Cited by 5,748Genomics and Phylogenetic StudiesBacterial Identification and Susceptibility TestingMicrobial Community Ecology and Physiology

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High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries

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Jain, Chirag, Rodriguez-R, Luis M., Phillippy, Adam M., Konstantinidis, Konstantinos T., Aluru, Srinivas·2018·Nature Communications

DOI 10.1038/s41467-018-07641-9PMC PMC6269478

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Abstract

A fundamental question in microbiology is whether there is continuum of genetic diversity among genomes, or clear species boundaries prevail instead. Whole-genome similarity metrics such as Average Nucleotide Identity (ANI) help address this question by facilitating high resolution taxonomic analysis of thousands of genomes from diverse phylogenetic lineages. To scale to available genomes and beyond, we present FastANI, a new method to estimate ANI using alignment-free approximate sequence mapping. FastANI is accurate for both finished and draft genomes, and is up to three orders of magnitude faster compared to alignment-based approaches. We leverage FastANI to compute pairwise ANI values among all prokaryotic genomes available in the NCBI database. Our results reveal clear genetic discontinuity, with 99.8% of the total 8 billion genome pairs analyzed conforming to >95% intra-species and <83% inter-species ANI values. This discontinuity is manifested with or without the most frequently sequenced species, and is robust to historic additions in the genome databases.

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Fig. 1 Correlation of FastANI and Mash-based ANI output with ANIb values for datasets D1–D5. Because FastANI assumes a probabilistic identity cutoff that is set to 80% by default, it reports 76, 570, 4271, 464, and 130 genome matches for the individual queries in datasets D1–D5 respectively. To enable a direct quality comparison against FastANI, Mash is executed for only those pairs that are reported by FastANI. Notice that each dataset encompasses a different nucleotide identity range (x-axes). Gray line represents a straight line y = x plot for reference. Pearson correlation coefficients corresponding to these plots are listed separately in Table 2. Last plot shows error of these methods w.r.t. ANIb using all five datasetsCC BY · PubMed Central

Fig. 2 Scaling up FastANI’s performance using multi-core parallel execution. We executed parallel FastANI processes on 40 physical cores, where each process was assigned an equally sized part of the reference D1–D5 databases. Left and right plots evaluate FastANI’s compute and indexing phase, respectively. FastANI achieves reasonable speedups on all datasets except the compute phase in D1 and D5, as their runtime on a single core is too small to begin with (Table 3)CC BY · PubMed Central

Fig. 3 Genetic discontinuity observed using 90 K genomes. a Histogram plot showing the distribution of ANI values among the 90 K genomes. Only ANI values in the 76–100% range are shown. Out of total 8.01 billion pairwise genome comparisons, FastANI reported only 17M ANI values (0.21%) with ANI between 83 and 95% indicating a genetic discontinuum. Multiple colors are used to show how genomes from different genera are contributing to this distribution. Few peaks in the histogram arise from genera that have been extensively sequenced and dominate the database. b Density curves of ANI values in the ANI range 76–100%. Each curve shows the density curve corresponding to the database at a particular time period. Discontinuity in all four curves is observed consistently. c. Distribution of ANI values with each comparison labeled by the nomenclature of genomes being compared. All the comparisons between Escherichia coli and Shigella spp. have been labeled separately. The 95% ANI threshold on x-axis serves as a valid classifier for comparisons belonging to same and different speciesCC BY · PubMed Central

Fig. 4 FastANI algorithm explained using synthetic and real examples. a Illustration of FastANI’s work-flow for computing ANI between a query genome and a reference genome. Five mappings are obtained from three query fragments using Mashmap24. Mforward saves the maximum identity mapping for each query fragment. In this example, Mforward = {m2, m4, m5}. From this set, Mreciprocal picks m4 and m5 as the maximum identity mapping for each reference bin. Mapping identities of orthologous mappings, thus found in Mreciprocal, are finally averaged to compute ANI. b FastANI supports visualization of the orthologous mappings Mreciprocal that are used to estimate the ANI value using genoPlotR39. In this figure, ANI is computed between Bartonella quintana strain (NC_018533.1) as query and Bartonella henselae strain (NC_005956.1) as reference. Red line segments denote the orthologous mappings computed by FastANI for ANI estimationCC BY · PubMed Central

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“This process allowed to identify and select most complete and less contaminated genomes within each species cluster,which yielded 7658non-redundant species-levelgenomeswith an average nucleotide identity below 95%, a threshold previously reported to delineate species level for prokaryotes 86 .”
Metabolic coupling between soil aerobic methanotrophs and denitrifiers in rice paddy fields
Chen, K.-H., Feng, J., Bodelier, P. L. E., Yang, Z., Huang, Q., Delgado‐Baquerizo, M., Cai, P., Tan, W., & Liu, Y. (2024) · Nature Communications · doi:10.1038/s41467-024-47827-y · Cited by 73
“0) was used tocalculate thevaluesof genome ANI as referred to GTDB database 97 .”
Expanding the human gut microbiome atlas of Africa
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“Genome-derived parameters, such as the 95% average nucleotide identity (ANI), have been shown to better encompass the named species based on isolates (8, 20) and the natural sequence-discrete populations sampled by metagenomics (21), as these parameters capture better than 16S rRNA gene sequence analysis the tradition…”
BackgroundSelf-citation
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“To identify MAGs that were recovered from both assembly methods, FastANI was run on all pairwise comparisons of the Illumina-only and ONT-only MAGs to the hybrid MAGs that were initially assessed using CheckM (82 hybrid, 44 Illumina-only, 35 ONT-only) (Jain et al., 2018).”
MethodInfluential
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Staphylococcal diversity in atopic dermatitis from an individual to a global scale
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Zhao, F., Yang, L., Zhang, T., Zhuang, D., Wu, Q., Yu, J., Tian, C., & Zhang, Z. (2023) · npj Biofilms and Microbiomes · doi:10.1038/s41522-023-00395-3 · Cited by 73
Plastics shape the black soldier fly larvae gut microbiome and select for biodegrading functions
Filippis, F. D., Bonelli, M., Bruno, D., Sequino, G., Montali, A., Reguzzoni, M., Pasolli, E., Savy, D., Cangemi, S., Cozzolino, V., et al. (2023) · Microbiome · doi:10.1186/s40168-023-01649-0 · Cited by 76
“To define subspecies, pairwise average nucleotide identities (ANI) were estimated between genomes falling in the same SGB through FastANI [71] and clustered using the Partitioning Around Medoid (PAM) algo-rithm in R, as described recently [72].”
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“33 54 , and only 15,643 genomes that exhibited ≥ 95% ANIs to the references were kept in down-stream analysis.”
Correlation of Key Physiological Properties of Methanosarcina Isolates with Environment of Origin
Zhou, J., Holmes, D. E., Tang, H., & Lovley, D. R. (2021) · Applied and Environmental Microbiology · doi:10.1128/aem.00731-21 · Cited by 72
“The genome of M. subterranea is currently not available; however, comparison of the strain DH-2 genome to other Methanosarcina genomes with the FastANI tool (average nucleotide identity [ANI], a measure of nucleotide-level genomic similarity between the coding regions of two genomes) (21) showed that DH-2 is most simi…”
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“32) [53] to compare the genomes for different data sets, and only one of the genomes was retained when the genomes were highly similar (pairwise ANI was 100”
Background
Genomic changes underlying host specialization in the bee gut symbiont Lactobacillus Firm5
Ellegaard, K., Brochet, S., Bonilla‐Rosso, G., Emery, O., Glover, N., Hadadi, N., Jaroň, K. S., van der Meer, J. R., Robinson‐Rechavi, M., Sentchilo, V., et al. (2019) · Molecular Ecology · doi:10.1111/mec.15075 · Cited by 70
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“Ecological distribution and environmental correlations For determining the ecological distribution and environmental correlations, a non-redundant set of MAGs was determined using FastANI (Jain et al., 2018) (v1.”
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APPLES: Scalable Distance-Based Phylogenetic Placement with or without Alignments
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Delineating yeast species with genome average nucleotide identity: a calibration of ANI with haplontic, heterothallic Metschnikowia species
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“This is at considerable variance with the large gap (83–96% ANI) separating interspecific and intraspecific values in prokaryotes (Jain et al. 2018).”
Background
Genome-centric analysis of short and long read metagenomes reveals uncharacterized microbiome diversity in Southeast Asians
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Reply to: “Re-evaluating the evidence for a universal genetic boundary among microbial species”
Rodriguez‐R, L. M., Jain, C., Conrad, R. E., Aluru, S., & Konstantinidis, K. T. (2021) · Nature Communications · doi:10.1038/s41467-021-24129-1 · Cited by 68
Self-citation
A Genome-Based Species Taxonomy of the Lactobacillus Genus Complex
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Diversity and evolution of surface polysaccharide synthesis loci in Enterobacteriales
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Genotypic and Phenotypic Diversity of Staphylococcus aureus Isolates from Cystic Fibrosis Patient Lung Infections and Their Interactions with Pseudomonas aeruginosa
Bernardy, E. E., Petit, R. A., Raghuram, V., Alexander, A. M., Read, T. D., & Goldberg, J. B. (2020) · mBio · doi:10.1128/mbio.00735-20 · Cited by 69
Recovery of strain-resolved genomes from human microbiome through an integration framework of single-cell genomics and metagenomics
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“ANI was calculated for selected SAGs using FastANI 1.3 [42].”
MethodInfluential
Compositional and Metabolic Responses of Autotrophic Microbial Community to Salinity in Lacustrine Environments
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“Average nucleotide identity (ANI) analysis demonstrated that each MAG represented a unique species based on the species demarcation threshold of 95% (24).”
Background
EnteroBase: hierarchical clustering of 100 000s of bacterial genomes into species/subspecies and populations
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“Fast 71 computational methods based on k-mer searches, such as FastANI [10], can perform 72 ANI-like calculations on large numbers of genomes, and these calculations are now 73 routinely used by bioinformaticians for taxonomic assignments.”
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Klapper, M., Hübner, A., Ibrahim, A., Wasmuth, I., Borry, M., Haensch, V. G., Zhang, S., Al‐Jammal, W. K., Suma, H. R., Yates, J. A. F., et al. (2023) · Science · doi:10.1126/science.adf5300 · Cited by 67
Lactococcus lactis in Dairy Fermentation—Health-Promoting and Probiotic Properties
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“The integration of a variety of tools, e.g., FastANI [377], mobileOG-db [378], CRISPR/Cas Finder, pLannotate [379], and CGView Builder [380], and their associated visualization capabilities facilitates the identiﬁcation of genome elements of interest.”
Method
Gut microbiota contributes to high-altitude hypoxia acclimatization of human populations
Su, Q., Zhuang, D., Li, Y., Chen, Y., Wang, X.-Y., Ge, M., Xue, T.-Y., Zhang, Q.-Y., Liu, X., Yin, F.-Q., et al. (2024) · Genome biology · doi:10.1186/s13059-024-03373-w · Cited by 73
“According to the 95% average nucleotide identity (ANI) threshold [13], a non-redundant genome set consisting of 4312 species-level genome bins (SGBs) was constructed based on these data and a previously published human microbial genome [14].”
Method
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Diesel and Crude Oil Biodegradation by Cold-Adapted Microbial Communities in the Labrador Sea
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“FastANI (118), with minimum fragment length set to 1,000 bp and other parameters set to default, was used to compare the percent average nucleotide identity (ANI) of select MAGs and published genomes.”
Method
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Methylobacterium ajmalii sp. nov., Isolated From the International Space Station
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“Genomes of all other strains used in this study were downloaded from NCBI, and the genomic relatedness of ISS strains was identified based on average nucleotide identity (ANI; FastANI) calculations (Jain et al., 2018) and digital DNA-DNA hybridization (dDDH) analysis (Meier-Kolthoff et al., 2013).”
Method
UG/Abi: a highly diverse family of prokaryotic reverse transcriptases associated with defense functions
Mestre, M. R., Gao, L. A., Shah, S. A., López-Beltrán, A., González-Delgado, A., Martínez‐Abarca, F., Iranzo, J., Redrejo‐Rodríguez, M., Zhang, F., & Toro, N. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac467 · Cited by 65
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“Average nucleotide identities (ANI) between these high-quality, nearly complete genomes ranged between 82.2% and 86.6%, which is below the intra-species cut-off of 95% [57] and suggests that these MAGs represent individual species.”
BackgroundInfluential
Comparative genomic analysis of the genus Novosphingobium and the description of two novel species Novosphingobium aerophilum sp. nov. and Novosphingobium jiangmenense sp. nov
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Opposite Sides of Pantoea agglomerans and Its Associated Commercial Outlook
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Authors: Jain, C., Rodriguez-R, L. M., Phillippy, A. M., Konstantinidis, K. T., & Aluru, S.
Affiliations: National Institutes of Health (US)
Georgia Institute of Technology (US)
Corresponding author: Konstantinidis, Konstantinos T.
Aluru, Srinivas
ORCID: Jain, Chirag
Rodriguez-R, Luis M.
Phillippy, Adam M.
Konstantinidis, Konstantinos T.
Aluru, Srinivas
Venue: Nature Communications
Publisher: Springer Science and Business Media LLC
Published: 2018-11-30
Volume: 9
Issue: 1
Pages: 5114-5114
ISSN: 2041-1723 (ISSN-L)
DOI: 10.1038/s41467-018-07641-9
PMC: PMC6269478
OpenAlex: W2951254987
Cited by: 5,748
References: 40
Citations by year: 2026: 1107 · 2025: 1110 · 2024: 977 · 2023: 789 · 2022: 695 · 2021: 617 · 2020: 305 · 2019: 128 · 2018: 16
FWCI: 96.11
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0 (tdm)
creativecommons.org/licenses/by/4.0 (vor)
Locations: Nature Communications (publishedVersion, cc-by)
bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, other-oa)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders: National Science Foundation (1416259, 1816027, 1356288)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
Health Sciences › Medicine › Microbiology (medical) › Bacterial Identification and Susceptibility Testing
Physical Sciences › Environmental Science › Ecology › Microbial Community Ecology and Physiology
Keywords: average nucleotide identity, prokaryotic genomes, species boundaries, taxonomic classification, draft genome sequence
MeSH terms: Phylogeny, Prokaryotic Cells, Genetic Variation, Databases, Factual, Genome, Bacterial, Sequence Analysis, DNA

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High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries

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