Inter-genomic displacement via lateral gene transfer of bacterial trp operons in an overall context of vertical genealogy

Gary Xie,Carol A Bonner,Nemat O Keyhani,Roy A Jensen,Jian Song

doi:10.1186/1741-7007-2-15

Gary Xie, Carol A Bonner + Show 3 more

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https://doi.org/10.1186/1741-7007-2-15

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Abstract

BackgroundThe growing conviction that lateral gene transfer plays a significant role in prokaryote genealogy opens up a need for comprehensive evaluations of gene-enzyme systems on a case-by-case basis. Genes of tryptophan biosynthesis are frequently organized as whole-pathway operons, an attribute that is expected to facilitate multi-gene transfer in a single step. We have asked whether events of lateral gene transfer are sufficient to have obscured our ability to track the vertical genealogy that underpins tryptophan biosynthesis.ResultsIn 47 complete-genome Bacteria, the genes encoding the seven catalytic domains that participate in primary tryptophan biosynthesis were distinguished from any paralogs or xenologs engaged in other specialized functions. A reliable list of orthologs with carefully ascertained functional roles has thus been assembled and should be valuable as an annotation resource. The protein domains associated with primary tryptophan biosynthesis were then concatenated, yielding single amino-acid sequence strings that represent the entire tryptophan pathway. Lateral gene transfer of several whole-pathway trp operons was demonstrated by use of phylogenetic analysis. Lateral gene transfer of partial-pathway trp operons was also shown, with newly recruited genes functioning either in primary biosynthesis (rarely) or specialized metabolism (more frequently).Conclusions(i) Concatenated tryptophan protein trees are congruent with 16S rRNA subtrees provided that the genomes represented are of sufficiently close phylogenetic spacing. There are currently seven tryptophan congruency groups in the Bacteria. Recognition of a succession of others can be expected in the near future, but ultimately these should coalesce to a single grouping that parallels the 16S rRNA tree (except for cases of lateral gene transfer). (ii) The vertical trace of evolution for tryptophan biosynthesis can be deduced. The daunting complexities engendered by paralogy, xenology, and idiosyncrasies of nomenclature at this point in time have necessitated an expert-assisted manual effort to achieve a correct analysis. Once recognized and sorted out, paralogy and xenology can be viewed as features that enrich evolutionary histories.

Highlights

The growing conviction that lateral gene transfer plays a significant role in prokaryote genealogy opens up a need for comprehensive evaluations of gene-enzyme systems on a case-by-case basis
In preliminary work with the individual protein trees corresponding to the seven catalytic domains of Trp biosynthesis, we noticed that at least seven subtree blocks on the Trp-protein trees tended to be congruent with corresponding subtree blocks of the 16S rRNA tree
The Gram-negative proteobacteria command special attention in this paper for the fortuitous reason that the greatest density of sequenced genomes is to be found in proteobacteria

Summary

Introduction

The growing conviction that lateral gene transfer plays a significant role in prokaryote genealogy opens up a need for comprehensive evaluations of gene-enzyme systems on a case-by-case basis. We have asked whether events of lateral gene transfer are sufficient to have obscured our ability to track the vertical genealogy that underpins tryptophan biosynthesis. (iii) During this time a crucial factor influencing survival will be whether the considerable demands imposed by the recipient genome for amelioration of alien genes can be met [2]. Even here a LGT insertion into a genome might be contra-selected for other reasons, for example, if the location of the insertion disrupts the symmetry and physical balance between the origin and terminus points of replication [3]. There is a balance in that one can expect alien sources of greatest novelty to be phylogenetically distant, yet genes from such remote sources will usually confront the greatest amelioration pressures. The most obvious candidates as successfully imported alien genes will encode novel functions that confer clear selective value, such as resistance to threatening environmental agents (e.g. antibiotics) or ability to utilize a new source of carbon and energy

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