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Genomic insights that advance the species definition for prokaryotes.

ABSTRACT: To help advance the species definition for prokaryotes, we have compared the gene content of 70 closely related and fully sequenced bacterial genomes to identify whether species boundaries exist, and to determine the role of the organism's ecology on its shared gene content. We found the average nucleotide identity (ANI) of the shared genes between two strains to be a robust means to compare genetic relatedness among strains, and that ANI values of approximately 94% corresponded to the traditional 70% DNA-DNA reassociation standard of the current species definition. At the 94% ANI cutoff, current species includes only moderately homogeneous strains, e.g., most of the >4-Mb genomes share only 65-90% of their genes, apparently as a result of the strains having evolved in different ecological settings. Furthermore, diagnostic genetic signatures (boundaries) are evident between groups of strains of the same species, and the intergroup genetic similarity can be as high as 98-99% ANI, indicating that justifiable species might be found even among organisms that are nearly identical at the nucleotide level. Notably, a large fraction, e.g., up to 65%, of the differences in gene content within species is associated with bacteriophage and transposase elements, revealing an important role of these elements during bacterial speciation. Our findings are consistent with a definition for species that would include a more homogeneous set of strains than provided by the current definition and one that considers the ecology of the strains in addition to their evolutionary distance.

SUBMITTER: Konstantinidis KT

PROVIDER: S-EPMC549018 | biostudies-literature | 2005 Feb

REPOSITORIES: biostudies-literature

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Genomic insights that advance the species definition for prokaryotes.

Konstantinidis Konstantinos T KT Tiedje James M JM

Proceedings of the National Academy of Sciences of the United States of America 20050208 7

To help advance the species definition for prokaryotes, we have compared the gene content of 70 closely related and fully sequenced bacterial genomes to identify whether species boundaries exist, and to determine the role of the organism's ecology on its shared gene content. We found the average nucleotide identity (ANI) of the shared genes between two strains to be a robust means to compare genetic relatedness among strains, and that ANI values of approximately 94% corresponded to the tradition ...[more]

PMID: 15701695

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Project description:BackgroundDNA word frequencies, normalized for genomic AT content, are remarkably stable within prokaryotic genomes and are therefore said to reflect a "genomic signature." The genomic signatures can be used to phylogenetically classify organisms from arbitrary sampled DNA. Genomic signatures can also be used to search for horizontally transferred DNA or DNA regions subjected to special selection forces. Thus, the stability of the genomic signature can be used as a measure of genomic homogeneity. The factors associated with the stability of the genomic signatures are not known, and this motivated us to investigate further. We analyzed the intra-genomic variance of genomic signatures based on AT content normalization (0(th) order Markov model) as well as genomic signatures normalized by smaller DNA words (1(st) and 2(nd) order Markov models) for 636 sequenced prokaryotic genomes. Regression models were fitted, with intra-genomic signature variance as the response variable, to a set of factors representing genomic properties such as genomic AT content, genome size, habitat, phylum, oxygen requirement, optimal growth temperature and oligonucleotide usage variance (OUV, a measure of oligonucleotide usage bias), measured as the variance between genomic tetranucleotide frequencies and Markov chain approximated tetranucleotide frequencies, as predictors.Principal findingsRegression analysis revealed that OUV was the most important factor (p<0.001) determining intra-genomic homogeneity as measured using genomic signatures. This means that the less random the oligonucleotide usage is in the sense of higher OUV, the more homogeneous the genome is in terms of the genomic signature. The other factors influencing variance in the genomic signature (p<0.001) were genomic AT content, phylum and oxygen requirement.ConclusionsGenomic homogeneity in prokaryotes is intimately linked to genomic GC content, oligonucleotide usage bias (OUV) and aerobiosis, while oligonucleotide usage bias (OUV) is associated with genomic GC content, aerobiosis and habitat.

Project description:BACKGROUND:Microbial taxonomy remains a conservative discipline, relying on phenotypic information derived from growth in pure culture and techniques that are time-consuming and difficult to standardize, particularly when compared to the ease of modern high-throughput genome sequencing. Here, drawing on the genus Acinetobacter as a test case, we examine whether bacterial taxonomy could abandon phenotypic approaches and DNA-DNA hybridization and, instead, rely exclusively on analyses of genome sequence data. RESULTS:In pursuit of this goal, we generated a set of thirteen new draft genome sequences, representing ten species, combined them with other publically available genome sequences and analyzed these 38 strains belonging to the genus. We found that analyses based on 16S rRNA gene sequences were not capable of delineating accepted species. However, a core genome phylogenetic tree proved consistent with the currently accepted taxonomy of the genus, while also identifying three misclassifications of strains in collections or databases. Among rapid distance-based methods, we found average-nucleotide identity (ANI) analyses delivered results consistent with traditional and phylogenetic classifications, whereas gene content based approaches appear to be too strongly influenced by the effects of horizontal gene transfer to agree with previously accepted species. CONCLUSION:We believe a combination of core genome phylogenetic analysis and ANI provides an appropriate method for bacterial species delineation, whereby bacterial species are defined as monophyletic groups of isolates with genomes that exhibit at least 95% pair-wise ANI. The proposed method is backwards compatible; it provides a scalable and uniform approach that works for both culturable and non-culturable species; is faster and cheaper than traditional taxonomic methods; is easily replicable and transferable among research institutions; and lastly, falls in line with Darwin's vision of classification becoming, as far as is possible, genealogical.

Dataset Information

Genomic insights that advance the species definition for prokaryotes.

Publications

Genomic insights that advance the species definition for prokaryotes.

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