The synergistic effect of concatenation in phylogenomics: the case in Pantoea

Abstract

With the increased availability of genome sequences for bacteria, it has become routine practice to construct genome-based phylogenies. These phylogenies have formed the basis for various taxonomic decisions, especially for resolving problematic relationships between taxa. Despite the popularity of concatenating shared genes to obtain well-supported phylogenies, various issues regarding this combined-evidence approach have been raised. These include the introduction of phylogenetic error into datasets, as well as incongruence due to organism-level evolutionary processes, particularly horizontal gene transfer and incomplete lineage sorting. Because of the huge effect that this could have on phylogenies, we evaluated the impact of phylogenetic conflict caused by organism-level evolutionary processes on the established species phylogeny for Pantoea, a member of the Enterobacterales. We explored the presence and distribution of phylogenetic conflict at the gene partition and nucleotide levels, by identifying putative inter-lineage recombination events that might have contributed to such conflict. Furthermore, we determined whether smaller, randomly constructed datasets had sufficient signal to reconstruct the current species tree hypothesis or if they would be overshadowed by phylogenetic incongruence. We found that no individual gene tree was fully congruent with the species phylogeny of Pantoea, although many of the expected nodes were supported by various individual genes across the genome. Evidence of recombination was found across all lineages within Pantoea, and provides support for organism-level evolutionary processes as a potential source of phylogenetic conflict. The phylogenetic signal from at least 70 random genes recovered robust, well-supported phylogenies for the backbone and most species relationships of Pantoea, and was unaffected by phylogenetic conflict within the dataset. Furthermore, despite providing limited resolution among taxa at the level of single gene trees, concatenated analyses of genes that were identified as having no signal resulted in a phylogeny that resembled the species phylogeny of Pantoea. This distribution of signal and noise across the genome presents the ideal situation for phylogenetic inference, as the topology from a ≥70-gene concatenated species phylogeny is not driven by single genes, and our data suggests that this finding may also hold true for smaller datasets. We thus argue that, by using a concatenation-based approach in phylogenomics, one can obtain robust phylogenies due to the synergistic effect of the combined signal obtained from multiple genes.

Streptococcus vicugnae sp. nov., isolated from faeces of alpacas (Vicugna pacos) and cattle (Bos taurus), Streptococcus zalophi sp. nov., and Streptococcus pacificus sp. nov., isolated from respiratory tract of California sea lions (Zalophus californianus)

“…ANI values were computed as described by Goris et al [44] and as implemented in JSpecies [45]. In this analysis, strains SL1232 T A further standard approach to obtain robust insights into the phylogeny of bacterial taxa is to use the core genome, the set of genes that have orthologous genes in all analysed strains [48], as a maximal set of marker genes. We again used the EDGAR platform to calculate a core genome of 14 type and non-type strain genomes of the genus Streptococcus, including the novel strains.…”

Sneathia vaginalis sp. nov. (Fusobacteriales, Leptotrichiaceae) as a replacement of the species ‘Sneathia amnii’ Harwich et al. 2012 and ‘Leptotrichia amnionii’ Shukla et al. 2002, and emended description of Sneathia Collins et al. 2001

“…Compared to reference genomes and the S. sanguinegens type strain genome very similar values were noted for genome size and G+C content (DSM 16630: 1 247 497 bp/29.0 mol%; 'S. amnii' Sn35: 1 339 284 bp/28.3 mol%; CCUG 41628 T : 1 291 023 bp/26.7 mol%).The phylogenetic position of strains DSM 16630 and DSM 16631 T was further examined by analysis of the core genome, the set of genes that have orthologs in all analysed strains[40], as maximal set of marker genes. The edgar platform was utilised to calculate a core genome of the strains under study with 17 type strain genomes of the family Leptotrichiaceae.Fig.…”

“…1). All Sneathia members were clearly The phylogenetic position of strains DSM 16630 and DSM 16631 T was further examined by analysis of the core genome, the set of genes that have orthologs in all analysed strains [40], as maximal set of marker genes. The edgar platform was utilised to calculate a core genome of the strains under study with 17 type strain genomes of the family Leptotrichiaceae.…”

Streptobacillus canis sp. nov. isolated from a dog

“…The phylogenetic position of strain IHIT1603-19 T was further enlarged upon a comprehensive insight into the core genome, the set of genes that have orthologous genes in all analysed strains [33], as a maximal set of marker genes. The edgar platform was utilized to calculate a core genome of 18 type strain genomes of the family Leptotrichiaceae .…”