Mondini Antonio, Anwar Muhammad Zohaib, Ellegaard-Jensen Lea, Lavin Paris, Jacobsen Carsten Suhr, Purcarea Cristina
Department of Microbiology, Institute of Biology, Bucharest, Romania.
Department of Environmental Science, Aarhus University, RISØ Campus, Roskilde, Denmark.
Front Microbiol. 2022 Mar 10;12:809076. doi: 10.3389/fmicb.2021.809076. eCollection 2021.
Ice caves constitute the newly investigated frozen and secluded model habitats for evaluating the resilience of ice-entrapped microbiomes in response to climate changes. This survey identified the total and active prokaryotic and eukaryotic communities from millennium-old ice accumulated in Scarisoara cave (Romania) using Illumina shotgun sequencing of the ribosomal RNA (rRNA) and messenger RNA (mRNA)-based functional analysis of the metatranscriptome. Also, the response of active microbiome to heat shock treatment mimicking the environmental shift during ice melting was evaluated at both the taxonomic and metabolic levels. The putatively active microbial community was dominated by bacterial taxa belonging to Proteobacteria and Bacteroidetes, which are highly resilient to thermal variations, while the scarcely present archaea belonging to Methanomicrobia was majorly affected by heat shock. Among eukaryotes, the fungal rRNA community was shared between the resilient Chytridiomycota and Blastocladiomycota, and the more sensitive Ascomycota and Basidiomycota taxa. A complex microeukaryotic community highly represented by Tardigrada and Rotifera (Metazoa), Ciliophora and Cercozoa (Protozoa), and Chlorophyta (Plantae) was evidenced for the first time in this habitat. This community showed a quick reaction to heat shock, followed by a partial recovery after prolonged incubation at 4°C due to possible predation processes on the prokaryotic cluster. Analysis of mRNA differential gene expression revealed the presence of an active microbiome in the perennial ice from the Scarisoara cave and associated molecular mechanisms for coping with temperature variations by the upregulation of genes involved in enzyme recovery, energy storage, carbon and nitrogen regulation, and cell motility. This first report on the active microbiome embedded in perennial ice from caves and its response to temperature stress provided a glimpse into the impact of glaciers melting and the resilience mechanisms in this habitat, contributing to the knowledge on the functional role of active microbes in frozen environments and their response to climatic changes.
冰洞是新发现的冷冻且与世隔绝的典型栖息地，用于评估被困于冰中的微生物群落对气候变化的恢复力。本调查通过对核糖体RNA（rRNA）进行Illumina鸟枪法测序以及基于信使RNA（mRNA）的宏转录组功能分析，确定了罗马尼亚斯卡里索拉洞穴中积累的千年老冰中的原核生物和真核生物群落总量及活性。此外，还在分类学和代谢水平上评估了活性微生物群落对模拟冰融化过程中环境变化的热休克处理的反应。假定的活性微生物群落主要由属于变形菌门和拟杆菌门的细菌类群主导，它们对温度变化具有高度恢复力，而属于甲烷微菌纲的稀少古菌则主要受到热休克的影响。在真核生物中，真菌rRNA群落存在于恢复力较强的壶菌门和芽枝霉门以及较敏感的子囊菌门和担子菌门分类群之间。首次在该栖息地证实了一个复杂的微型真核生物群落，其中缓步动物门和轮虫纲（后生动物）、纤毛虫纲和丝足虫纲（原生动物）以及绿藻门（植物）占主导地位。该群落对热休克反应迅速，由于可能对原核生物集群的捕食过程，在4°C下长时间孵育后部分恢复。对mRNA差异基因表达的分析表明，斯卡里索拉洞穴的常年冰中存在活性微生物群落，以及通过上调参与酶恢复、能量储存、碳和氮调节以及细胞运动的基因来应对温度变化的相关分子机制。这份关于洞穴常年冰中活性微生物群落及其对温度胁迫反应的首次报告，让人得以一窥冰川融化的影响以及该栖息地的恢复机制，有助于了解活性微生物在冰冻环境中的功能作用及其对气候变化的反应。
