Global extent of horizontal gene transfer

Horizontal gene transfer (HGT) is thought to play an important role in the evolution of species and innovation of genomes. There have been many convincing evidences for HGT for specific genes or gene families, but there has been no estimate of the global extent of HGT. Here, we present a method of identifying HGT events within a given protein family and estimate the global extent of HGT in all curated protein domain families ( approximately 8,000) listed in the Pfam database. The results suggest four conclusions: (i) for all protein domain families in Pfam, the fixation of genes horizontally transferred is not a rampant phenomenon between organisms with substantial phylogenetic separations (1.1-9.7% of Pfam families surveyed at three taxonomic ranges studied show indication of HGT); (ii) however, at the level of domains, >50% of Archaea have one or more protein domains acquired by HGT, and nearly 30-50% of Bacteria did the same when examined at three taxonomic ranges. But, the equivalent value for Eukarya is <10%; (iii) HGT will have very little impact in the construction of organism phylogeny, when the construction methods use whole genomes, large numbers of common genes, or SSU rRNAs; and (iv) there appears to be no strong preference of HGT for protein families of particular cellular or molecular functions.     

Mobile genetic elements of the human gastrointestinal tract

The human intestine is an important location for horizontal gene transfer (HGT) due to the presence of a densely populated community of microorganisms which are essential to the health of the human superorganism. HGT in this niche has the potential to influence the evolution of members of this microbial community and to mediate the spread of antibiotic resistance genes from commensal organisms to potential pathogens. Recent culture-independent techniques and metagenomic studies have provided an insight into the distribution of mobile genetic elements (MGEs) and the extent of HGT in the human gastrointestinal tract. In this mini-review, we explore the current knowledge of mobile genetic elements in the gastrointestinal tract, the progress of research into the distribution of antibiotic resistance genes in the gut and the potential role of MGEs in the spread of antibiotic resistance. In the face of reduced treatment options for many clinical infections, understanding environmental and commensal antibiotic resistance and spread is critical to the future development of meaningful and long lasting anti-microbial therapies.     

Decoding the genomic tree of life

Genomes hold within them the record of the evolution of life on Earth. But genome fusions and horizontal gene transfer (HGT) seem to have obscured sufficiently the gene sequence record such that it is difficult to reconstruct the phylogenetic tree of life. HGT among prokaryotes is not random, however. Some genes (informational genes) are more difficult to transfer than others (operational genes). Furthermore, environmental, metabolic, and genetic differences among organisms restrict HGT, so that prokaryotes preferentially share genes with other prokaryotes having properties in common, including genome size, genome G+C composition, carbon utilization, oxygen utilization/sensitivity, and temperature optima, further complicating attempts to reconstruct the tree of life. A new method of phylogenetic reconstruction based on gene presence and absence, called conditioned reconstruction, has improved our prospects for reconstructing prokaryotic evolution. It is also able to detect past genome fusions, such as the fusion that appears to have created the first eukaryote. This genome fusion between a deep branching eubacterium, possibly an ancestor of the cyanobacterium and a proteobacterium, with an archaeal eocyte (crenarchaea), appears to be the result of an early symbiosis. Given new tools and new genes from relevant organisms, it should soon be possible to test current and future fusion theories for the origin of eukaryotes and to discover the general outlines of the prokaryotic tree of life.     

Amplification of an ancestral mammalian L1 family of long interspersed repeated DNA occurred just before the murine radiation.

Each mammalian genus examined so far contains 50,000-100,000 members of an L1 (LINE 1) family of long interspersed repeated DNA elements. Current knowledge on the evolution of L1 families presents a paradox because, although L1 families have been in mammalian genomes since before the mammalian radiation approximately 80 million years ago, most members of the L1 families are only a few million years old. Accordingly it has been suggested either that the extensive amplification that characterizes present-day L1 families did not occur in the past or that old members were removed as new ones were generated. However, we show here that an ancestral rodent L1 family was extensively amplified approximately 10 million years ago and that the relics (approximately 60,000 copies) of this amplification have persisted in modern murine genomes (Old World rats and mice). This amplification occurred just before the divergence of modern murine genera from their common ancestor and identifies the murine node in the lineage of modern muroid rodents. Our results suggest that repeated amplification of L1 elements is a feature of the evolution of mammalian genomes and that ancestral amplification events could provide a useful tool for determining mammalian lineages.     

The impact of long-distance horizontal gene transfer on prokaryotic genome size

Horizontal gene transfer (HGT) is one of the most dominant forces molding prokaryotic gene repertoires. These repertoires can be as small as ≈200 genes in intracellular organisms or as large as ≈9,000 genes in large, free-living bacteria. In this article we ask what is the impact of HGT from phylogenetically distant sources, relative to the size of the gene repertoire. Using different approaches for HGT detection and focusing on both cumulative and recent evolutionary histories, we find a surprising pattern of nonlinear enrichment of long-distance transfers in large genomes. Moreover, we find a strong positive correlation between the sizes of the donor and recipient genomes. Our results also show that distant horizontal transfers are biased toward those functional groups that are enriched in large genomes, showing that the trends in functional gene content and the impact of distant transfers are interdependent. These results highlight the intimate relationship between environmental and genomic complexity in microbes and suggest that an ecological, as opposed to phylogenetic, signal in gene content gains relative importance in large-genomed bacteria.     

Biased gene transfer mimics patterns created through shared ancestry

In phylogenetic reconstruction, two types of bacterial tyrosyl-tRNA synthetases (TyrRS) form distinct clades with many bacterial phyla represented in both clades. Very few taxa possess both forms, and maximum likelihood analysis of the distribution of TyrRS types suggests horizontal gene transfer (HGT), rather than an ancient duplication followed by differential gene loss, as the contributor to the evolutionary history of TyrRS in bacteria. However, for each TyrRS type, phylogenetic reconstruction yields phylogenies similar to the ribosomal phylogeny, revealing that frequent gene transfer has not destroyed the expected phylogeny; rather, the expected phylogenetic signal was reinforced or even created by HGT. We show that biased HGT can mimic patterns created through shared ancestry by in silico simulation. Furthermore, in cases where genomic synteny is sufficient to allow comparisons of relative gene positions, both tyrRS types occupy equivalent positions in closely related genomes, rejecting the loss hypothesis. Although the two types of bacterial TyrRS are only distantly related and only rarely coexist in a single genome, they have many features in common with alleles that are swapped between related lineages. We propose to label these functionally similar homologs as homeoalleles. We conclude that the observed phylogenetic pattern reflects both vertical inheritance and biased HGT and that the signal caused by common organismal descent is difficult to distinguish from the signal due to biased gene transfer.     

Elevated evolutionary rates in the laboratory strain of Saccharomyces cerevisiae

By using the maximum likelihood method, we made a genome-wide comparison of the evolutionary rates in the lineages leading to the laboratory strain (S288c) and a wild strain (YJM789) of Saccharomyces cerevisiae and found that genes in the laboratory strain tend to evolve faster than in the wild strain. The pattern of elevated evolution suggests that relaxation of selection intensity is the dominant underlying reason, which is consistent with recurrent bottlenecks in the S. cerevisiae laboratory strain population. Supporting this conclusion are the following observations: (i) the increases in nonsynonymous evolutionary rate occur for genes in all functional categories; (ii) most of the synonymous evolutionary rate increases in S288c occur in genes with strong codon usage bias; (iii) genes under stronger negative selection have a larger increase in nonsynonymous evolutionary rate; and (iv) more genes with adaptive evolution were detected in the laboratory strain, but they do not account for the majority of the increased evolution. The present discoveries suggest that experimental and possible industrial manipulations of the laboratory strain of yeast could have had a strong effect on the genetic makeup of this model organism. Furthermore, they imply an evolution of laboratory model organisms away from their wild counterparts, questioning the relevancy of the models especially when extensive laboratory cultivation has occurred. In addition, these results shed light on the evolution of livestock and crop species that have been under human domestication for years.     

Phylogeny from function: evidence from the molecular fossil record that tRNA originated in replication, not translation.

We propose a phylogeny for the evolution of tRNA that is based on the ubiquity and conservation of tRNA-like structures in the replication of contemporary genomes. This phylogeny is unique in suggesting that the function of tRNA in replication dates back to the very beginnings of life on earth, before the advent of templated protein synthesis. The origin we propose for tRNA has distinct implications for the order in which other components of the modern translational apparatus evolved. We further suggest that the "top half" of modern tRNA-a coaxial stack of the acceptor stem on the T psi C arm--is the ancient structural and functional domain and that the "bottom half" of tRNA--a coaxial stack of the dihydrouracil arm on the anticodon arm--arose later to provide additional specificity.     

Recurrent invasion and extinction of a selfish gene

Homing endonuclease genes show super-Mendelian inheritance, which allows them to spread in populations even when they are of no benefit to the host organism. To test the idea that regular horizontal transmission is necessary for the long-term persistence of these genes, we surveyed 20 species of yeasts for the omega-homing endonuclease gene and associated group I intron. The status of omega could be categorized into three states (functional, nonfunctional, or absent), and status was not clustered on the host phylogeny. Moreover, the phylogeny of omega differed significantly from that of the host, strong evidence of horizontal transmission. Further analyses indicate that horizontal transmission is more common than transposition, and that it occurs preferentially between closely related species. Parsimony analysis and coalescent theory suggest that there have been 15 horizontal transmission events in the ancestry of our yeast species, through simulations indicate that this value is probably an underestimate. Overall, the data support a cyclical model of invasion, degeneration, and loss, followed by reinvasion, and each of these transitions is estimated to occur about once every 2 million years. The data are thus consistent with the idea that frequent horizontal transmission is necessary for the long-term persistence of homing endonuclease genes, and further, that this requirement limits these genes to organisms with easily accessible germ lines. The data also show that mitochondrial DNA sequences are transferred intact between yeast species; if other genes do not show such high levels of horizontal transmission, it would be due to lack of selection, rather than lack of opportunity.     

Molecular phylogenetic analysis of evolutionary trends in stonefly wing structure and locomotor behavior

Insects in the order Plecoptera (stoneflies) use a form of two-dimensional aerodynamic locomotion called surface skimming to move across water surfaces. Because their weight is supported by water, skimmers can achieve effective aerodynamic locomotion even with small wings and weak flight muscles. These mechanical features stimulated the hypothesis that surface skimming may have been an intermediate stage in the evolution of insect flight, which has perhaps been retained in certain modern stoneflies. Here we present a phylogeny of Plecoptera based on nucleotide sequence data from the small subunit rRNA (18S) gene. By mapping locomotor behavior and wing structural data onto the phylogeny, we distinguish between the competing hypotheses that skimming is a retained ancestral trait or, alternatively, a relatively recent loss of flight. Our results show that basal stoneflies are surface skimmers, and that various forms of surface skimming are distributed widely across the plecopteran phylogeny. Stonefly wings show evolutionary trends in the number of cross veins and the thickness of the cuticle of the longitudinal veins that are consistent with elaboration and diversification of flight-related traits. These data support the hypothesis that the first stoneflies were surface skimmers, and that wing structures important for aerial flight have become elaborated and more diverse during the radiation of modern stoneflies.     

Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium).

Polyploidy is a prominent process in plant evolution; yet few data address the question of whether homeologous sequences evolve independently subsequent to polyploidization. We report on ribosomal DNA (rDNA) evolution in five allopolyploid (AD genome) species of cotton (Gossypium) and species representing their diploid progenitors (A genome, D genome). Sequence data from the internal transcribed spacer regions (ITS1 and ITS2) and the 5.8S gene indicate that rDNA arrays are homogeneous, or nearly so, in all diploids and allopolyploids examined. Because these arrays occur at four chromosomal loci in allopolyploid cotton, two in each subgenome, repeats from different arrays must have become homogenized by interlocus concerted evolution. Southern hybridization analysis combined with copy-number estimation demonstrate that this process has gone to completion in the diploids and to completion or near-completion in all allopolyploid species and that it most likely involves the entire rDNA repeat. Phylogenetic analysis demonstrates that interlocus concerted evolution has been bidirectional in allopolyploid species--i.e., rDNA from four polyploid lineages has been homogenized to a D genome repeat type, whereas sequences from Gossypium mustelinum have concerted to an A genome repeat type. Although little is known regarding the functional significance of interlocus concerted evolution of homeologous sequences, this study demonstrates that the process occurs for tandemly repeated sequences in diploid and polyploid plants. That interlocus concerted evolution can occur bidirectionally subsequent to hybidization and polyploidization has significant implications for phylogeny reconstruction, especially when based on rDNA sequences.     

The Sahara as a vicariant agent,and the role of Miocene climatic events,in the diversification of the mammalian order Macroscelidea (elephant shrews)

Although the Sahara is a major geographical feature of the African continent, its role in the diversification of animal species is not well understood. We present here a molecular phylogeny for members of the endemic African mammalian order Macroscelidea (elephant shrews) with molecular-clock calculations; this molecular phylogeny provides convincing evidence that the genus Elephantulus is diphyletic. Elephantulus rozeti, the only elephant shrew species that resides north of the Sahara, is the sister group of a species from a different genus (Petrodromus tetradactylus), which resides just south of the Sahara. The split between these taxa coincided with major Miocene climatic events, which triggered the cooling and aridification of midlatitude continental regions, and a shift in the Sahara from a tropical to an arid environment. Thus, the North African distribution of E. rozeti is not the result of dispersion from an eastern species of the genus, but instead the result of a vicariant event involving the formation of the Sahara. The splitting events involved with most Elephantulus species in our analysis appear to coincide with these climatic events. This coincidence suggests that the environmental consequences associated with this period played an important role in the radiation of this order of mammals. The strongly supported phylogeny provides compelling evidence for a complex history of mosaic evolution, including pronounced bradytelic morphological evolution in some lineages, accelerated morphological evolution in others, and a remarkably slow rate of evolution of the male reproductive structure.     

Molecular phylogenetic evidence for the independent evolutionary origin of an arthropod compound eye

Eyes often take a central role in discussions of evolution, with debate focused on how often such complex organs might have evolved. One such debate is whether arthropod compound eyes are the product of single or multiple origins. Here we use molecular phylogeny to address this long-standing debate and find results favoring the multiple-origins hypothesis. Our analyses of DNA sequences encoding rRNA unequivocally indicate that myodocopids--the only Ostracoda (Crustacea) with compound eyes--are nested phylogenetically within several groups that lack compound eyes. With our well-supported phylogeny, standard maximum likelihood (ML) character reconstruction methods significantly reconstruct ancestral ostracods as lacking compound eyes. We also introduce a likelihood sensitivity analysis, and show that the single-origin hypothesis is not significantly favored unless we assume a highly asymmetric model of evolution (one favoring eye loss more than 30:1 over gain). These results illustrate exactly why arthropod compound eye evolution has remained controversial, because one of two seemingly very unlikely evolutionary histories must be true. Either compound eyes with detailed similarities evolved multiple times in different arthropod groups or compound eyes have been lost in a seemingly inordinate number of arthropod lineages.     

Adaptive horizontal transfer of a bacterial gene to an invasive insect pest of coffee

Horizontal gene transfer (HGT) involves the nonsexual transmission of genetic material across species boundaries. Although often detected in prokaryotes, examples of HGT involving animals are relatively rare, and any evolutionary advantage conferred to the recipient is typically obscure. We identified a gene (HhMAN1) from the coffee berry borer beetle, Hypothenemus hampei, a devastating pest of coffee, which shows clear evidence of HGT from bacteria. HhMAN1 encodes a mannanase, representing a class of glycosyl hydrolases that has not previously been reported in insects. Recombinant HhMAN1 protein hydrolyzes coffee berry galactomannan, the major storage polysaccharide in this species and the presumed food of H. hampei. HhMAN1 was found to be widespread in a broad biogeographic survey of H. hampei accessions, indicating that the HGT event occurred before radiation of the insect from West Africa to Asia and South America. However, the gene was not detected in the closely related species H. obscurus (the tropical nut borer or "false berry borer"), which does not colonize coffee beans. Thus, HGT of HhMAN1 from bacteria represents a likely adaptation to a specific ecological niche and may have been promoted by intensive agricultural practices.     

Dynamic patterns of adaptive radiation

Adaptive radiation is defined as the evolution of ecological and phenotypic diversity within a rapidly multiplying lineage. When it occurs, adaptive radiation typically follows the colonization of a new environment or the establishment of a "key innovation," which opens new ecological niches and/or new paths for evolution. Here, we take advantage of recent developments in speciation theory and modern computing power to build and explore a large-scale, stochastic, spatially explicit, individual-based model of adaptive radiation driven by adaptation to multidimensional ecological niches. We are able to model evolutionary dynamics of populations with hundreds of thousands of sexual diploid individuals over a time span of 100,000 generations assuming realistic mutation rates and allowing for genetic variation in a large number of both selected and neutral loci. Our results provide theoretical support and explanation for a number of empirical patterns including "area effect," "overshooting effect," and "least action effect," as well as for the idea of a "porous genome." Our findings suggest that the genetic architecture of traits involved in the most spectacular radiations might be rather simple. We show that a great majority of speciation events are concentrated early in the phylogeny. Our results emphasize the importance of ecological opportunity and genetic constraints in controlling the dynamics of adaptive radiation.     

On the evolution of cells

A theory for the evolution of cellular organization is presented. The model is based on the (data supported) conjecture that the dynamic of horizontal gene transfer (HGT) is primarily determined by the organization of the recipient cell. Aboriginal cell designs are taken to be simple and loosely organized enough that all cellular componentry can be altered and/or displaced through HGT, making HGT the principal driving force in early cellular evolution. Primitive cells did not carry a stable organismal genealogical trace. Primitive cellular evolution is basically communal. The high level of novelty required to evolve cell designs is a product of communal invention, of the universal HGT field, not intralineage variation. It is the community as a whole, the ecosystem, which evolves. The individual cell designs that evolved in this way are nevertheless fundamentally distinct, because the initial conditions in each case are somewhat different. As a cell design becomes more complex and interconnected a critical point is reached where a more integrated cellular organization emerges, and vertically generated novelty can and does assume greater importance. This critical point is called the "Darwinian Threshold" for the reasons given.     

The rise of the ants: a phylogenetic and ecological explanation

In the past two decades, studies of anatomy, behavior, and, most recently, DNA sequences have clarified the phylogeny of the ants at the subfamily and generic levels. In addition, a rich new harvest of Cretaceous and Paleogene fossils has helped to date the major evolutionary radiations. We collate this information and then add data from the natural history of the modern fauna to sketch a history of major ecological adaptations at the subfamily level. The key events appear to have been, first, a mid-Cretaceous initial radiation in forest ground litter and soil coincident with the rise of the angiosperms (flowering plants), then a Paleogene advance to ecological dominance in concert with that of the angiosperms in tropical forests, and, finally, an expansion of some of the lineages, aided by changes in diet away from dependence on predation, upward into the canopy, and outward into more xeric environments.     

From the Cover: Evidence for an ancient adaptive episode of convergent molecular evolution

Documented cases of convergent molecular evolution due to selection are fairly unusual, and examples to date have involved only a few amino acid positions. However, because convergence mimics shared ancestry and is not accommodated by current phylogenetic methods, it can strongly mislead phylogenetic inference when it does occur. Here, we present a case of extensive convergent molecular evolution between snake and agamid lizard mitochondrial genomes that overcomes an otherwise strong phylogenetic signal. Evidence from morphology, nuclear genes, and most sites in the mitochondrial genome support one phylogenetic tree, but a subset of mostly amino acid-altering substitutions (primarily at the first and second codon positions) across multiple mitochondrial genes strongly supports a radically different phylogeny. The relevant sites generally evolved slowly but converged between ancient lineages of snakes and agamids. We estimate that ≈44 of 113 predicted convergent changes distributed across all 13 mitochondrial protein-coding genes are expected to have arisen from nonneutral causes—a remarkably large number. Combined with strong previous evidence for adaptive evolution in snake mitochondrial proteins, it is likely that much of this convergent evolution was driven by adaptation. These results indicate that nonneutral convergent molecular evolution in mitochondria can occur at a scale and intensity far beyond what has been documented previously, and they highlight the vulnerability of standard phylogenetic methods to the presence of nonneutral convergent sequence evolution.     

Thinking in three's: Changing surgical patient safety practices in the complex modern operating room

The three surgical patient safety events, wrong site surgery, retained surgical items (RSI) and surgical fires are rare occurrences and thus their effects on the complex modern operating room (OR) are difficult to study. The likelihood of occurrence and the magnitude of risk for each of these surgical safety events are undefined. Many providers may never have a personal experience with one of these events and training and education on these topics are sparse. These circumstances lead to faulty thinking that a provider won’t ever have an event or if one does occur the provider will intuitively know what to do. Surgeons are not preoccupied with failure and tend to usually consider good outcomes, which leads them to ignore or diminish the importance of implementing and following simple safety practices. These circumstances contribute to the persistent low level occurrence of these three events and to the difficulty in generating sufficient interest to resource solutions. Individual facilities rarely have the time or talent to understand these events and develop lasting solutions. More often than not, even the most well meaning internal review results in a new line to a policy and some rigorous enforcement mandate. This approach routinely fails and is another reason why these problems are so persistent. Vigilance actions alone have been unsuccessful so hospitals now have to take a systematic approach to implementing safer processes and providing the resources for surgeons and other stakeholders to optimize the OR environment. This article discusses standardized processes of care for mitigation of injury or outright prevention of wrong site surgery, RSI and surgical fires in an action-oriented framework illustrating the strategic elements important in each event and focusing on the responsibilities for each of the three major OR agents-anesthesiologists, surgeons and nurses. A Surgical Patient Safety Checklist is discussed that incorporates the necessary elements to bring these team members together and influence the emergence of a safer OR.