Glaciers represent a unique inventory of microbial genetic diversity and a record of evolution. The Tibetan Plateau contains the largest area of low-latitude glaciers and is particularly vulnerable to global warming. By sequencing 85 metagenomes and 883 cultured isolates from 21 Tibetan glaciers covering snow, ice and cryoconite habitats, we present a specialized glacier microbial genome and gene catalog to archive glacial genomic and functional diversity. This comprehensive Tibetan Glacier Genome and Gene (TG2G) catalog includes 883 genomes and 2,358 metagenome-assembled genomes, which represent 968 candidate species spanning 30 phyla. The catalog also contains over 25 million non-redundant protein-encoding genes, the utility of which is demonstrated by the exploration of secondary metabolite biosynthetic potentials, virulence factor identification and global glacier metagenome comparison. The TG2G catalog is a valuable resource that enables enhanced understanding of the structure and functions of Tibetan glacial microbiomes.
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The TG2G catalog is organized in three levels: Assembled contigs, Genes and Genomes (Supplementary Fig. 9). The assembled contig section contains the sequence of non-redundant contigs and the coverage of each contig across all samples; the gene section contains the sequences of non-redundant ORFs, the coverage of each gene across all samples and the annotation of all genes using eggNOG, CARD, CAZy, COG, VFDB and KEGG; and the genome section contains the genomes quality assessment file, taxonomic classification, the representative genomes of OTUs and their coverage across all samples, as well as the annotation of genes against the same databases as the gene section of the catalog. The catalog in the structure described is available at the National Omics Data Encyclopedia under project ID OEP003083. Raw reads are also deposited in the NCBI under the project Tibetan Glacier Genome and Gene Catalogue (PRJNA813429) with SRA numbers SRR18576994–SRR18577078 (ref. 69). Additional global glacier metagenomes were downloaded from the NCBI under project IDs PRJNA445613, PRJNA360211, PRJEB12327 and PRJNA283341. The supplementary table file is available at https://doi.org/10.6084/m9.figshare.19766653.
Zawierucha, K. & Shain, D. H. Disappearing Kilimanjaro snow—are we the last generation to explore equatorial glacier biodiversity? Ecol. Evol. 9, 8911–8918 (2019).
Hodson, A. et al. Glacial ecosystems. Ecol. Monogr. 78, 41–67 (2008).
Anesio, A. M., Lutz, S., Chrismas, N. A. M. & Benning, L. G. The microbiome of glaciers and ice sheets. NPJ Biofilms Microbiomes 3, 10 (2017).
Stibal, M., Sabacka, M. & Zarsky, J. Biological processes on glacier and ice sheet surfaces. Nat. Geosci. 5, 771–774 (2012).
Pittino, F. et al. Bacterial communities of cryoconite holes of a temperate alpine glacier show both seasonal trends and year-to-year variability. Ann. Glaciol. 59, 1–9 (2018).
Boetius, A., Anesio, A. M., Deming, J. W., Mikucki, J. A. & Rapp, J. Z. Microbial ecology of the cryosphere: sea ice and glacial habitats. Nat. Rev. Microbiol. 13, 677–690 (2015).
Yarzábal, L. A., Salazar, L. M. B. & Batista-García, R. A. Climate change, melting cryosphere and frozen pathogens: should we worry…? Environ. Sustain. 4, 489–501 (2021).
Knowlton, C., Veerapaneni, R., D’Elia, T. & Rogers, S. O. Microbial analyses of ancient ice core sections from greenland and antarctica. Biology 2, 206–232 (2013).
Miteva, V. I. & Brenchley, J. E. Detection and isolation of ultrasmall microorganisms from a 120,000-year-old Greenland glacier ice core. Appl. Environ. Microbiol. 71, 7806–7818 (2005).
Ma, L.-J., Rogers, S. O., Catranis, C. M. & Starmer, W. T. Detection and characterization of ancient fungi entrapped in glacial ice. Mycologia 92, 286–295 (2000).
Christner, B. C., Mosley-Thompson, E., Thompson, L. G. & Reeve, J. N. Bacterial recovery from ancient glacial ice. Environ. Microbiol. 5, 433–436 (2003).
Santibanez, P. A. et al. Prokaryotes in the WAIS Divide ice core reflect source and transport changes between Last Glacial Maximum and the early Holocene. Glob. Chang. Biol. 24, 2182–2197 (2018).
Yao, T. et al. Different glacier status with atmospheric circulations in Tibetan Plateau and surroundings. Nat. Clim. Chang. 2, 663–667 (2012).
Bibi, S. et al. Climatic and associated cryospheric, biospheric, and hydrological changes on the Tibetan Plateau: a review. Int. J. Climatol. 38, e1–e17 (2018).
Cauvy-Fraunié, S. & Dangles, O. A global synthesis of biodiversity responses to glacier retreat. Nat. Ecol. Evol. 3, 1675–1685 (2019).
Stibal, M. et al. Glacial ecosystems are essential to understanding biodiversity responses to glacier retreat. Nat. Ecol. Evol. 4, 686–687 (2020).
Souney, J. M. et al. Core handling, transportation and processing for the South Pole ice core (SPICEcore) project. Ann. Glaciol. 62, 118–130 (2021).
Nayfach, S. et al. A genomic catalog of Earth’s microbiomes. Nat. Biotechnol. 39, 499–509 (2021).
Mogrovejo-Arias, D. C., Brill, F. H. H. & Wagner, D. Potentially pathogenic bacteria isolated from diverse habitats in Spitsbergen, Svalbard. Environ. Earth Sci. 79, 109 (2020).
Abedon, S. T. & Lejeune, J. T. Why bacteriophage encode exotoxins and other virulence factors. Evol. Bioinform. Online 1, 97–110 (2007).
Casacuberta, E. & Gonzalez, J. The impact of transposable elements in environmental adaptation. Mol. Ecol. 22, 1503–1517 (2013).
Soucy, S. M., Huang, J. & Gogarten, J. P. Horizontal gene transfer: building the web of life. Nat. Rev. Genet. 16, 472–482 (2015).
Bowers, R. M. et al. Minimum information about a single amplified genome (MISAG) and a metagenome-assembled genome (MIMAG) of bacteria and archaea. Nat. Biotechnol. 35, 725–731 (2017).
Cao, S. et al. Structure and function of the Arctic and Antarctic marine microbiota as revealed by metagenomics. Microbiome 8, 47 (2020).
Royo-Llonch, M. et al. Compendium of 530 metagenome-assembled bacterial and archaeal genomes from the polar Arctic Ocean. Nat. Microbiol. 6, 1561–1574 (2021).
Chaumeil, P. A., Mussig, A. J., Hugenholtz, P. & Parks, D. H. GTDB-Tk: a toolkit to classify genomes with the Genome Taxonomy Database. Bioinformatics 36, 1925–1927 (2019).
Benaud, N. et al. Harnessing long-read amplicon sequencing to uncover NRPS and type I PKS gene sequence diversity in polar desert soils. FEMS Microbiol. Ecol. 95, fiz031 (2019).
Kautsar, S. A. et al. MIBiG 2.0: a repository for biosynthetic gene clusters of known function. Nucleic Acids Res. 48, D454–D458 (2019).
Vila, E., Hornero-Méndez, D., Azziz, G., Lareo, C. & Saravia, V. Carotenoids from heterotrophic bacteria isolated from Fildes Peninsula, King George Island, Antarctica. Biotechnol. Rep. (Amst). 21, e00306 (2019).
Moeller, R., Horneck, G., Facius, R. & Stackebrandt, E. Role of pigmentation in protecting Bacillus sp. endospores against environmental UV radiation. FEMS Microbiol. Ecol. 51, 231–236 (2005).
Nupur, L. N. U. et al. ProCarDB: a database of bacterial carotenoids. BMC Microbiol. 16, 96–96 (2016).
Anesio, A. M. & Laybourn-Parry, J. Glaciers and ice sheets as a biome. Trends Ecol. Evol. 27, 219–225 (2012).
Feller, G. Life at low temperatures: is disorder the driving force? Extremophiles 11, 211–216 (2007).
Houwenhuyse, S., Macke, E., Reyserhove, L., Bulteel, L. & Decaestecker, E. Back to the future in a petri dish: origin and impact of resurrected microbes in natural populations. Evol. Appl. 11, 29–41 (2017).
Bankevich, A. et al. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455–477 (2012).
Li, D., Liu, C. M., Luo, R., Sadakane, K. & Lam, T. W. MEGAHIT: an ultra-fast single-node solution for large and complex metagenomics assembly via succinct de Bruijn graph. Bioinformatics 31, 1674–1676 (2015).
Langmead, B. & Salzberg, S. L. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357–359 (2012).
Buchfink, B., Reuter, K. & Drost, H. G. Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat. Methods 18, 366–368 (2021).
Kang, D. D. et al. MetaBAT 2: an adaptive binning algorithm for robust and efficient genome reconstruction from metagenome assemblies. PeerJ 7, e7359 (2019).
Wu, Y. W., Simmons, B. A. & Singer, S. W. MaxBin 2.0: an automated binning algorithm to recover genomes from multiple metagenomic datasets. Bioinformatics 32, 605–607 (2016).
Nissen, J. N. et al. Improved metagenome binning and assembly using deep variational autoencoders. Nat. Biotechnol. 39, 555–560 (2021).
Parks, D. H. et al. Recovery of nearly 8,000 metagenome-assembled genomes substantially expands the tree of life. Nat. Microbiol. 2, 1533–1542 (2017).
Parks, D. H., Imelfort, M., Skennerton, C. T., Hugenholtz, P. & Tyson, G. W. CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes. Genome Res. 25, 1043–1055 (2015).
Lowe, T. M. & Eddy, S. R. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25, 955–964 (1997).
Nawrocki, E. P., Kolbe, D. L. & Eddy, S. R. Infernal 1.0: inference of RNA alignments. Bioinformatics 25, 1335–1337 (2009).
Kalvari, I. et al. Rfam 13.0: shifting to a genome-centric resource for non-coding RNA families. Nucleic Acids Res. 46, D335–d342 (2018).
Olm, M. R., Brown, C. T., Brooks, B. & Banfield, J. F. dRep: a tool for fast and accurate genomic comparisons that enables improved genome recovery from metagenomes through de-replication. ISME J. 11, 2864–2868 (2017).
Almeida, A. et al. A unified catalog of 204,938 reference genomes from the human gut microbiome. Nat. Biotechnol. 39, 105–114 (2021).
Parks, D. H. et al. A complete domain-to-species taxonomy for Bacteria and Archaea. Nat. Biotechnol. 38, 1079–1086 (2020).
Letunic, I. & Bork, P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 47, W256–w259 (2019).
Hyatt, D. et al. Prodigal: prokaryotic gene recognition and translation initiation site identification. BMC Bioinformatics 11, 119 (2010).
Steinegger, M. & Söding, J. MMseqs2 enables sensitive protein sequence searching for the analysis of massive data sets. Nat. Biotechnol. 35, 1026–1028 (2017).
Li, J. et al. An integrated catalog of reference genes in the human gut microbiome. Nat. Biotechnol. 32, 834–841 (2014).
Patro, R., Duggal, G., Love, M. I., Irizarry, R. A. & Kingsford, C. Salmon provides fast and bias-aware quantification of transcript expression. Nat. Methods 14, 417–419 (2017).
Boeckmann, B. et al. The SWISS-PROT protein knowledgebase and its supplement TrEMBL in 2003. Nucleic Acids Res. 31, 365–370 (2003).
Suzek, B. E., Wang, Y., Huang, H., McGarvey, P. B. & Wu, C. H. UniRef clusters: a comprehensive and scalable alternative for improving sequence similarity searches. Bioinformatics 31, 926–932 (2015).
Huerta-Cepas, J. et al. Fast genome-wide functional annotation through orthology assignment by eggNOG-Mapper. Mol. Biol. Evol. 34, 2115–2122 (2017).
Huerta-Cepas, J. et al. eggNOG 5.0: a hierarchical, functionally and phylogenetically annotated orthology resource based on 5090 organisms and 2502 viruses. Nucleic Acids Res. 47, D309–D314 (2019).
Kanehisa, M., Furumichi, M., Tanabe, M., Sato, Y. & Morishima, K. KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res. 45, D353–d361 (2017).
Levasseur, A., Drula, E., Lombard, V., Coutinho, P. M. & Henrissat, B. Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes. Biotechnol. Biofuels 6, 41 (2013).
Tatusov, R. L. et al. The COG database: an updated version includes eukaryotes. BMC Bioinformatics 4, 41 (2003).
Jia, B. et al. CARD 2017: expansion and model-centric curation of the comprehensive antibiotic resistance database. Nucleic Acids Res. 45, D566–D573 (2017).
Alcock, B. P. et al. CARD 2020: antibiotic resistome surveillance with the comprehensive antibiotic resistance database. Nucleic Acids Res. 48, D517–D525 (2020).
Liu, B., Zheng, D., Jin, Q., Chen, L. & Yang, J. VFDB 2019: a comparative pathogenomic platform with an interactive web interface. Nucleic Acids Res. 47, D687–D692 (2019).
Seemann, T. Prokka: rapid prokaryotic genome annotation. Bioinformatics 30, 2068–2069 (2014).
de Nies, L. et al. PathoFact: a pipeline for the prediction of virulence factors and antimicrobial resistance genes in metagenomic data. Microbiome 9, 49 (2021).
Blin, K. et al. antiSMASH 5.0: updates to the secondary metabolite genome mining pipeline. Nucleic Acids Res. 47, W81–w87 (2019).
Navarro-Muñoz, J. C. et al. A computational framework to explore large-scale biosynthetic diversity. Nat. Chem. Biol. 16, 60–68 (2020).
Tibetan Glacier Genome and Gene catalogue Raw sequence reads. Tibetan Glacier Genome and Gene catalogue. National Center for Biotechnology Information. https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJEB12327 (2022).
This study was supported by the Second Tibetan Plateau Scientific Expedition and Research Program (STEP) 2019QZKK0503 (Y. Liu and K.L.) and 2021QZKK0100 (P.L., Y. Luo and T. Yu); the National Key Research and Development Plans 2019YFC1509103 (Y. Liu) and 2021YFC2300904 (M.J.); and the Major Research Plan of the National Natural Science Foundation of China 91851207 (Y. Liu and Y.C.).
The authors declare no competing interests.
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Liu, Y., Ji, M., Yu, T. et al. A genome and gene catalog of glacier microbiomes. Nat Biotechnol 40, 1341–1348 (2022). https://doi.org/10.1038/s41587-022-01367-2
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