Predominance of Anaerobic, Spore-Forming Bacteria in Metabolically Active Microbial Communities from Ancient Siberian Permafrost

Predominance of Anaerobic, Spore-Forming Bacteria in Metabolically Active Microbial Communities from Ancient Siberian Permafrost
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DOI:
10.1128/aem.00560-19
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发表时间:
2019-08-01
影响因子:
4.4
通讯作者:
Onstott, Tullis C.
Onstott, Tullis C.
中科院分区:
生物学2区
文献类型:
--
作者:
Liang, Renxing;Lau, Maggie;Onstott, Tullis C.

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多年冻土中微生物生命的普遍存在已有数百万年(Ma)的历史,已有充分记录。然而,埋藏微生物在这段时间内的长期生存能力、进化和代谢活动仍未得到充分探索。我们将天冬氨酸 (Asp) 外消旋化测定与宏基因组测序相结合,以表征西伯利亚东北部连续冰冻永久冻土的类似于 0.01 至 1.1 Ma 时间序列的本土微生物群落的微生物活性、系统发育多样性和代谢功能。尽管较老的沉积物(0.8 至 1.1 Ma)中的天冬氨酸相对于最年轻的沉积物(类似于 0.01 Ma)中的天冬氨酸经历了严重的外消旋作用,但从所有样品中分离出的细胞中 D-天冬氨酸/L-天冬氨酸的比率(0.05 至 0.14)要低得多,这表明本土微生物群落在 1.1 Ma 的古代永久冻土中仍然存活且代谢活跃。最年轻的沉积物中的微生物群落最为多样化,以放线菌门和变形菌门为主。相比之下,较古老的沉积物中的微生物多样性急剧下降,厚壁菌门内的厌氧、孢子形成细菌成为压倒性的优势。除了与孢子形成相关的基因富集之外,参与厌氧代谢途径(例如发酵、硫酸盐还原和产甲烷)的功能基因在较老的沉积物中也更加丰富。总而言之,较旧沉积物中孢子形成细菌和相关厌氧代谢的优势表明,在地质时期内,被困在永久冻土中的原始本土微生物群落的一个子集在埋藏过程中幸存下来。 重要性 了解数百万年前冻结的古代永久冻土中微生物的长期生存能力和相关代谢特征,为了解埋藏和保存提供了一个独特的窗口 由于永久冻土的水文隔离和特殊的 DNA 保存,沉积物中的地下微生物通常经历的过程。我们采用天冬氨酸外消旋模型和宏基因组学来确定西伯利亚东北部 1.1 Ma 永久冻土中哪些微生物群落具有代谢活性。细胞外和细胞内基因组 DNA 的同步测序提供了对这段时间内在冷冻条件下区分已灭绝微生物和现存微生物的代谢潜力的深入了解。这种深入的宏基因组测序增进了我们对早期更新世永久冻土层现存微生物群的微生物多样性和代谢功能的理解。因此,这些发现将我们对永久冻土中微生物生存能力的认识从 33,000 年延伸到了 1.1 Ma。
The prevalence of microbial life in permafrost up to several million years (Ma) old has been well documented. However, the long-term survivability, evolution, and metabolic activity of the entombed microbes over this time span remain underexplored. We integrated aspartic acid (Asp) racemization assays with metagenomic sequencing to characterize the microbial activity, phylogenetic diversity, and metabolic functions of indigenous microbial communities across a similar to 0.01-to 1.1-Ma chronosequence of continuously frozen permafrost from northeastern Siberia. Although Asp in the older bulk sediments (0.8 to 1.1 Ma) underwent severe racemization relative to that in the youngest sediment (similar to 0.01 Ma), the much lower D-Asp/L-Asp ratio (0.05 to 0.14) in the separated cells from all samples suggested that indigenous microbial communities were viable and metabolically active in ancient permafrost up to 1.1 Ma. The microbial community in the youngest sediment was the most diverse and was dominated by the phyla Actinobacteria and Proteobacteria. In contrast, microbial diversity decreased dramatically in the older sediments, and anaerobic, spore-forming bacteria within Firmicutes became overwhelmingly dominant. In addition to the enrichment of sporulation-related genes, functional genes involved in anaerobic metabolic pathways such as fermentation, sulfate reduction, and methanogenesis were more abundant in the older sediments. Taken together, the predominance of spore-forming bacteria and associated anaerobic metabolism in the older sediments suggest that a subset of the original indigenous microbial community entrapped in the permafrost survived burial over geological time.IMPORTANCE Understanding the long-term survivability and associated metabolic traits of microorganisms in ancient permafrost frozen millions of years ago provides a unique window into the burial and preservation processes experienced in general by subsurface microorganisms in sedimentary deposits because of permafrost's hydrological isolation and exceptional DNA preservation. We employed aspartic acid racemization modeling and metagenomics to determine which microbial communities were metabolically active in the 1.1-Ma permafrost from northeastern Siberia. The simultaneous sequencing of extracellular and intracellular genomic DNA provided insight into the metabolic potential distinguishing extinct from extant microorganisms under frozen conditions over this time interval. This in-depth metagenomic sequencing advances our understanding of the microbial diversity and metabolic functions of extant microbiomes from early Pleistocene permafrost. Therefore, these findings extend our knowledge of the survivability of microbes in permafrost from 33,000 years to 1.1 Ma.