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

BMC Biology Inter-genomic displacement via lateral gene transfer of bacterial trp operons in an overall context of vertical genealogy Gary Xie 1 Carol A Bonner 0 Jian Song 1 Nemat O Keyhani 0 Roy A Jensen 0 1 0 Department of Microbiology & Cell Science, University of Florida , PO Box 110700, Gainesville, Florida, 32611 , USA 1 Los Alamos National Laboratory , Los Alamos, New Mexico, 87544 , USA Background: 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. 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. Results: In 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. - Background The process of LGT Lateral gene transfer (LGT) undoubtedly occurs with high frequency [1]. But what is required for any given LGT event to escape transience and actually survive as a nonvertical contributor to the evolutionary history of a species? (i) Initially the incoming gene(s) must be replicated in the original recipient cell and its immediate progeny. (ii) Selective advantages of the LGT-gene(s) must be sufficient to foster eventual domination of the species population. (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]. Obviously, there will be less amelioration pressure if the donor and recipient genomes are phylogenetically close and have similar guanine/cytosine base ratios, dinucleotide frequencies, promotor motifs, and so on. 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. Enhanced probability of LGT success can be expected if only a single gene is needed for the novel function. This does not necessarily rule out the acquisition of a new function that is complex and multi-genic. Sometimes where existing functions are complex and multi-step, a single incoming gene can create a new metabolic linkage. For example, an organism having a multi-step pathway for tyrosine catabolism could acquire a previously unavailable ability to also catabolize phenylalanine through import of a gene encoding phenylalanine hydroxylase (which converts phenylalanine to tyrosine). In cases where the total repertoire of multiple steps that define a novel function are all absent in a given organism, acquisition of that function by LGT would be highly improbable were it not for the existence of operon modules in prokaryotes. Lawrence has proposed, in fact, that gene organization as operons largely exists because of "selfish" properties that operate at the hierarchical level of genes [4,5]. Although genes of L-tryptophan (Trp) biosynthesis, a classic operon system, are completely dispersed in some prokaryote genomes (e.g. Aquifex, Chlorobium, Wolinella and unicellular cyanobacteria such as Synechococcus, Synechocystis, and Prochlorococcus), they usually exist either as whole-pathway operons or as a combination of several partial-pathway operons [6]. Approaches for the detection of LGT events are either phylogenetic or parametric. Parametric approaches include the detection of nucleotide composition, dinucleotide frequencies and codon-usage biases in gene segments that are atypical of the recipient genome. Such parametric analysis is well illustrated by a study of the Escherichia coli genome [1]. However, such atypical parametric properties will drift with time toward those of the recipient genome (amelioration). Therefore, parametric analysis is limited to detection of genes that were acquired recently. We have found only a single example where trp genes exhibited parametric features suggesting LGT. In this case a low-GC gene block in Xylella fastidiosa contains seven genes, of which two encode the subunits of anthranilate synthase and one encodes a repressor, TrpR [7]. On the other hand, phylogenetic analysis can detect ancient events of LGT, and this approach has allowed the recognition of a number of whole-pathway and partial-pathway trp operons that were acquired by LGT. Presumably, the initial aberrant parametric properties associated with LGT have been ameliorated. Phylogenetic analysis also is a much more powerful indicator of the likely donor lineage following gene acquisition by LGT. En bloc importation of primary pathways via LGT Ubiquitous pathways of primary biosynthesis, having a long (...truncated)