Importance Of Lateral Gene Transfer Research Articles

Population Structure and Antimicrobial Resistance Profiles of Streptococcus suis Serotype 2 Sequence Type 25 Strains.

Strains of serotype 2 Streptococcus suis are responsible for swine and human infections. Different serotype 2 genetic backgrounds have been defined using multilocus sequence typing (MLST). However, little is known about the genetic diversity within each MLST sequence type (ST). Here, we used whole-genome sequencing to test the hypothesis that S. suis serotype 2 strains of the ST25 lineage are genetically heterogeneous. We evaluated 51 serotype 2 ST25 S. suis strains isolated from diseased pigs and humans in Canada, the United States of America, and Thailand. Whole-genome sequencing revealed numerous large-scale rearrangements in the ST25 genome, compared to the genomes of ST1 and ST28 S. suis strains, which result, among other changes, in disruption of a pilus island locus. We report that recombination and lateral gene transfer contribute to ST25 genetic diversity. Phylogenetic analysis identified two main and distinct Thai and North American clades grouping most strains investigated. These clades also possessed distinct patterns of antimicrobial resistance genes, which correlated with acquisition of different integrative and conjugative elements (ICEs). Some of these ICEs were found to be integrated at a recombination hot spot, previously identified as the site of integration of the 89K pathogenicity island in serotype 2 ST7 S. suis strains. Our results highlight the limitations of MLST for phylogenetic analysis of S. suis, and the importance of lateral gene transfer and recombination as drivers of diversity in this swine pathogen and zoonotic agent.

Horizontal Gene Transfers from Bacteria to Entamoeba Complex: A Strategy for Dating Events along Species Divergence.

Horizontal gene transfer has proved to be relevant in eukaryotic evolution, as it has been found more often than expected and related to adaptation to certain niches. A relatively large list of laterally transferred genes has been proposed and evaluated for the parasite Entamoeba histolytica. The goals of this work were to elucidate the importance of lateral gene transfer along the evolutionary history of some members of the genus Entamoeba, through identifying donor groups and estimating the divergence time of some of these events. In order to estimate the divergence time of some of the horizontal gene transfer events, the dating of some Entamoeba species was necessary, following an indirect dating strategy based on the fossil record of plausible hosts. The divergence between E. histolytica and E. nuttallii probably occurred 5.93 million years ago (Mya); this lineage diverged from E. dispar 9.97 Mya, while the ancestor of the latter separated from E. invadens 68.18 Mya. We estimated times for 22 transferences; the most recent occurred 31.45 Mya and the oldest 253.59 Mya. Indeed, the acquisition of genes through lateral transfer may have triggered a period of adaptive radiation, thus playing a major role in the evolution of the Entamoeba genus.

The Singular Quest for a Universal Tree of Life

Carl Woese developed a unique research program, based on rRNA, for discerning bacterial relationships and constructing a universal tree of life. Woese's interest in the evolution of the genetic code led to him to investigate the deep roots of evolution, develop the concept of the progenote, and conceive of the Archaea. In so doing, he and his colleagues at the University of Illinois in Urbana revolutionized microbiology and brought the classification of microbes into an evolutionary framework. Woese also provided definitive evidence for the role of symbiosis in the evolution of the eukaryotic cell while underscoring the importance of lateral gene transfer in microbial evolution. Woese and colleagues' proposal of three fundamental domains of life was brought forward in direct conflict with the prokaryote-eukaryote dichotomy. Together with several colleagues and associates, he brought together diverse evidence to support the rRNA evidence for the fundamentally tripartite nature of life. This paper aims to provide insight into his accomplishments, how he achieved them, and his place in the history of biology.

Multi‐locus sequence analysis, taxonomic resolution and biogeography of marine Synechococcus

Conserved markers such as the 16S rRNA gene do not provide sufficient molecular resolution to identify spatially structured populations of marine Synechococcus, or 'ecotypes' adapted to distinct ecological niches. Multi-locus sequence analysis targeting seven 'core' genes was employed to taxonomically resolve Synechococcus isolates and correlate previous phylogenetic analyses encompassing a range of markers. Despite the recognized importance of lateral gene transfer in shaping the genomes of marine cyanobacteria, multi-locus sequence analysis of more than 120 isolates reflects a clonal population structure of major lineages and subgroups. A single core genome locus, petB, encoding the cytochrome b(6) subunit of the cytochrome b(6) f complex, was selected to expand our understanding of the diversity and ecology of marine Synechococcus populations. Environmental petB sequences cloned from contrasting sites highlight numerous genetically and ecologically distinct clusters, some of which represent novel, environmentally abundant clades without cultured representatives. With a view to scaling ecological analyses, the short sequence, taxonomic resolution and accurate automated alignment of petB is ideally suited to high-throughput and high-resolution sequencing projects to explore links between the ecology, evolution and biology of marine Synechococcus.

Comparative genomics and the role of lateral gene transfer in the evolution of bovine adapted Streptococcus agalactiae

In addition to causing severe invasive infections in humans, Streptococcus agalactiae, or group B Streptococcus (GBS), is also a major cause of bovine mastitis. Here we provide the first genome sequence for S. agalactiae isolated from a cow diagnosed with clinical mastitis (strain FSL S3-026). Comparison to eight S. agalactiae genomes obtained from human disease isolates revealed 183 genes specific to the bovine strain. Subsequent polymerase chain reaction (PCR) screening for the presence/absence of a subset of these loci in additional bovine and human strains revealed strong differentiation between the two groups (Fisher exact test: p<0.0001). The majority of the bovine strain-specific genes (∼85%) clustered tightly into eight genomic islands, suggesting these genes were acquired through lateral gene transfer (LGT). This bovine GBS also contained an unusually high proportion of insertion sequences (4.3% of the total genome), suggesting frequent genomic rearrangement. Comparison to other mastitis-causing species of bacteria provided strong evidence for two cases of interspecies LGT within the shared bovine environment: bovine S. agalactiae with Streptococcus uberis (nisin U operon) and Streptococcus dysgalactiae subsp. dysgalactiae (lactose operon). We also found evidence for LGT, involving the salivaricin operon, between the bovine S. agalactiae strain and either Streptococcus pyogenes or Streptococcus salivarius. Our findings provide insight into mechanisms facilitating environmental adaptation and acquisition of potential virulence factors, while highlighting both the key role LGT has played in the recent evolution of the bovine S. agalactiae strain, and the importance of LGT among pathogens within a shared environment.

On the need for integrative phylogenomics, and some steps toward its creation

Recently improved understanding of evolutionary processes suggests that tree-based phylogenetic analyses of evolutionary change cannot adequately explain the divergent evolutionary histories of a great many genes and gene complexes. In particular, genetic diversity in the genomes of prokaryotes, phages, and plasmids cannot be fit into classic tree-like models of evolution. These findings entail the need for fundamental reform of our understanding of molecular evolution and the need to devise alternative apparatus for integrated analysis of these genomes. We advocate the development of integrative phylogenomics for analyzing these genomes and their histories, with tools suited to analyzing the importance of lateral gene transfer (LGT) and of DNA evolution in extra-cellular mobile genetic elements (e.g., viruses, plasmids). These phenomena greatly increase the complexity of relationships among interacting genetic partners, as they exchange functional genetic units. We examine the ontology of functional genetic units, interacting genetic partners, and emergent genetic associations, argue that these three categories of entities are required for a successful integrated phylogenomics. We conclude with arguments to suggest that the proposed new perspective and associated tools are suitable, and perhaps required, as a replacement for the bifurcating trees that have dominated evolutionary thinking for the last 150 years.

Gene Transfer and Diversification of Microbial Eukaryotes

The importance of lateral gene transfer in genome evolution of microbial eukaryotes is slowly being appreciated. Acquisitions of genes have led to metabolic adaptation in diverse eukaryotic lineages. In most cases the metabolic genes have originated from prokaryotes, often followed by sequential transfers between eukaryotes. However, the knowledge of gene transfer in eukaryotes is still mainly based on anecdotal evidence. Some of the observed patterns may be biases in experimental approaches and sequence databases rather than evolutionary trends. Rigorous systematic studies of gene acquisitions that allow for the possibility of exchanges of all categories of genes from all sources are needed to get a more objective view of gene transfer in eukaryote evolution. It may be that the role of gene transfer in the diversification process of microbial eukaryotes currently is underestimated.

Comparative Genomics Begins to Unravel the Ecophysiology of Bioleaching

The metabolic potential of 16 bioleaching microorganisms (Eubacteria and Archaea) has been investigated, allowing the prediction of potential inter- and intra-species physiological interactions (ecophysiology) during spatial and temporal changes that are known to occur within industrial bioleaching heaps. Genome analysis has allowed preliminary models to be built for genes and pathways involved in key processes such as nitrogen and carbon cycling, sulfur and iron uptake and homeostasis, extra-cellular polysaccharide biosynthesis, heavy metal resistance and energy metabolism. This paper will focus on the diverse ways that microorganisms obtain carbon from their environment with a particular emphasis on elucidating how these processes might be expected to vary over space and time during the lifetime of a bioleaching operation. It is anticipated that this knowledge will improve our understanding of fundamental biological processes in extremely acidic environments and it is hoped that it will capture usable knowledge that can be applied to bioleaching. Comparative genomics between two strains of Acidthiobacillus ferrooxidans highlights the importance of lateral gene transfer in increasing genetic and metabolic potential and suggests that classical molecular DNA techniques, such as rDNA typing, significantly underestimate the microbial diversity of bioleaching heaps.

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.

A Protein Structure (or Function ?) Initiative

Departments of Biochemistry and Chemistry, University of Illinois at Urbana-Champaign, 600 South Mathews Avenue,Urbana, IL 61801, USA*Correspondence: j-gerlt@uiuc.eduDOI 10.1016/j.str.2007.10.003As a mechanistic enzymologist, myperspective on the Protein StructureInitiative (PSI) may be somewhat dif-ferent than those of many readersof Structure. I do not consider a highresolution structure as the end to aresearch problem but, instead, thebeginning that allows the formulationof structure-based hypotheses for en-zyme mechanisms and experimentalstrategies for elucidation of both thechemicalandstructuralbasesofthosemechanisms. Indeed, for much of mycareer I have enjoyed productive col-laborations with X-ray crystallogra-phers that always provided interestinginsights into structure-function rela-tionships for a variety of enzyme-cata-lyzed reactions.I admit to having been a discon-nected observer when PSI-1 was initi-ated. Those early stages of the PSIdid little to impact the direction of myscience, although I did wonder exactlyhow the influx of structures that even-tually would emerge could impact myviews on and approaches to enzymol-ogy. I was aware of and perhaps evensympathetic to criticisms that struc-tures would be available for manyhighly divergent proteins of unknownfunction, but with no obvious way toput them to use. I was reminded of myearly, short-sighted views of genomesequencing in which I questioned thewisdom of robotic sequencing of vaststretches of DNA.But, with the passage of a few yearsandthecontinuedevolutionofmyownresearchinterests,Ihavecometoreal-ize that the biological, even the enzy-mological, landscape has changedsignificantly.Morethansixhundredge-nomes later, unanticipated complex-ities in both biology and enzymologyhave become apparent. We all havecome to appreciate that an unexpect-edlysmallnumberofgenesenablesthecomplexities of human biology, chal-lengingsimpleviewsofbiologicalfunc-tion. We also have learned of the im-portance of lateral gene transfer, evenbetween prokaryotes and eukaryotes,and that its role in the acquisition ofadaptive advantage is far more wide-spread than we could have expected.And, even in my own niche in mecha-nistic enzymology, we have come toappreciate that the creation of ‘‘new’’enzymatic functions by divergent evo-lution from ancestral proteins is ex-ceedingly widespread.Pointmutationsandsubsequentse-lective pressure can produce changesin substrate specificity while retaininga common chemical mechanism. Thedivergent members of such super-families (e.g., chymotrypsin, trypsin,elastase, and their homologs) canbe termed ‘‘specificity diverse’’ (GerltandBabbitt,2001).But,divergentevo-lutionalso canproducechanges intheoverall reactions that are catalyzedwhile retaining a partial chemical re-action (mechanistically diverse en-zyme superfamilies). Perhaps evenmore surprising, divergent evolutionfromacommonprogenitorcanproduceenzymes that share neither substratespecificitiesnorchemicalmechanisms(mechanistically distinct enzyme su-prafamilies). In retrospect, the forma-tion of enzyme superfamilies andsuprafamilies reflects the structuraladaptability of a relatively small num-ber of folds to catalyze an amazinglydiverse range of chemistry. For exam-ple, the (b/a)

Integrative genomic, transcriptional, and proteomic diversity in natural isolates of the human pathogen Burkholderia pseudomallei.

Natural isolates of pathogenic bacteria can exhibit a broad range of phenotypic traits. To investigate the molecular mechanisms contributing to such phenotypic variability, we compared the genomes, transcriptomes, and proteomes of two natural isolates of the gram-negative bacterium Burkholderia pseudomallei, the causative agent of the human disease melioidosis. Significant intrinsic genomic, transcriptional, and proteomic variations were observed between the two strains involving genes of diverse functions. We identified 16 strain-specific regions in the B. pseudomallei K96243 reference genome, and for eight regions their differential presence could be ascribed to either DNA acquisition or loss. A remarkable 43% of the transcriptional differences between the strains could be attributed to genes that were differentially present between K96243 and Bp15682, demonstrating the importance of lateral gene transfer or gene loss events in contributing to pathogen diversity at the gene expression level. Proteins expressed in a strain-specific manner were similarly correlated at the gene expression level, but up to 38% of the global proteomic variation between strains comprised proteins expressed in both strains but associated with strain-specific protein isoforms. Collectively, >65 hypothetical genes were transcriptionally or proteomically expressed, supporting their bona fide biological presence. Our results provide, for the first time, an integrated framework for classifying the repertoire of natural variations existing at distinct molecular levels for an important human pathogen.

Does the ‘Ring of Life’ ring true?

In a recent stimulating paper, Rivera and Lake applied a new phylogenetic method to study the evolution of genomes, which challenges the classical representation of the Tree of Life. Acknowledging the evolutionary importance of lateral gene transfer, they used the conditioned genome approach to reconstruct the Tree of Life, and in the end proposed a Ring of Life. They explained that the Ring of Life structure is a result of a single fusion event between two prokaryotic genomes at the base of the eukaryotic tree, probably between the ancestors of a photosynthetic bacterium and an archaeon. Because this constitutes an important conclusion with regards to the evolutionary process and origin of the eukaryotic cell, their work deserves further attention before these conclusions can be accepted. Here we question the reconstruction and the meaning of the Ring of Life. In addition to general problems associated with gene-content-based phylogenetic analyses, we discuss some implicit premises and potential weaknesses of the conditioned genome method and conclude that, although Rivera and Lake's conclusions might be right, they have not been established by their current approach.

Detection of lateral gene transfer events in the prokaryotic tRNA synthetases by the ratios of evolutionary distances method.

The availability of large numbers of genomic sequences has demonstrated the importance of lateral gene transfer (LGT) in prokaryotic evolution. However, considerable uncertainty remains concerning the frequency of LGT compared to other evolutionary processes. To examine LGTs in ancient lineages of prokaryotes a method was developed that utilizes the ratios of evolutionary distances (RED) to distinguish between alternative evolutionary histories. The advantages of this approach are that the variability inherent in comparing protein sequences is transparent, the direction of LGT and the relative rates of evolution are readily identified, and it is possible to detect other types of evolutionary events. This method was standardized using 35 genes encoding ribosomal proteins that were believed to share a vertical evolution. Using RED-T, an original computer program designed to implement the RED method, the evolution of the genes encoding the 20 aminoacyl-tRNA synthetases was examined. Although LGTs were common in the evolution of the aminoacyl-tRNA synthetases, they were not sufficient to obscure the organismal phylogeny. Moreover, much of the apparent complexity of the gene tree was consistent with the formation of the paralogs in the ancestors to the modern lineages followed by more recent loss of one paralog or the other.

Lateral gene transfer and the evolution of plastid-targeted proteins in the secondary plastid-containing alga Bigelowiella natans.

Chlorarachniophytes are amoeboflagellate algae that acquired photosynthesis secondarily by engulfing a green alga and retaining its plastid (chloroplast). An important consequence of secondary endosymbiosis in chlorarachniophytes is that most of the nuclear genes encoding plastid-targeted proteins have moved from the nucleus of the endosymbiont to the host nucleus. We have sequenced and analyzed 83 cDNAs encoding 78 plastid-targeted proteins from the model chlorarachniophyte Bigelowiella natans (formerly Chlorarachnion sp. CCMP621). Phylogenies inferred from the majority of these genes are consistent with a chlorophyte green algal origin. However, a significant number of genes ( approximately 21%) show signs of having been acquired by lateral gene transfer from numerous other sources: streptophyte algae, red algae (or algae with red algal endosymbionts), as well as bacteria. The chlorarachniophyte plastid proteome may therefore be regarded as a mosaic derived from various organisms in addition to the ancestral chlorophyte plastid. In contrast, the homologous genes from the chlorophyte Chlamydomonas reinhardtii do not show any indications of lateral gene transfer. This difference is likely a reflection of the mixotrophic nature of Bigelowiella (i.e., it is photosynthetic and phagotrophic), whereas Chlamydomonas is strictly autotrophic. These results underscore the importance of lateral gene transfer in contributing foreign proteins to eukaryotic cells and their organelles, and also suggest that its impact can vary from lineage to lineage.

Lipopolysaccharide endotoxins.

Bacterial lipopolysaccharides (LPS) typically consist of a hydrophobic domain known as lipid A (or endotoxin), a nonrepeating "core" oligosaccharide, and a distal polysaccharide (or O-antigen). Recent genomic data have facilitated study of LPS assembly in diverse Gram-negative bacteria, many of which are human or plant pathogens, and have established the importance of lateral gene transfer in generating structural diversity of O-antigens. Many enzymes of lipid A biosynthesis like LpxC have been validated as targets for development of new antibiotics. Key genes for lipid A biosynthesis have unexpectedly also been found in higher plants, indicating that eukaryotic lipid A-like molecules may exist. Most significant has been the identification of the plasma membrane protein TLR4 as the lipid A signaling receptor of animal cells. TLR4 belongs to a family of innate immunity receptors that possess a large extracellular domain of leucine-rich repeats, a single trans-membrane segment, and a smaller cytoplasmic signaling region that engages the adaptor protein MyD88. The expanding knowledge of TLR4 specificity and its downstream signaling pathways should provide new opportunities for blocking inflammation associated with infection.