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1,003 reference genomes of bacterial and archaeal isolates expand coverage of the tree of life

Mukherjee, Supratim, Seshadri, Rekha, Varghese, Neha J, Eloe-Fadrosh, Emiley A, Meier-Kolthoff, Jan P, Göker, Markus, Coates, R Cameron, Hadjithomas, Michalis, Pavlopoulos, Georgios A, Paez-Espino, David, Yoshikuni, Yasuo, Visel, Axel, Whitman, William B, Garrity, George M, Eisen, Jonathan A, Hugenholtz, Philip, Pati, Amrita, Ivanova, Natalia N, Woyke, Tanja, Klenk, Hans-Peter, Kyrpides, Nikos C·2017·Nature Biotechnology
DOI 10.1038/nbt.3886
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Abstract

We present 1,003 reference genomes that were sequenced as part of the Genomic Encyclopedia of Bacteria and Archaea (GEBA) initiative, selected to maximize sequence coverage of phylogenetic space. These genomes double the number of existing type strains and expand their overall phylogenetic diversity by 25%. Comparative analyses with previously available finished and draft genomes reveal a 10.5% increase in novel protein families as a function of phylogenetic diversity. The GEBA genomes recruit 25 million previously unassigned metagenomic proteins from 4,650 samples, improving their phylogenetic and functional interpretation. We identify numerous biosynthetic clusters and experimentally validate a divergent phenazine cluster with potential new chemical structure and antimicrobial activity. This Resource is the largest single release of reference genomes to date. Bacterial and archaeal isolate sequence space is still far from saturated, and future endeavors in this direction will continue to be a valuable resource for scientific discovery.

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Figure 1 GEBA-I strain phylogeny and distribution. ( a ) Maximum likelihood tree based on concatenated alignment of 56 conserved protein markers from representative genomes from all cultivated phyla. Phyla containing a GEBA-I genome are colored red, while all other phyla are colored gray. Pie charts represent the fraction of genera contributed by GEBA-I genomes (red) to the total number of genera per phylum (blue). The number of new genera added by GEBA-I per phylum is displayed next to the pie charts. Bootstrap support values ≥ 50% are shown with small circles on nodes with robust phylogenetic support. ( b ) Overall increase in 16S rRNA gene diversity relative to all the type strains. Blue denotes the genetic diversity covered by 828 genomes of type strains before GEBA-I, red denotes the diversity covered by the GEBA-I genomes and gray denotes the remaining type strains lacking a genome sequence. Balanced relative phylogenetic diversity (bRPD) was calculated by adding branch lengths between each leaf and root node in the tree followed by proportional downweighting of internal branches 6 .
Figure 1 GEBA-I strain phylogeny and distribution. ( a ) Maximum likelihood tree based on concatenated alignment of 56 conserved protein markers from representative genomes from all cultivated phyla. Phyla containing a GEBA-I genome are colored red, while all other phyla are colored gray. Pie charts represent the fraction of genera contributed by GEBA-I genomes (red) to the total number of genera per phylum (blue). The number of new genera added by GEBA-I per phylum is displayed next to the pie charts. Bootstrap support values ≥ 50% are shown with small circles on nodes with robust phylogenetic support. ( b ) Overall increase in 16S rRNA gene diversity relative to all the type strains. Blue denotes the genetic diversity covered by 828 genomes of type strains before GEBA-I, red denotes the diversity covered by the GEBA-I genomes and gray denotes the remaining type strains lacking a genome sequence. Balanced relative phylogenetic diversity (bRPD) was calculated by adding branch lengths between each leaf and root node in the tree followed by proportional downweighting of internal branches 6 .CC-BY · From the PDF
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CC-BY · From the PDF
Figure 2 Protein clusters identified using GEBA-I genomes. ( a ) Change in growth rate of protein families identified per 1,000 genomes over the years and increase in number of new protein families over time, as new genomes were sequenced and added to public databases (inset). ( b ) Relationship between number of genes in protein clusters and singletons and the minimum 16S rRNA distance of each GEBA-I genome to its closest non-GEBA relative. Outliers, defined as points beyond 90% of the data with the smallest absolute residuals with a linear model, are depicted as red open circles. ( c ) Maximum 16S rRNA distance of genomes contributing a GEBA-I-only protein cluster. Each data point represents a single GEBA-I-only protein cluster and is colored by the cluster type, x axis is the total number of genes in each cluster, and y axis is the maximum 16S distance of genomes contributing to that cluster.
Figure 2 Protein clusters identified using GEBA-I genomes. ( a ) Change in growth rate of protein families identified per 1,000 genomes over the years and increase in number of new protein families over time, as new genomes were sequenced and added to public databases (inset). ( b ) Relationship between number of genes in protein clusters and singletons and the minimum 16S rRNA distance of each GEBA-I genome to its closest non-GEBA relative. Outliers, defined as points beyond 90% of the data with the smallest absolute residuals with a linear model, are depicted as red open circles. ( c ) Maximum 16S rRNA distance of genomes contributing a GEBA-I-only protein cluster. Each data point represents a single GEBA-I-only protein cluster and is colored by the cluster type, x axis is the total number of genes in each cluster, and y axis is the maximum 16S distance of genomes contributing to that cluster.CC-BY · From the PDF
Figure 3 Distribution of biosynthetic clusters (BCs) in GEBA-I genomes. ( a ) Maximum likelihood phylogenetic tree using 56 conserved single-copy genes with horizontal bars representing the percentage of genome encoding biosynthetic gene clusters. Blue stars highlight GEBA-I genomes with the greatest percentage of BCs per genome. The red star indicates the phylogenetic placement of Photobacterium halotolerans DSM 18316 described in b and c . ( b ) Liquid chromatography-mass spectrometry (LC/MS) chromatogram from a crude extract of P. halotolerans DSM 18316 with labeled phenazine peaks. ( c ) Phenazine operon in P. halotolerans DSM 18316 compared to those from Pseudomonas fluorescens 2-79 and Pantoea agglomerans Eh1087.
Figure 3 Distribution of biosynthetic clusters (BCs) in GEBA-I genomes. ( a ) Maximum likelihood phylogenetic tree using 56 conserved single-copy genes with horizontal bars representing the percentage of genome encoding biosynthetic gene clusters. Blue stars highlight GEBA-I genomes with the greatest percentage of BCs per genome. The red star indicates the phylogenetic placement of Photobacterium halotolerans DSM 18316 described in b and c . ( b ) Liquid chromatography-mass spectrometry (LC/MS) chromatogram from a crude extract of P. halotolerans DSM 18316 with labeled phenazine peaks. ( c ) Phenazine operon in P. halotolerans DSM 18316 compared to those from Pseudomonas fluorescens 2-79 and Pantoea agglomerans Eh1087.CC-BY · From the PDF
Figure 4 Recruitment of metagenomic sequences by GEBA-I genomes. ( a ) Overview of metagenomic protein sequence recruitment by individual GEBA-I genomes. Phylogenetic analyses of whole genome sequences were conducted using the high-throughput version of the Genome-Blast Distance Phylogeny approach. Internal branch support above 60% is colored in a range from red (60%) to green (100%) The colored dots decorating the terminus of every tree branch indicates the isolation source habitat for the given GEBA-I genome. The outermost circle bearing a black bar chart denotes the total number of metagenomic sequences with protein blast hits to that GEBA-I genome ( Supplementary Fig. 7 and Supplementary Table 4 ). The habitat distribution for these hits is given in the colored concentric circles that follow. The intensity of color is weighted by fraction of total hits to a habitat. ( b ) Protein recruitment plot showing amino acid percent identity ( y axis) of top hits of Desulfomicrobium baculatum DSM 4028 CDS against metagenomic sample from biofilm of a corroded oil pipeline (IMG taxon_oid: 3300002702). CDS are ordered on the x axis by position on one contiguous scaffold available for this genome. ( c ) Protein recruitment plot showing percent identity ( y axis) of Rudaea cellulosilytica DSM 22992 CDS top protein blast hits against metagenomic sample from corn rhizoplane (IMG taxon_oid: 3300001904). For contrast, top hits against two other rhizosphere samples are included (switchgrass (IMG taxon_oid: 3300002128), and Miscanthus (IMG taxon_oid: 3300001991). CDS are ordered on the x axis by position on six discrete scaffolds (which are themselves ordered by descending sequence length) available for this genome.
Figure 4 Recruitment of metagenomic sequences by GEBA-I genomes. ( a ) Overview of metagenomic protein sequence recruitment by individual GEBA-I genomes. Phylogenetic analyses of whole genome sequences were conducted using the high-throughput version of the Genome-Blast Distance Phylogeny approach. Internal branch support above 60% is colored in a range from red (60%) to green (100%) The colored dots decorating the terminus of every tree branch indicates the isolation source habitat for the given GEBA-I genome. The outermost circle bearing a black bar chart denotes the total number of metagenomic sequences with protein blast hits to that GEBA-I genome ( Supplementary Fig. 7 and Supplementary Table 4 ). The habitat distribution for these hits is given in the colored concentric circles that follow. The intensity of color is weighted by fraction of total hits to a habitat. ( b ) Protein recruitment plot showing amino acid percent identity ( y axis) of top hits of Desulfomicrobium baculatum DSM 4028 CDS against metagenomic sample from biofilm of a corroded oil pipeline (IMG taxon_oid: 3300002702). CDS are ordered on the x axis by position on one contiguous scaffold available for this genome. ( c ) Protein recruitment plot showing percent identity ( y axis) of Rudaea cellulosilytica DSM 22992 CDS top protein blast hits against metagenomic sample from corn rhizoplane (IMG taxon_oid: 3300001904). For contrast, top hits against two other rhizosphere samples are included (switchgrass (IMG taxon_oid: 3300002128), and Miscanthus (IMG taxon_oid: 3300001991). CDS are ordered on the x axis by position on six discrete scaffolds (which are themselves ordered by descending sequence length) available for this genome.CC-BY · From the PDF

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Authors
Mukherjee, S., Seshadri, R., Varghese, N. J., Eloe-Fadrosh, E. A., Meier-Kolthoff, J. P., Göker, M., Coates, R. C., Hadjithomas, M., Pavlopoulos, G. A., Paez-Espino, D., Yoshikuni, Y., Visel, A., Whitman, W. B., Garrity, G. M., Eisen, J. A., Hugenholtz, P., Pati, A., Ivanova, N. N., Woyke, T., Klenk, H.-P., & Kyrpides, N. C.
Venue
Nature Biotechnology
Publisher
Springer Science and Business Media LLC
Published
2017-06-12
Volume
35
Issue
7
Pages
676-683
ISSN
  • 1087-0156
  • 1546-1696
DOI
10.1038/nbt.3886
Cited by
267
References
2
Language
en
Update notices
erratum (2018-04-01)
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