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Genome-centric resolution of novel microbial lineages in an excavated Centrosaurus dinosaur fossil bone from the Late Cretaceous of North America
Environmental Microbiome ( IF 6.2 ) Pub Date : 2020-03-19 , DOI: 10.1186/s40793-020-00355-w
Renxing Liang , Maggie C. Y. Lau , Evan T. Saitta , Zachary K. Garvin , Tullis C. Onstott

Exceptional preservation of endogenous organics such as collagens and blood vessels has been frequently reported in Mesozoic dinosaur fossils. The persistence of these soft tissues in Mesozoic fossil bones has been challenged because of the susceptibility of proteins to degradation and because bone porosity allows microorganisms to colonize the inner microenvironments through geological time. Although protein lability has been studied extensively, the genomic diversity of microbiomes in dinosaur fossil bones and their potential roles in bone taphonomy remain underexplored. Genome-resolved metagenomics was performed, therefore, on the microbiomes recovered from a Late Cretaceous Centrosaurus bone and its encompassing mudstone in order to provide insight into the genomic potential for microbial alteration of fossil bone. Co-assembly and binning of metagenomic reads resulted in a total of 46 high-quality metagenome-assembled genomes (MAGs) affiliated to six bacterial phyla (Actinobacteria, Proteobacteria, Nitrospira, Acidobacteria, Gemmatimonadetes and Chloroflexi) and 1 archaeal phylum (Thaumarchaeota). The majority of the MAGs represented uncultivated, novel microbial lineages from class to species levels based on phylogenetics, phylogenomics and average amino acid identity. Several MAGs from the classes Nitriliruptoria, Deltaproteobacteria and Betaproteobacteria were highly enriched in the bone relative to the adjacent mudstone. Annotation of the MAGs revealed that the distinct putative metabolic functions of different taxonomic groups were linked to carbon, nitrogen, sulfur and iron metabolism. Metaproteomics revealed gene expression from many of the MAGs, but no endogenous collagen peptides were identified in the bone that could have been derived from the dinosaur. Estimated in situ replication rates among the bacterial MAGs suggested that most of the microbial populations in the bone might have been actively growing but at a slow rate. Our results indicate that excavated dinosaur bones are habitats for microorganisms including novel microbial lineages. The distinctive microhabitats and geochemistry of fossil bone interiors compared to that of the external sediment enrich a microbial biomass comprised of various novel taxa that harbor multiple gene sets related to interconnected biogeochemical processes. Therefore, the presence of these microbiomes in Mesozoic dinosaur fossils urges extra caution to be taken in the science of paleontology when hunting for endogenous biomolecules preserved from deep time.

中文翻译:

北美白垩纪晚期出土的迅龙恐龙化石骨骼中新型微生物谱系的基因组中心解析

中生代恐龙化石中经常报告内源性有机物(如胶原蛋白和血管)的特殊保存。这些软组织在中生代化石骨骼中的持久性受到了挑战,这是因为蛋白质易于降解,并且骨骼的孔隙度允许微生物在整个地质时间内定居在内部微环境中。尽管对蛋白质的不稳定性已进行了广泛的研究,但恐龙化石骨骼中微生物群的基因组多样性及其在骨拓扑学中的潜在作用仍未得到充分研究。因此,对从白垩纪晚骨骨及其周围的泥岩中回收的微生物群进行了基因组分辨的宏基因组学研究,以提供对化石骨微生物改变的基因组潜力的见解。宏基因组读取的共同组装和分档产生了总共46个高质量的基因组组装基因组(MAGs),与6个细菌门(放线菌,变形杆菌,硝化螺旋菌,酸性细菌,芽孢杆菌和叶绿藻)和1个古细菌门(Thaumarchaeota)相关。多数MAG代表了从无到有的新型微生物谱系,从种系到物种水平都基于系统发育,系统发育组学和平均氨基酸同一性。相对于邻近的泥岩,来自硝化细菌,变形杆菌和β变形细菌类的几种MAG在骨骼中高度富集。MAG的注释显示,不同分类组的独特的假定代谢功能与碳,氮,硫和铁的代谢有关。元蛋白质组学揭示了许多MAG的基因表达,但在骨骼中未​​发现可能源自恐龙的内源性胶原蛋白肽。细菌MAG之间的原位复制速率估计表明,骨骼中的大多数微生物种群可能一直在活跃地生长,但速度缓慢。我们的结果表明,挖掘出的恐龙骨骼是包括新微生物谱系在内的微生物的栖息地。与外部沉积物相比,化石骨骼内部独特的微生境和地球化学丰富了由各种新型生物分类组成的微生物生物量,这些生物分类具有与相互联系的生物地球化学过程有关的多个基因集。因此,
更新日期:2020-03-19
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