Genome-centric resolution of novel microbial lineages in an excavated Centrosaurus dinosaur fossil bone from the Late Cretaceous of North America
Abstract Background 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 degradati...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2020-03-01
|
| Series: | Environmental Microbiome |
| Subjects: | |
| Online Access: | http://link.springer.com/article/10.1186/s40793-020-00355-w |
| _version_ | 1818986623305515008 |
|---|---|
| author | Renxing Liang Maggie C. Y. Lau Evan T. Saitta Zachary K. Garvin Tullis C. Onstott |
| author_facet | Renxing Liang Maggie C. Y. Lau Evan T. Saitta Zachary K. Garvin Tullis C. Onstott |
| author_sort | Renxing Liang |
| collection | DOAJ |
| description | Abstract Background 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. Results 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. Conclusions 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. |
| first_indexed | 2024-12-20T18:53:44Z |
| format | Article |
| id | doaj.art-db20ec54caac437ba6b8fc0980c9df58 |
| institution | Directory Open Access Journal |
| issn | 2524-6372 |
| language | English |
| last_indexed | 2024-12-20T18:53:44Z |
| publishDate | 2020-03-01 |
| publisher | BMC |
| record_format | Article |
| series | Environmental Microbiome |
| spelling | doaj.art-db20ec54caac437ba6b8fc0980c9df582022-12-21T19:29:34ZengBMCEnvironmental Microbiome2524-63722020-03-0115111810.1186/s40793-020-00355-wGenome-centric resolution of novel microbial lineages in an excavated Centrosaurus dinosaur fossil bone from the Late Cretaceous of North AmericaRenxing Liang0Maggie C. Y. Lau1Evan T. Saitta2Zachary K. Garvin3Tullis C. Onstott4Department of Geosciences, Princeton UniversityDepartment of Geosciences, Princeton UniversityIntegrative Research Center, Section of Earth Sciences, Field Museum of Natural HistoryDepartment of Geosciences, Princeton UniversityDepartment of Geosciences, Princeton UniversityAbstract Background 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. Results 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. Conclusions 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.http://link.springer.com/article/10.1186/s40793-020-00355-wCentrosaurus fossil boneDiagenesisRare ActinobacteriaHalotolerant bacteriaLate CretaceousUncultured microbial lineages |
| spellingShingle | Renxing Liang Maggie C. Y. Lau Evan T. Saitta Zachary K. Garvin Tullis C. Onstott Genome-centric resolution of novel microbial lineages in an excavated Centrosaurus dinosaur fossil bone from the Late Cretaceous of North America Environmental Microbiome Centrosaurus fossil bone Diagenesis Rare Actinobacteria Halotolerant bacteria Late Cretaceous Uncultured microbial lineages |
| title | Genome-centric resolution of novel microbial lineages in an excavated Centrosaurus dinosaur fossil bone from the Late Cretaceous of North America |
| title_full | Genome-centric resolution of novel microbial lineages in an excavated Centrosaurus dinosaur fossil bone from the Late Cretaceous of North America |
| title_fullStr | Genome-centric resolution of novel microbial lineages in an excavated Centrosaurus dinosaur fossil bone from the Late Cretaceous of North America |
| title_full_unstemmed | Genome-centric resolution of novel microbial lineages in an excavated Centrosaurus dinosaur fossil bone from the Late Cretaceous of North America |
| title_short | Genome-centric resolution of novel microbial lineages in an excavated Centrosaurus dinosaur fossil bone from the Late Cretaceous of North America |
| title_sort | genome centric resolution of novel microbial lineages in an excavated centrosaurus dinosaur fossil bone from the late cretaceous of north america |
| topic | Centrosaurus fossil bone Diagenesis Rare Actinobacteria Halotolerant bacteria Late Cretaceous Uncultured microbial lineages |
| url | http://link.springer.com/article/10.1186/s40793-020-00355-w |
| work_keys_str_mv | AT renxingliang genomecentricresolutionofnovelmicrobiallineagesinanexcavatedcentrosaurusdinosaurfossilbonefromthelatecretaceousofnorthamerica AT maggiecylau genomecentricresolutionofnovelmicrobiallineagesinanexcavatedcentrosaurusdinosaurfossilbonefromthelatecretaceousofnorthamerica AT evantsaitta genomecentricresolutionofnovelmicrobiallineagesinanexcavatedcentrosaurusdinosaurfossilbonefromthelatecretaceousofnorthamerica AT zacharykgarvin genomecentricresolutionofnovelmicrobiallineagesinanexcavatedcentrosaurusdinosaurfossilbonefromthelatecretaceousofnorthamerica AT tullisconstott genomecentricresolutionofnovelmicrobiallineagesinanexcavatedcentrosaurusdinosaurfossilbonefromthelatecretaceousofnorthamerica |