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.2018 Oct 3;19(1):724.
doi: 10.1186/s12864-018-5099-6.

Exclusivity offers a sound yet practical species criterion for bacteria despite abundant gene flow

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Exclusivity offers a sound yet practical species criterion for bacteria despite abundant gene flow

Erik S Wright et al. BMC Genomics..

Abstract

Background: The question of whether bacterial species objectively exist has long divided microbiologists. A major source of contention stems from the fact that bacteria regularly engage in horizontal gene transfer (HGT), making it difficult to ascertain relatedness and draw boundaries between taxa. A natural way to define taxa is based on exclusivity of relatedness, which applies when members of a taxon are more closely related to each other than they are to any outsider. It is largely unknown whether exclusive bacterial taxa exist when averaging over the genome or are rare due to rampant hybridization.

Results: Here, we analyze a collection of 701 genomes representing a wide variety of environmental isolates from the family Streptomycetaceae, whose members are competent at HGT. We find that the presence/absence of auxiliary genes in the pan-genome displays a hierarchical (tree-like) structure that correlates significantly with the genealogy of the core-genome. Moreover, we identified the existence of many exclusive taxa, although individual genes often contradict these taxa. These conclusions were supported by repeating the analysis on 1,586 genomes belonging to the genus Bacillus. However, despite confirming the existence of exclusive groups (taxa), we were unable to identify an objective threshold at which to assign the rank of species.

Conclusions: The existence of bacterial taxa is justified by considering average relatedness across the entire genome, as captured by exclusivity, but is rejected if one requires unanimous agreement of all parts of the genome. We propose using exclusivity to delimit taxa and conventional genome similarity thresholds to assign bacterial taxa to the species rank. This approach recognizes species that are phylogenetically meaningful, while also establishing some degree of comparability across species-ranked taxa in different bacterial clades.

Keywords: Classification; Horizontal gene transfer; Phylogeny; Species; Taxonomy.

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Figures

Fig. 1
Fig. 1
Common measures of the species rank exhibit widely different correlations with gene content similarity in Streptomycetaceae. The 16S rRNA sequence showed little correlation with gene content similarity (R2 = 0.38), whereas therpoB gene sequence displayed good correlation (R2 = 0.75). Two genome-wide measures of similarity, average nucleotide identity (ANI) and alignment fraction (AF), were strongly correlated with gene content similarity. Horizontal dashed lines denote commonly used species-level cutoffs for each measure (e.g., > 97% 16S sequence identity)
Fig. 2
Fig. 2
Strong correspondence between trees based on the core-genome and pan-genome in Streptomycetaceae. A maximum-likelihood tree from the core-genome (left) and a UPGMA tree based on gene content similarity (right) are similar in structure. The same 701 tips on both trees are connected by colored lines showing the degree of entanglement. Note that tips on the maximum likelihood core-genome tree (left) are extended by gray lines to the same horizontal position because the tree is not ultrametric like the pan-genome UPGMA tree (right)
Fig. 3
Fig. 3
UPGMA tree of gene content similarity showing the distribution of exclusivity among 701 Streptomycetaceae genomes. Internal edges of the tree are colored based on their degree of exclusivity (see Methods), from not exclusive (orange) to exclusive (blue). Leaves of the tree are shown in dark blue because they are trivially exclusive (*). The horizontal bar below leaf tips is colored according to the 12 largest species (otherwise gray), here defined as single-linkage groups having AF > 0.6 and ANI > 96.5%. Exclusive groups are more frequent at lower taxonomic levels, which suggests either a lack of consistent signal to resolve deep relationships or true non-exclusivity due to wide hybridization events
Fig. 4
Fig. 4
Exclusivity is unlikely to be the result of subsampling Streptomycetaceae genomes. Black lines show average measures of exclusivity for all clades on the pan-genome UPGMA tree for Streptomycetaceae, with ± one standard deviation indicated by the surrounding gray region. Clades are considered exclusive if their exclusivity score determined from the core-genome is greater than zero. Except for very small subsamples, exclusivity quickly plateaus with increasing sample size, suggesting that the existence of exclusivity is not the result of subsampling the total population of genomes
Fig. 5
Fig. 5
Absence of an abrupt transition for denoting the species rank. The average degree of exclusivity based on the core-genome average patristic distances (y-axis) is shown for clades with increasing breadth (x-axis) on the pan-genome tree. The lack of a relationship between exclusivity and clade diversity (maximum in-group distance) in Streptomycetaceae (left) orBacillus (right) shows that there is no phase transition in exclusivity that could serve as an objective species-level ranking criterion. The gray region shows ± one standard deviation from the average exclusivity at each maximum in-group distance
Fig. 6
Fig. 6
Core-genome tree depicting species groups defined in Streptomycetaceae with our methodology. A UPGMA tree was constructed using the average of 157 matrices containing the pairwise patristic distances derived from each core-gene tree. Exclusive groups were defined according to the same matrix of average patristic distances for the 701 genomes. We then delineated as species the largest exclusive groups whose members met the joint ANI/AF criterion with a single-linkage approach. Singleton species are represented by blue leaves, whereas species with multiple genomes appear as a group of black leaves subtended by a brown edge
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