Long Non-coding RNAs in the Human Genome Acquired by Horizontal Gene Transfer

Background: Horizontal gene transfer of mobile genetic elements is an essential component of prokaryotic evolution. These insertion events in eukaryotes and particularly in the human genome have been investigated by various methodologies with varying results. Objective: In this paper, we implement a sequence composition approach to investigate insertions of genomic islands in the human genome. Methods: A modified version of a prokaryotic GI identifier, SeqWord Gene Island Sniffer v.2.0, was used to predict genomic islands in the hg38 version of the human genome. Results: Predicted genomic islands were enriched with long non-coding RNAs and also contributed to the acquisition and modification of proteins associated with the immune system and gonad development, albeit to a lesser extent. The estimated rate of acquisition of these genomic islands in vertebrate genomes was non-linear with regards to species divergence times with an acceleration at the time of vertebrate land invasion and during the transition of prosimians to monkeys soon after the Cretaceous-Paleogene extinction. Conclusion: The rapid acquisition of non-conserved long non-coding RNAs in the human genome and probably in vertebrata genomes was facilitated by horizontal gene transfer. All predicted human genomic islands and supporting information are freely accessible from http://hislands.bi.up.ac.za.

Aerobiosis is not associated with GC content and G to T mutations are not the signature of oxidative stress in prokaryotic evolution

Background: Among the four bases, guanine is the most susceptible to damage from oxidative stress. Replication of DNA containing damaged guanines result in G to T mutations. Therefore, the mutations resulting from oxidative DNA damage are generally expected to predominantly consist of G to T (and C to A when the damaged guanine is not in the reference strand) and result in decreased GC content. However, the opposite pattern was reported 16 years ago in a study of prokaryotic genomes. Although that result has been widely cited and confirmed by nine later studies with similar methods, the omission of the effect of shared ancestry requires a re-examination of the reliability of the results.Results: We retrieved 70 aerobe-anaerobe pairs of prokaryotes, and members of each pair were adjacent on the phylogenetic tree. Pairwise comparisons of either whole-genome GC content or the GC content at 4-fold degenerate sites of orthologous genes among these 70 pairs did not show significant differences between aerobes and anaerobes. The signature of guanine oxidation on GC content evolution has not been detected even after extensive controlling of other influencing factors. Furthermore, the anaerobes were not different from the aerobes in the rate of either G to T, C to A, or other directions of substitutions. The presence of the enzymes responsible for guanine oxidation in anaerobic prokaryotes provided additional evidence that guanine oxidation might be prevalent in anaerobic prokaryotes. In either aerobes or anaerobes, the rates of G:C to T:A mutations were not significantly higher than the reverse mutations.Conclusions: The previous counterintuitive results on the relationship between oxygen requirement and GC content should be attributed to the methodological artefact resulting from phylogenetically non-independence among the analysed samples. Our results showed that aerobiosis does not increase or decrease GC content in evolution. Furthermore, our study challenged the widespread belief that abundant G:C to T:A transversions are the signature of oxidative stress in prokaryotic evolution.

Phylo SI: a new genome-wide approach for prokaryotic phylogeny

The evolutionary history of all life forms is usually represented as a vertical tree-like process. In prokaryotes, however, the vertical signal is partly obscured by the massive influence of horizontal gene transfer (HGT). The HGT creates widespread discordance between evolutionary histories of different genes as genomes become mosaics of gene histories. Thus, the Tree of Life (TOL) has been questioned as an appropriate representation of the evolution of prokaryotes. Nevertheless a common hypothesis is that prokaryotic evolution is primarily tree-like, and a routine effort is made to place new isolates in their appropriate location in the TOL. Moreover, it appears desirable to exploit non–tree-like evolutionary processes for the task of microbial classification. In this work, we present a novel technique that builds on the straightforward observation that gene order conservation (‘synteny’) decreases in time as a result of gene mobility. This is particularly true in prokaryotes, mainly due to HGT. Using a ‘synteny index’ (SI) that measures the average synteny between a pair of genomes, we developed the phylogenetic reconstruction tool ‘Phylo SI’. Phylo SI offers several attractive properties such as easy bootstrapping, high sensitivity in cases where phylogenetic signal is weak and computational efficiency. Phylo SI was tested both on simulated data and on two bacterial data sets and compared with two well-established phylogenetic methods. Phylo SI is particularly efficient on short evolutionary distances where synteny footprints remain detectable, whereas the nucleotide substitution signal is too weak for reliable sequence-based phylogenetic reconstruction. The method is publicly available at http://research.haifa.ac.il/ssagi/software/PhyloSI.zip.

Microbial evolution of sulphate reduction when lateral gene transfer is geographically restricted

Lateral gene transfer (LGT) is an important mechanism by which micro-organisms acquire new functions. This process has been suggested to be central to prokaryotic evolution in various environments. However, the influence of geographical constraints on the evolution of laterally acquired genes in microbial metabolic evolution is not yet well understood. In this study, the influence of geographical isolation on the evolution of laterally acquired dissimilatory sulphite reductase (dsr) gene sequences in the sulphate-reducing micro-organisms (SRM) was investigated. Sequences on four continental blocks related to SRM known to have received dsr by LGT were analysed using standard phylogenetic and multidimensional statistical methods. Sequences related to lineages with large genetic diversity correlated positively with habitat divergence. Those affiliated to Thermodesulfobacterium indicated strong biogeographical delineation; hydrothermal-vent sequences clustered independently from hot-spring sequences. Some of the hydrothermal-vent and hot-spring sequences suggested to have been acquired from a common ancestral source may have diverged upon isolation within distinct habitats. In contrast, analysis of some Desulfotomaculum sequences indicated they could have been transferred from different ancestral sources but converged upon isolation within the same niche. These results hint that, after lateral acquisition of dsr genes, barriers to gene flow probably play a strong role in their subsequent evolution.

Horizontal gene transfer in evolution: facts and challenges

The contribution of horizontal gene transfer to evolution has been controversial since it was suggested to be a force driving evolution in the microbial world. In this paper, I review the current standpoint on horizontal gene transfer in evolutionary thinking and discuss how important horizontal gene transfer is in evolution in the broad sense, and particularly in prokaryotic evolution. I review recent literature, asking, first, which processes are involved in the evolutionary success of transferred genes and, secondly, about the extent of horizontal gene transfer towards different evolutionary times. Moreover, I discuss the feasibility of reconstructing ancient phylogenetic relationships in the face of horizontal gene transfer. Finally, I discuss how horizontal gene transfer fits in the current neo-Darwinian evolutionary paradigm and conclude there is a need for a new evolutionary paradigm that includes horizontal gene transfer as well as other mechanisms in the explanation of evolution.

Stepping stones towards a new prokaryotic taxonomy

Technological developments provide new insights into prokaryotic evolution and diversity and provoke a continuous need to update taxonomy and revise classification schemes. Our present species concept and definition are being challenged by the growing amount of whole genomic information, which should allow improvements in the natural species definition. The continuous quest for an objective and stable method for sorting strains into coherent homogeneous groups is inherent to prokaryotic systematics and nomenclature. Morphological, biochemical, physiological, phenotypic and chemotaxonomic criteria have been complemented by molecular data and pragmatic, purpose built, species definitions are being replaced by more natural ones based on evolutionary insights. It is imperative to give due consideration to both fundamental and applied aspects of future species concepts and definitions. The present paper discusses the present practice in prokaryotic taxonomy of how this system developed and how it may evolve in the future.