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Distant horizontal gene transfer is rare for multiple families of prokaryotic insertion sequences

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Abstract

Horizontal gene transfer in prokaryotes is rampant on short and intermediate evolutionary time scales. It poses a fundamental problem to our ability to reconstruct the evolutionary tree of life. Is it also frequent over long evolutionary distances? To address this question, we analyzed the evolution of 2,091 insertion sequences from all 20 major families in 438 completely sequenced prokaryotic genomes. Specifically, we mapped insertion sequence occurrence on a 16S rDNA tree of the genomes we analyzed, and we also constructed phylogenetic trees of the insertion sequence transposase coding sequences. We found only 30 cases of likely horizontal transfer among distantly related prokaryotic clades. Most of these horizontal transfer events are ancient. Only seven events are recent. Almost all of these transfer events occur between pairs of human pathogens or commensals. If true also for other, non-mobile DNA, the rarity of distant horizontal transfer increases the odds of reliable phylogenetic inference from sequence data.

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Acknowledgments

Support through SNF grant 315200-116814 is gratefully acknowledged. We thank C. Lewis for technical assistance.

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Authors and Affiliations

  1. Department of Biochemistry, University of Zurich, Bldg. Y27, Winterthurerstrasse 190, 8057, Zurich, Switzerland

    Andreas Wagner & Nicole de la Chaux

  2. The Santa Fe Institute, Santa Fe, NM, USA

    Andreas Wagner

  3. The Swiss Institute of Bioinformatics, Basel, Switzerland

    Andreas Wagner & Nicole de la Chaux

  4. The University of New Mexico, Albuquerque, NM, USA

    Andreas Wagner

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Correspondence to Andreas Wagner.

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Communicated by D. Ussery.

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Figure S1:

Two phylogenetic signatures of horizontal gene transfer are a) phylogeneticincongruence of species and gene tree (or of two gene trees), b) patchy phylogeneticdistribution, where ISs occur only in a small number of distantly related clades on a muchlarger tree. Red arrows indicate hypothetical horizontal transfer events. (PDF 8 kb)

Figure S2:

a) Distribution of pairwise 16S rDNA divergence (fraction of differingnucleotides) among the genomes studied here. Note the scale break on the vertical axis.b) Distribution of synonymous divergence Ks for ISs that occur in different genomes,where Ks<1 (pooled for all IS families). The inset shows the same distribution, but alsofor extremely divergent IS pairs, where Ks>1, and where Ks for individual pairs cannot bereliably estimated, because of this much greater divergence. Note the logarithmic scale onthe inset’s vertical axis.(PDF 19 kb)

Figure S3:

Pruned maximum likelihood 16S rDNA prokaryotic trees showing onlyselected clades and ISs. Lengths of bars indicate IS numbers per genome, with colorscoded as in Figure 1. a) IS1 in the Escherichia coli/Shigella clade. b) IS110 inBurkholderia spp. Numerical values printed on branches correspond to boostrap values.Note the low bootstrap support for multiple clades. The phylogenies of these genomes cannot be resolved with 16S rDNA, and neither can therefore individual horizontal genetransfer events. These examples are representative of all other ISs: we did not find asingle phylogenetically well-resolved clade of closely related bacterial species wheremultiple members contained ISs of a given family. Multi-locus approaches can resolvesuch local clades (Godoy et al. 2003), but they are too computationally costly to apply tothe large number of genomes we study. Trees are displayed with ITOL (Letunic and Bork2007).(PDF 520 kb)

Figure S4

a). Hypothetical phylogeny of ISs in a genome where an IS from the samefamily entered the genome in three independent transfer events (T1, T2, T3). If an amountof time elapses between transfer events that is much greater than the rate at whichnucleotide changes accumulate in ISs, then such transfer events could be distinguished bythree well-separated within-genome IS clades. b) Phylogeny of IS982, which occurs onlyin 2 subspecies of Lactococcus lactis. Note the poor separation of different IS clades, andthe low boostrap values on many branches. The poorly resolved phylogeny is due to thehigh similarity of IS982 elements (mean / maximum Ks of all IS982 pairs within agenome: 0.016/0.017; n=1132). c) Histogram of the maximal within-genomesynonymous divergence Ks,max for all IS families and all genomes that contain at least oneIS pair of a given family. The arrows connecting the distant branches on the tree in theinset indicate that Ks,max is calculated from the most highly diverged ISs within a genome.Of the 116 values plotted here, only 6% (7/116) of genomes contain ISs with saturatedsynonymous divergence Ks. These are included in the right-most bar of the histogram (Ks,max>1). The median (mean, standard deviation) of Ks, max is 0.0087 (0.17, 0.41).(PDF 636 kb)

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Wagner, A., de la Chaux, N. Distant horizontal gene transfer is rare for multiple families of prokaryotic insertion sequences. Mol Genet Genomics 280, 397–408 (2008). https://doi.org/10.1007/s00438-008-0373-y

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