Japan Collection of Microorganisms (JCM), RIKEN BioResource Research Center, Tsukuba, Ibaraki, Japan.
Graduate School of Science, Osaka Metropolitan University, Osaka, Japan.
J Bacteriol. 2024 Feb 22;206(2):e0035123. doi: 10.1128/jb.00351-23. Epub 2024 Jan 30.
The DPANN archaeal clade includes obligately ectosymbiotic species. Their cell surfaces potentially play an important role in the symbiotic interaction between the ectosymbionts and their hosts. However, little is known about the mechanism of ectosymbiosis. Here, we show cell surface structures of the cultivated DPANN archaeon strain MJ1 and its host strain MJ1HA, using a variety of electron microscopy techniques, i.e., negative-staining transmission electron microscopy, quick-freeze deep-etch TEM, and 3D electron tomography. The thickness, unit size, and lattice symmetry of the S-layer of strain MJ1 were different from those of the host archaeon strain MJ1HA. Genomic and transcriptomic analyses highlighted the most highly expressed MJ1 gene for a putative S-layer protein with multiple glycosylation sites and immunoglobulin-like folds, which has no sequence homology to known S-layer proteins. In addition, genes for putative pectin lyase- or lectin-like extracellular proteins, which are potentially involved in symbiotic interaction, were found in the MJ1T genome based on 3D protein structure prediction. Live cell imaging at the optimum growth temperature of 65°C indicated that cell complexes of strains MJ1 and MJ1HA were motile, but sole MJ1 cells were not. Taken together, we propose a model of the symbiotic interaction and cell cycle of .IMPORTANCEDPANN archaea are widely distributed in a variety of natural and artificial environments and may play a considerable role in the microbial ecosystem. All of the cultivated DPANN archaea so far need host organisms for their growth, i.e., obligately ectosymbiotic. However, the mechanism of the ectosymbiosis by DPANN archaea is largely unknown. To this end, we performed a comprehensive analysis of the cultivated DPANN archaeon, , using electron microscopy, live cell imaging, transcriptomics, and genomics, including 3D protein structure prediction. Based on the results, we propose a reasonable model of the symbiotic interaction and cell cycle of , which will enhance our understanding of the enigmatic physiology and ecological significance of DPANN archaea.
DPANN 古菌包括专性外共生种。它们的细胞表面可能在共生体与其宿主之间的共生相互作用中发挥重要作用。然而，对于外共生的机制知之甚少。在这里，我们使用各种电子显微镜技术，即负染色透射电子显微镜、快速冷冻深蚀刻 TEM 和 3D 电子断层扫描，展示了培养的 DPANN 古菌 菌株 MJ1 及其宿主 菌株 MJ1HA 的细胞表面结构。菌株 MJ1 的 S 层的厚度、单位大小和晶格对称性与宿主古菌菌株 MJ1HA 不同。基因组和转录组分析突出了最具表达能力的 MJ1 基因，该基因编码一种具有多个糖基化位点和免疫球蛋白样折叠的假定 S 层蛋白，与已知的 S 层蛋白没有序列同源性。此外，根据 3D 蛋白质结构预测，在 MJ1T 基因组中发现了潜在参与共生相互作用的假定果胶裂解酶或凝集素样细胞外蛋白的基因。在最适生长温度 65°C 的活细胞成像表明，菌株 MJ1 和 MJ1HA 的细胞复合物是运动的，但单独的 MJ1 细胞不是。综上所述，我们提出了一种共生相互作用和细胞周期的模型。
重要性 DPANN 古菌广泛分布于各种自然和人工环境中，可能在微生物生态系统中发挥重要作用。迄今为止，所有培养的 DPANN 古菌都需要宿主生物来生长，即专性外共生。然而，DPANN 古菌的外共生机制在很大程度上是未知的。为此，我们使用电子显微镜、活细胞成像、转录组学和基因组学，包括 3D 蛋白质结构预测，对培养的 DPANN 古菌 进行了全面分析。基于这些结果，我们提出了一个合理的共生相互作用和细胞周期模型，这将增强我们对 DPANN 古菌神秘生理学和生态意义的理解。
