Horizontal gene transfer in microbial genome evolution

Horizontal gene transfer is the collective name for processes that permit the exchange of DNA among organisms of different species. Only recently has it been recognized as a significant contribution to inter-organismal gene exchange. Traditionally, it was thought that microorganisms evolved clonally, passing genes from mother to daughter cells with little or no exchange of DNA among diverse species. Studies of microbial genomes, however, have shown that genomes contain genes that are closely related to a number of different prokaryotes, sometimes to phylogenetically very distantly related ones. (Doolittle et al., 1990, J. Mol. Evol. 31, 383-388; Karlin et al., 1997, J. Bacteriol. 179, 3899-3913; Karlin et al., 1998, Annu. Rev. Genet. 32, 185-225; Lawrence and Ochman, 1998, Proc. Natl. Acad. Sci. USA 95, 9413-9417; Rivera et al., 1998, Proc. Natl. Acad. Sci. USA 95, 6239-6244; Campbell, 2000, Theor. Popul. Biol. 57 71-77; Doolittle, 2000, Sci. Am. 282, 90-95; Ochman and Jones, 2000, Embo. J. 19, 6637-6643; Boucher et al. 2001, Curr. Opin., Microbiol. 4, 285-289; Wang et al., 2001, Mol. Biol. Evol. 18, 792-800). Whereas prokaryotic and eukaryotic evolution was once reconstructed from a single 16S ribosomal RNA (rRNA) gene, the analysis of complete genomes is beginning to yield a different picture of microbial evolution, one that is wrought with the lateral movement of genes across vast phylogenetic distances. (Lane et al., 1988, Methods Enzymol. 167, 138-144; Lake and Rivera, 1996, Proc. Natl. Acad. Sci. USA 91, 2880-2881; Lake et al., 1999, Science 283, 2027-2028).     

Interspecific evolution: microbial symbiosis,endosymbiosis and gene transfer

Microbial symbioses are interesting in their own right and also serve as exemplary models to help biologists to understand two important symbioses in the evolutionary past of eukaryotic cells: the origins of chloroplasts and mitochondria. Most, if not all, microbial symbioses have a chemical basis: compounds produced by one partner are useful for the other. But symbioses can also entail the transfer of genes from one partner to the other, which in some cases cements two cells into a bipartite, co-evolving unit. Here, we discuss some microbial symbioses in which progress is being made in uncovering the nature of symbiotic interactions: anaerobic methane-oxidizing consortia, marine worms that possess endosymbionts instead of a digestive tract, amino acid-producing endosymbionts of aphids, prokaryotic endosymbionts living within a prokaryotic host within mealybugs, endosymbionts of an insect vector of human disease and a photosynthetic sea slug that steals chloroplasts from algae. In the case of chloroplasts and mitochondria, examples of recent and ancient gene transfer to the chromosomes of their host cell illustrate the process of genetic merger in the wake of organelle origins.     

Biased gene conversion: implications for genome and sex evolution

Classical genetic studies show that gene conversion can favour some alleles over others. Molecular experiments suggest that gene conversion could favour GC over AT basepairs, leading to the concept of biased gene conversion towards GC (BGC(GC)). The expected consequence of such a process is the GC-enrichment of DNA sequences under gene conversion. Recent genomic work suggests that BGC(GC) affects the base composition of yeast, invertebrate and mammalian genomes. Hypotheses for the mechanisms and evolutionary origin of such a strange phenomenon have been proposed. Most BGC(GC) events probably occur during meiosis, which has implications for our understanding of the evolution of sex and recombination.     

Horizontal gene transfer in eukaryotic evolution

Horizontal gene transfer (HGT; also known as lateral gene transfer) has had an important role in eukaryotic genome evolution, but its importance is often overshadowed by the greater prevalence and our more advanced understanding of gene transfer in prokaryotes. Recurrent endosymbioses and the generally poor sampling of most nuclear genes from diverse lineages have also complicated the search for transferred genes. Nevertheless, the number of well-supported cases of transfer from both prokaryotes and eukaryotes, many with significant functional implications, is now expanding rapidly. Major recent trends include the important role of HGT in adaptation to certain specialized niches and the highly variable impact of HGT in different lineages.     

Prokaryotic evolution in light of gene transfer

Accumulating prokaryotic gene and genome sequences reveal that the exchange of genetic information through both homology-dependent recombination and horizontal (lateral) gene transfer (HGT) is far more important, in quantity and quality, than hitherto imagined. The traditional view, that prokaryotic evolution can be understood primarily in terms of clonal divergence and periodic selection, must be augmented to embrace gene exchange as a creative force, itself responsible for much of the pattern of similarities and differences we see between prokaryotic microbes. Rather than replacing periodic selection on genetic diversity, gene loss, and other chromosomal alterations as important players in adaptive evolution, gene exchange acts in concert with these processes to provide a rich explanatory paradigm-some of whose implications we explore here. In particular, we discuss (1) the role of recombination and HGT in giving phenotypic "coherence" to prokaryotic taxa at all levels of inclusiveness, (2) the implications of these processes for the reconstruction and meaning of "phylogeny," and (3) new views of prokaryotic adaptation and diversification based on gene acquisition and exchange.     

Detection of lateral gene transfer among microbial genomes

An increasingly comprehensive assessment is being developed of the extent and potential significance of lateral gene transfer among microbial genomes. Genomic sequences can be identified as being of putatively lateral origin by their unexpected phyletic distribution, atypical sequence composition, differential presence or absence in closely related genomes, or incongruent phylogenetic trees. These complementary approaches sometimes yield inconsistent results. Not only more data but also quantitative models and simulations are needed urgently.     

Lateral gene transfer challenges principles of microbial systematics

Evolutionists strive to learn about the natural historical process that gave rise to various taxa, while also attempting to classify them efficiently and make generalizations about them. The quantitative importance of lateral gene transfer inferred from genomic data, although well acknowledged by microbiologists, is in conflict with the conceptual foundations of the traditional phylogenetic system erected to achieve these goals. To provide a true account of microbial evolution, we suggest developing an alternative conception of natural groups and introduce a new notion--the composite evolutionary unit. Furthermore, we argue that a comprehensive database containing overlapping taxonomical groups would constitute a step forward regarding the classification of microbes in the presence of lateral gene transfer.     

Horizontal gene transfer in an acid mine drainage microbial community

Background

Horizontal gene transfer (HGT) has been widely identified in complete prokaryotic genomes. However, the roles of HGT among members of a microbial community and in evolution remain largely unknown. With the emergence of metagenomics, it is nontrivial to investigate such horizontal flow of genetic materials among members in a microbial community from the natural environment. Because of the lack of suitable methods for metagenomics gene transfer detection, microorganisms from a low-complexity community acid mine drainage (AMD) with near-complete genomes were used to detect possible gene transfer events and suggest the biological significance.

Results

Using the annotation of coding regions by the current tools, a phylogenetic approach, and an approximately unbiased test, we found that HGTs in AMD organisms are not rare, and we predicted 119 putative transferred genes. Among them, 14 HGT events were determined to be transfer events among the AMD members. Further analysis of the 14 transferred genes revealed that the HGT events affected the functional evolution of archaea or bacteria in AMD, and it probably shaped the community structure, such as the dominance of G-plasma in archaea in AMD through HGT.

Conclusions

Our study provides a novel insight into HGT events among microorganisms in natural communities. The interconnectedness between HGT and community evolution is essential to understand microbial community formation and development.

Electronic supplementary material

The online version of this article (doi:10.1186/s12864-015-1720-0) contains supplementary material, which is available to authorized users.     

Endosymbiotic evolution: RNA intermediates in endosymbiotic gene transfer

More than a billion years of endosymbiotic evolution has resulted in extensive gene relocation between the genetic compartments of eukaryotic cells. A new study uses chloroplast genome transformation to shed light on the mechanisms involved.     

Functional biogeography as evidence of gene transfer in hypersaline microbial communities

Background

Horizontal gene transfer (HGT) plays a major role in speciation and evolution of bacteria and archaea by controlling gene distribution within an environment. However, information that links HGT to a natural community using relevant population-genetics parameters and spatial considerations is scarce. The Great Salt Lake (Utah, USA) provides an excellent model for studying HGT in the context of biogeography because it is a contiguous system with dispersal limitations due to a strong selective salinity gradient. We hypothesize that in spite of the barrier to phylogenetic dispersal, functional characteristics—in the form of HGT—expand beyond phylogenetic limitations due to selective pressure.

Methodology and Results

To assay the functional genes and microorganisms throughout the GSL, we used a 16S rRNA oligonucleotide microarray (Phylochip) and a functional gene array (GeoChip) to measure biogeographic patterns of nine microbial communities. We found a significant difference in biogeography based on microarray analyses when comparing Sørensen similarity values for presence/absence of function and phylogeny (Student''s t-test; p = 0.005).

Conclusion and Significance

Biogeographic patterns exhibit behavior associated with horizontal gene transfer in that informational genes (16S rRNA) have a lower similarity than functional genes, and functional similarity is positively correlated with lake-wide selective pressure. Specifically, high concentrations of chromium throughout GSL correspond to an average similarity of chromium resistance genes that is 22% higher than taxonomic similarity. This suggests active HGT may be measured at the population level in microbial communities and these biogeographic patterns may serve as a model to study bacteria adaptation and speciation.     

Horizontal gene transfer, genome innovation and evolution

To what extent is the tree of life the best representation of the evolutionary history of microorganisms? Recent work has shown that, among sets of prokaryotic genomes in which most homologous genes show extremely low sequence divergence, gene content can vary enormously, implying that those genes that are variably present or absent are frequently horizontally transferred. Traditionally, successful horizontal gene transfer was assumed to provide a selective advantage to either the host or the gene itself, but could horizontally transferred genes be neutral or nearly neutral? We suggest that for many prokaryotes, the boundaries between species are fuzzy, and therefore the principles of population genetics must be broadened so that they can be applied to higher taxonomic categories.     

Horizontal gene transfer accelerates genome innovation and evolution

Horizontal gene transfer (HGT) spreads genetic diversity by moving genes across species boundaries. By rapidly introducing newly evolved genes into existing genomes, HGT circumvents the slow step of ab initio gene creation and accelerates genome innovation. However, HGT can only affect organisms that readily exchange genes (exchange communities). In order to define exchange communities and understand the internal and external environmental factors that regulate HGT, we analyzed approximately 20,000 genes contained in eight free-living prokaryotic genomes. These analyses indicate that HGT occurs among organisms that share similar factors. The most significant are genome size, genome G/C composition, carbon utilization, and oxygen tolerance.     

Mechanisms in microbial evolution

Molecular genetic studies with prokaryotic microorganisms reveal that many different molecular processes contribute to the formation of spontaneous mutations. Besides infidelities in DNA replication and the consequences of environmental mutagens, enzyme-mediated DNA rearrangements bring about important, evolutionarily relevant alterations in the genetic information. Particular attention is given in this article to site-specific recombination at secondary crossover sites and to the transposition of mobile genetic elements with relaxed target specificity. Besides these diverse processes of genomic mutation the acquisition of genetic information from other organisms plays an uncontested role in microbial evolution. Enzymes and organelles mediating any of these mutational processes can be looked at as biological functions acting at the level of populations for the needs of biological evolution, rather than to fulfill the needs of individual living organisms.     

Elements in microbial evolution

Spontaneous mutation, selection, and isolation are key elements in biological evolution. Molecular genetic approaches reveal a multitude of different mechanisms by which spontaneous mutants arise. Many of these mechanisms depend on enzymes, which often do not act fully at random on the DNA, although a large number of sites of action can be observed. Of particular interest in this respect are DNA rearrangement processes, e.g., by transposition and by site-specific recombination systems. The development of gene functions has thus to be seen as the result of both DNA rearrangement processes and sequence alterations brought about by nucleotide substitutions and small local deletions, insertions, and duplications. Prokaryotic microorganisms are particularly appropriate for studying the effects of spontaneous mutation and thus microbial evolution, as they have haploid genomes, so that genetic alterations become rapidly apparent phenotypically. In addition, bacteria and their viruses and plasmids have relatively small genomes and short generation times, which also facilitate research on evolutionary processes. Besides the strategy of development of gene functions in the vertical transmission of genomes from generation to generation, the acquisition of short DNA segments from other organisms appears to be an important strategy in microbial evolution. In this process of horizontal evolution natural vector DNA molecules are often involved. Because of acquisition barriers, the acquisition strategy works best for relatively small DNA segments, hence at the level of domains, single genes, or at most operons. Among the many enzymes and functional systems involved in vertical and horizontal microbial evolution, some may serve primarily for essential life functions in each individual and only secondarily contribute to evolution.(ABSTRACT TRUNCATED AT 250 WORDS)     

Ancient lateral gene transfer in the evolution of Bdellovibrio bacteriovorus

The recently sequenced genome of the predatory delta-proteobacterium Bdellovibrio bacteriovorus provides many insights into its metabolism and evolution. Because its genes are reasonably uniform in G+C content, it was suggested that B. bacteriovorus actively resists recombination with foreign DNA and horizontal transfer of DNA from other bacteria. To investigate this further, we carried out a variety of phylogenetic and comparative genomics analyses using data from >200 microbial genomes, including several published delta-proteobacteria. Although there might be little evidence for the extensive recent transfer of genes, we demonstrate that ancient lateral gene acquisition has shaped the B. bacteriovorus genome to a great extent.     

Genome-wide molecular clock and horizontal gene transfer in bacterial evolution

We describe a simple theoretical framework for identifying orthologous sets of genes that deviate from a clock-like model of evolution. The approach used is based on comparing the evolutionary distances within a set of orthologs to a standard intergenomic distance, which was defined as the median of the distribution of the distances between all one-to-one orthologs. Under the clock-like model, the points on a plot of intergenic distances versus intergenomic distances are expected to fit a straight line. A statistical technique to identify significant deviations from the clock-like behavior is described. For several hundred analyzed orthologous sets representing three well-defined bacterial lineages, the alpha-Proteobacteria, the gamma-Proteobacteria, and the Bacillus-Clostridium group, the clock-like null hypothesis could not be rejected for approximately 70% of the sets, whereas the rest showed substantial anomalies. Subsequent detailed phylogenetic analysis of the genes with the strongest deviations indicated that over one-half of these genes probably underwent a distinct form of horizontal gene transfer, xenologous gene displacement, in which a gene is displaced by an ortholog from a different lineage. The remaining deviations from the clock-like model could be explained by lineage-specific acceleration of evolution. The results indicate that although xenologous gene displacement is a major force in bacterial evolution, a significant majority of orthologous gene sets in three major bacterial lineages evolved in accordance with the clock-like model. The approach described here allows rapid detection of deviations from this mode of evolution on the genome scale.