo-ku, Tokyo, Japan.
Japan Collection of Microorganisms (JCM), RIKEN BioResource Research Center, Tsukuba, Ibaraki, Japan.
ISME J. 2024 Jan 8;18(1). doi: 10.1093/ismejo/wrae207.
Recent successes in the cultivation of DPANN archaea with their hosts have demonstrated an episymbiotic lifestyle, whereas the lifestyle of DPANN archaea in natural habitats is largely unknown. A free-living lifestyle is speculated in oxygen-deprived fluids circulated through rock media, where apparent hosts of DPANN archaea are lacking. Alternatively, DPANN archaea may be detached from their hosts and/or rock surfaces. To understand the ecology of rock-hosted DPANN archaea, rocks rather than fluids should be directly characterized. Here, we investigated a deep-sea hydrothermal vent chimney without fluid venting where our previous study revealed the high proportion of Pacearchaeota, one of the widespread and enigmatic lineages of DPANN archaea. Using spectroscopic methods with submicron soft X-ray and infrared beams, the microbial habitat was specified to be silica-filled pores in the inner chimney wall comprising chalcopyrite. Metagenomic analysis of the inner wall revealed the lack of biosynthetic genes for nucleotides, amino acids, cofactors, and lipids in the Pacearchaeota genomes. Genome-resolved metaproteomic analysis clarified the co-occurrence of a novel thermophilic lineage actively fixing carbon and nitrogen and thermophilic archaea in the inner chimney wall. We infer that the shift in metabolically active microbial populations from the thermophiles to the mesophilic DPANN archaea occurs after the termination of fluid venting. The infilling of mineral pores by hydrothermal silica deposition might be a preferred environmental factor for the colonization of free-living Pacearchaeota with ultrasmall cells depending on metabolites synthesized by the co-occurring thermophiles during fluid venting.
最近，在培养与 DPANN 古菌共生的宿主方面取得了成功，这证明了它们具有共生生活方式，而 DPANN 古菌在自然栖息地的生活方式在很大程度上是未知的。在缺氧的流体循环通过岩石介质中，推测存在自由生活方式，而 DPANN 古菌的明显宿主却缺乏。或者，DPANN 古菌可能与它们的宿主和/或岩石表面分离。为了了解岩石栖息的 DPANN 古菌的生态学，应该直接对岩石进行描述，而不是对流体进行描述。在这里，我们研究了一个没有流体排放的深海热液喷口烟囱，在我们之前的研究中，该烟囱揭示了 Pacearchaeota 的高比例，Pacearchaeota 是 DPANN 古菌广泛而神秘的谱系之一。使用具有亚微米软 X 射线和红外光束的光谱方法，将微生物栖息地指定为含有黄铜矿的内部烟囱壁的充满硅的孔隙。内壁的宏基因组分析表明，Pacearchaeota 基因组中缺乏核苷酸、氨基酸、辅因子和脂质的生物合成基因。基于基因组的宏蛋白质组学分析阐明了一种新型嗜热谱系与嗜热古菌在内部烟囱壁中共同固定碳和氮的情况。我们推断，在流体排放停止后，从嗜热菌到代谢活跃的中温 DPANN 古菌的代谢活跃微生物种群发生了转变。热液二氧化硅的沉淀会填充矿物孔隙，这可能是依赖于在流体排放期间共生嗜热菌合成的代谢物的超小细胞自由生活的 Pacearchaeota 定植的首选环境因素。
