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Biased gene transfer in microbial evolution

Key Points

  • Phylogenies of aminoacyl-tRNA synthetases reveal that horizontal gene transfer (HGT) is biased towards more closely related individuals and species, and occurs more rarely between distant relatives.

  • This bias in HGT frequency towards more similar partners can reinforce patterns of evolution that are generated through shared ancestry.

  • Most HGT events do not introduce noise to phylogenetic reconstruction; HGT between close relatives is difficult to detect using phylogenetic approaches.

  • Homeoalleles encode enzymes that have identical functions but dissimilar characteristics. For example, homeoalleles for aminoacyl-tRNA synthetases are present in the Bacteria and the Archaea. Usually, individual species maintain only a single version of a homeoallele; however, the type of homeoallele can be switched through HGT from a related species.

  • Homeoalleles function like alleles at a higher taxonomic level. Organisms may acquire multiple versions of these alleles, and loss of the ancestral homeoalleles changes the phylogenetic signal.

  • Shared ancestry and biased HGT contribute to maintaining recognizable natural taxonomic groups. However, the correct interpretation of phylogenetic analyses needs to take into consideration the fact that genetic inheritance is not simply vertical.

Abstract

Horizontal gene transfer (HGT) is an important evolutionary process that allows the spread of innovations between distantly related organisms. We present evidence that prokaryotes (bacteria and archaea) are more likely to transfer genetic material with their close relatives than with distantly related lineages. This bias in transfer partners can create phylogenetic signals that are difficult to distinguish from the signal created through shared ancestry. Preferences for transfer partners can be revealed by studying the distribution patterns of divergent genes with identical functions. In many respects, these genes are similar to alleles in a population, except that they coexist only in higher taxonomic groupings and are acquired by a species through HGT. We also discuss the role of biased gene transfer in the formation of taxonomically recognizable natural groups in the tree or net of life.

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Figure 1: Phylogenetic analysis of bacterial tyrosyl-tRNA synthetase amino acid sequences and the corresponding concatenated 16S–23S ribosomal RNA phylogeny.
Figure 2: Gene neighbourhood of the two tyrosyl-tRNA synthetases in two members of the Deltaproteobacteria.
Figure 3: Phylogenetic analysis of bacterial tryptophanyl-tRNA synthetase amino acid sequences and the corresponding concatenated 16S–23S ribosomal RNA phylogeny.
Figure 4: Phylogenetic analysis of archaeal seryl-tRNA synthetase amino acid sequences.
Figure 5: Model of the tree or net of life incorporating extinct lineages, shared ancestry and exchange groups.

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Acknowledgements

The authors thank P. Lapierre, D. Williams, T. Harlow, V. Kask and the Biotechnology Bioservices Center of the University of Connecticut, Storrs, USA, for technical support. This work was supported by a US National Science Foundation Grant (DEB 0830024).

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Correspondence to J. Peter Gogarten.

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Supplementary information S1

Detailed version of the phylogenetic analysis of bacterial (a) TyrRS amino acid sequences and (b) their corresponding concatenated 16S.23S rRNA phylogeny as shown in Figure 1. (PDF 509 kb)

Supplementary information S2

Scatterplots of pairwise evolutionary distances between the combined 16S.23S rRNA (x-axis) and (a) TyrRS and (b.d) TrpRS sequences in a diverse sampling of Bacteria. (PDF 676 kb)

Supplementary information S3

Figure legend overleaf. (PDF 2344 kb)

Supplementary information S4

Statistical analysis using non-parametric bootstrap to assess the probability that the gene loss only model could have given rise to the observed distribution of the rare and common form of SerRS. (PDF 290 kb)

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Glossary

Phylogenetics

The study of the evolutionary (or natural) relationships of organisms as they change through time. Phylogenies can be strictly furcating (often bifurcating) or can include reticulations.

Biased gene transfer

Horizontal gene transfer between preferred partners (usually close relatives) rather than random transfer between any species. Other factors, such as shared ecological niches or symbiotic relationships, can also create a bias in transfer partners.

Aminoacyl-tRNA synthetases

(aaRSs). A family of enzymes that are responsible for the specific attachment of each amino acid to its cognate tRNA during the translation process.

Homeoallele

One of several divergent but functionally identical genes that are swapped within an exchange group (a group of organisms that has a higher rate for within-group gene transfers than for between-group transfers) which contains organisms belonging to different higher-level taxa.

Last universal common ancestor

(LUCA). The most recent organism (or organisms) from which all organisms that are now living on Earth descend. It is necessary to distinguish between the organismal LUCA and the most recent common ancestors of molecules and genes.

Monophyly

A phylogenetic characteristic of a group of organisms, such that the group contains all the descendants of the recent common ancestor of the group members.

Cladistics

A method of classifying organisms into clades based on shared derived characteristics that arise from a common ancestor.

Phenetics

A method of classifying organisms based on their overall similarity.

Tree of life

The tree-like representation of the history of all extant and extinct organisms.

Net of life

The depiction of evolutionary history that integrates both vertical ancestry and horizontal gene transfer events.

Bifurcating scheme

A phylogenetic tree in which all internal nodes have exactly two descendants.

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Andam, C., Gogarten, J. Biased gene transfer in microbial evolution. Nat Rev Microbiol 9, 543–555 (2011). https://doi.org/10.1038/nrmicro2593

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