Key Laboratory of Earth and Planetary Physics, Institute of Geology and Geophysics, Chinese Academy of Sciences, Beijing, 100029, China.
France-China Joint Laboratory for Evolution and Development of Magnetotactic Multicellular Organisms, Chinese Academy of Sciences, Beijing, 100029, China.
Microbiome. 2024 Aug 24;12(1):158. doi: 10.1186/s40168-024-01837-6.
Magnetotactic bacteria (MTB) are a unique group of microorganisms that sense and navigate through the geomagnetic field by biomineralizing magnetic nanoparticles. MTB from the phylum Nitrospirota (previously known as Nitrospirae) thrive in diverse aquatic ecosystems. They are of great interest due to their production of hundreds of magnetite (FeO) magnetosome nanoparticles per cell, which far exceeds that of other MTB. The morphological, phylogenetic, and genomic diversity of Nitrospirota MTB have been extensively studied. However, the metabolism and ecophysiology of Nitrospirota MTB are largely unknown due to the lack of cultivation techniques.
Here, we established a method to link the morphological, genomic, and metabolic investigations of an uncultured Nitrospirota MTB population (named LHC-1) at the single-cell level using nanoscale secondary-ion mass spectrometry (NanoSIMS) in combination with rRNA-based in situ hybridization and target-specific mini-metagenomics.
We magnetically separated LHC-1 from a freshwater lake and reconstructed the draft genome of LHC-1 using genome-resolved mini-metagenomics. We found that 10 LHC-1 cells were sufficient as a template to obtain a high-quality draft genome. Genomic analysis revealed that LHC-1 has the potential for CO fixation and NO reduction, which was further characterized at the single-cell level by combining stable-isotope incubations and NanoSIMS analyses over time. Additionally, the NanoSIMS results revealed specific element distributions in LHC-1, and that the heterogeneity of CO and NO metabolisms among different LHC-1 cells increased with incubation time.
To our knowledge, this study provides the first metabolic measurements of individual Nitrospirota MTB cells to decipher their ecophysiological traits. The procedure constructed in this study provides a promising strategy to simultaneously investigate the morphology, genome, and ecophysiology of uncultured microbes in natural environments. Video Abstract.
磁细菌（MTB）是一组独特的微生物，它们通过生物矿化磁性纳米颗粒来感知和导航地磁场。来自硝化螺旋菌门（以前称为硝化螺旋体）的 MTB 在各种水生生态系统中茁壮成长。它们之所以受到关注，是因为它们每细胞可产生数百个磁铁矿（FeO）磁小体纳米颗粒，这远远超过其他 MTB。硝化螺旋菌 MTB 的形态、系统发育和基因组多样性已经得到了广泛的研究。然而，由于缺乏培养技术，硝化螺旋菌 MTB 的代谢和生态生理学在很大程度上仍是未知的。
在这里，我们建立了一种方法，通过纳米二次离子质谱（NanoSIMS）结合 rRNA 原位杂交和靶向特异性 mini 宏基因组学，在单细胞水平上对未培养的硝化螺旋菌 MTB 种群（命名为 LHC-1）进行形态、基因组和代谢研究。
我们从一个淡水湖中磁性分离出 LHC-1，并使用基因组解析的 mini 宏基因组学重建了 LHC-1 的草图基因组。我们发现，10 个 LHC-1 细胞足以作为模板获得高质量的草图基因组。基因组分析表明，LHC-1 具有 CO 固定和 NO 还原的潜力，这在单细胞水平上通过结合稳定同位素孵育和随时间进行的 NanoSIMS 分析进一步得到了表征。此外，NanoSIMS 结果揭示了 LHC-1 中特定元素的分布，并且不同 LHC-1 细胞之间 CO 和 NO 代谢的异质性随着孵育时间的增加而增加。
据我们所知，这项研究首次对单个硝化螺旋菌 MTB 细胞进行了代谢测量，以破译它们的生态生理学特征。本研究构建的方法为同时研究自然环境中未培养微生物的形态、基因组和生态生理学提供了一种有前途的策略。视频摘要。
