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ELife Mar 2021Horizontal gene transfer is a major force in bacterial evolution. Mobile genetic elements are responsible for much of horizontal gene transfer and also carry beneficial...
Horizontal gene transfer is a major force in bacterial evolution. Mobile genetic elements are responsible for much of horizontal gene transfer and also carry beneficial cargo genes. Uncovering strategies used by mobile genetic elements to benefit host cells is crucial for understanding their stability and spread in populations. We describe a benefit that ICE, an integrative and conjugative element of , provides to its host cells. Activation of ICE conferred a frequency-dependent selective advantage to host cells during two different developmental processes: biofilm formation and sporulation. These benefits were due to inhibition of biofilm-associated gene expression and delayed sporulation by ICE-containing cells, enabling them to exploit their neighbors and grow more prior to development. A single ICE gene, (formerly ), was both necessary and sufficient for inhibition of development. Manipulation of host developmental programs allows ICE to increase host fitness, thereby increasing propagation of the element.
Topics: Bacillus subtilis; DNA, Bacterial; Gene Transfer, Horizontal; Genetic Fitness; Host Microbial Interactions; Interspersed Repetitive Sequences
PubMed: 33655883
DOI: 10.7554/eLife.65924 -
Molecular Microbiology Sep 2016Horizontal transfer of genetic information is a major driving force of evolution. In bacteria, genome plasticity is intimately linked to the ability of the bacterium to... (Review)
Review
Horizontal transfer of genetic information is a major driving force of evolution. In bacteria, genome plasticity is intimately linked to the ability of the bacterium to integrate novel material into existing gene expression circuits. Small RNAs (sRNAs) are a versatile class of regulatory molecules, and have recently been discovered to perform important tasks in the interplay between core genomic elements and horizontally-acquired DNA. Together with auxiliary proteins such as the RNA-chaperone Hfq and cellular ribonucleases, sRNAs typically act post-transcriptionally to either promote or restrict the expression of multiple target genes. Bacterial sRNAs have been identified in core and peripheral (acquired) genome sequences, and their target suites may likewise include genes from both locations. In this review, we discuss how sRNAs influence the expression of foreign genetic material in enterobacterial pathogens, and outline the processes that foster the integration of horizontally-acquired RNAs into existing regulatory networks. We also consider potential benefits and risks of horizontal gene transfer for RNA-based gene regulation.
Topics: Enterobacteriaceae; Gene Expression Regulation, Bacterial; Gene Transfer, Horizontal; Interspersed Repetitive Sequences; RNA, Bacterial; RNA, Small Cytoplasmic; Regulatory Sequences, Ribonucleic Acid
PubMed: 27232692
DOI: 10.1111/mmi.13428 -
Microbiology Spectrum Jun 2016There has been a dramatic increase in the last decade in the number of carbapenem-resistant Enterobacteriaceae, often leaving patients and their providers with few...
There has been a dramatic increase in the last decade in the number of carbapenem-resistant Enterobacteriaceae, often leaving patients and their providers with few treatment options and resultant poor outcomes when an infection develops. The majority of the carbapenem resistance is mediated by bacterial acquisition of one of three carbapenemases (Klebsiella pneumoniae carbapenemase [KPC], oxacillinase-48-like [OXA-48], and the New Delhi metallo-β-lactamase [NDM]). Each of these enzymes has a unique global epidemiology and microbiology. The genes which encode the most globally widespread carbapenemases are typically carried on mobile pieces of DNA which can be freely exchanged between bacterial strains and species via horizontal gene transfer. Unfortunately, most of the antimicrobial surveillance systems target specific strains or species and therefore are not well equipped for examining genes of drug resistance. Examination of not only the carbapenemase gene itself but also the genetic context which can predispose a gene to mobilize within a diversity of species and environments will likely be central to understanding the factors contributing to the global dissemination of carbapenem resistance. Using the three most prevalent carbapenemase genes as examples, this chapter highlights the potential impact the associated genetic mobile elements have on the epidemiology and microbiology for each carbapenemase. Understanding how a carbapenemase gene mobilizes through a bacterial population will be critical for detection methods and ultimately inform infection control practices. Understanding gene mobilization and tracking will require novel approaches to surveillance, which will be required to slow the spread of this emerging resistance.
Topics: Anti-Bacterial Agents; Bacterial Proteins; Carbapenems; Drug Resistance, Multiple, Bacterial; Enterobacteriaceae; Enterobacteriaceae Infections; Humans; Interspersed Repetitive Sequences; Microbial Sensitivity Tests; beta-Lactamases
PubMed: 27337454
DOI: 10.1128/microbiolspec.EI10-0010-2015 -
Philosophical Transactions of the Royal... Aug 2016The history of life is punctuated by evolutionary transitions which engender emergence of new levels of biological organization that involves selection acting at... (Review)
Review
The history of life is punctuated by evolutionary transitions which engender emergence of new levels of biological organization that involves selection acting at increasingly complex ensembles of biological entities. Major evolutionary transitions include the origin of prokaryotic and then eukaryotic cells, multicellular organisms and eusocial animals. All or nearly all cellular life forms are hosts to diverse selfish genetic elements with various levels of autonomy including plasmids, transposons and viruses. I present evidence that, at least up to and including the origin of multicellularity, evolutionary transitions are driven by the coevolution of hosts with these genetic parasites along with sharing of 'public goods'. Selfish elements drive evolutionary transitions at two distinct levels. First, mathematical modelling of evolutionary processes, such as evolution of primitive replicator populations or unicellular organisms, indicates that only increasing organizational complexity, e.g. emergence of multicellular aggregates, can prevent the collapse of the host-parasite system under the pressure of parasites. Second, comparative genomic analysis reveals numerous cases of recruitment of genes with essential functions in cellular life forms, including those that enable evolutionary transitions.This article is part of the themed issue 'The major synthetic evolutionary transitions'.
Topics: Biological Evolution; Interspersed Repetitive Sequences; Viruses
PubMed: 27431520
DOI: 10.1098/rstb.2015.0442 -
Applied and Environmental Microbiology Jan 2019Denitrification ability is sporadically distributed among diverse bacteria, archaea, and fungi. In addition, disagreement has been found between denitrification gene...
Denitrification ability is sporadically distributed among diverse bacteria, archaea, and fungi. In addition, disagreement has been found between denitrification gene phylogenies and the 16S rRNA gene phylogeny. These facts have suggested potential occurrences of horizontal gene transfer (HGT) for the denitrification genes. However, evidence of HGT has not been clearly presented thus far. In this study, we identified the sequences and the localization of the nitrite reductase genes in the genomes of 41 denitrifying sp. strains and searched for mobile genetic elements that contain denitrification genes. All sp. strains examined in this study possessed multiple replicons (4 to 11 replicons), with their sizes ranging from 7 to 1,031 kbp. Among those, the nitrite reductase gene was located on large replicons (549 to 941 kbp). Genome sequencing showed that strains that had similar sequences also shared similar gene arrangements, especially between the TSH58, Sp7, and Sp245 strains. In addition to the high similarity between gene clusters among the three strains, a composite transposon structure was identified in the genome of strain TSH58, which contains the gene cluster and the novel IS family insertion sequences (IS and IS). The gene within the composite transposon system was actively transcribed under denitrification-inducing conditions. Although not experimentally verified in this study, the composite transposon system containing the gene cluster could be transferred to other cells if it is moved to a prophage region and the phage becomes activated and released outside the cells. Taken together, strain TSH58 most likely acquired its denitrification ability by HGT from closely related sp. denitrifiers. The evolutionary history of denitrification is complex. While the occurrence of horizontal gene transfer has been suggested for denitrification genes, most studies report circumstantial evidences, such as disagreement between denitrification gene phylogenies and the 16S rRNA gene phylogeny. Based on the comparative genome analyses of sp. denitrifiers, we identified denitrification genes, including and , located on a mobile genetic element in the genome of sp. strain TSH58. The was actively transcribed under denitrification-inducing conditions. Since this gene was the sole nitrite reductase gene in strain TSH58, this strain most likely benefitted by acquiring denitrification genes via horizontal gene transfer. This finding will significantly advance our scientific knowledge regarding the ecology and evolution of denitrification.
Topics: Azospirillum; DNA Transposable Elements; DNA, Bacterial; Denitrification; Gene Transfer, Horizontal; Genes, Bacterial; Interspersed Repetitive Sequences; Nitrite Reductases; Phylogeny; RNA, Bacterial; RNA, Ribosomal, 16S
PubMed: 30413471
DOI: 10.1128/AEM.02474-18 -
Philosophical Transactions of the Royal... Oct 2022Horizontal gene transfer (HGT) drives microbial adaptation but is often under the control of mobile genetic elements (MGEs) whose interests are not necessarily aligned... (Review)
Review
Horizontal gene transfer (HGT) drives microbial adaptation but is often under the control of mobile genetic elements (MGEs) whose interests are not necessarily aligned with those of their hosts. In general, transfer is costly to the donor cell while potentially beneficial to the recipients. The diversity and plasticity of cell-MGEs interactions, and those among MGEs, result in complex evolutionary processes where the source, or even the existence of selection for maintaining a function in the genome, is often unclear. For example, MGE-driven HGT depends on cell envelope structures and defense systems, but many of these are transferred by MGEs themselves. MGEs can spur periods of intense gene transfer by increasing their own rates of horizontal transmission upon communicating, eavesdropping, or sensing the environment and the host physiology. This may result in high-frequency transfer of host genes unrelated to the MGE. Here, we review how MGEs drive HGT and how their transfer mechanisms, selective pressures and genomic traits affect gene flow, and therefore adaptation, in microbial populations. The encoding of many adaptive niche-defining microbial traits in MGEs means that intragenomic conflicts and alliances between cells and their MGEs are key to microbial functional diversification. This article is part of a discussion meeting issue 'Genomic population structures of microbial pathogens'.
Topics: Biological Evolution; Gene Transfer, Horizontal; Interspersed Repetitive Sequences
PubMed: 35989606
DOI: 10.1098/rstb.2021.0234 -
Trends in Genetics : TIG Dec 2019Our recent ability to sequence entire genomes, along with all of their transcribed RNAs, has led to the surprising finding that only ∼1% of the human genome is used to... (Review)
Review
Our recent ability to sequence entire genomes, along with all of their transcribed RNAs, has led to the surprising finding that only ∼1% of the human genome is used to encode proteins. This finding has led to vigorous debate over the functional importance of the transcribed but untranslated portions of the genome. Currently, scientists tend to assume coding genes are functional until proven not to be, while the opposite is true for noncoding genes. This review takes a new look at the evidence for and against widespread noncoding gene functionality. We focus in particular on long noncoding RNA (noncoding RNAs longer than 200 nucleotides) genes and their 'junk' associates, transposable elements, and satellite repeats. Taken together, the suggestion put forward is that more of this junk DNA may be functional than nonfunctional and that noncoding RNAs and transposable elements act symbiotically to drive evolution.
Topics: Animals; DNA, Intergenic; Evolution, Molecular; Genetic Association Studies; Genome; Genomics; Humans; Interspersed Repetitive Sequences; Phenotype; RNA, Long Noncoding; Spermatogenesis
PubMed: 31662190
DOI: 10.1016/j.tig.2019.09.006 -
Trends in Genetics : TIG Oct 2009Duplicated sequences are substrates for the emergence of new genes and are an important source of genetic instability associated with rare and common diseases. Analyses... (Review)
Review
Duplicated sequences are substrates for the emergence of new genes and are an important source of genetic instability associated with rare and common diseases. Analyses of primate genomes have shown an increase in the proportion of interspersed segmental duplications (SDs) within the genomes of humans and great apes. This contrasts with other mammalian genomes that seem to have their recently duplicated sequences organized in a tandem configuration. In this review, we focus on the mechanistic origin and impact of this difference with respect to evolution, genetic diversity and primate phenotype. Although many genomes will be sequenced in the future, resolution of this aspect of genomic architecture still requires high quality sequences and detailed analyses.
Topics: Animals; Evolution, Molecular; Gene Duplication; Genetic Variation; Genome; Humans; Interspersed Repetitive Sequences; Models, Genetic; Phylogeny; Primates
PubMed: 19796838
DOI: 10.1016/j.tig.2009.08.002 -
Current Opinion in Genetics &... Jun 2013The human genome is replete with interspersed repetitive sequences derived from the propagation of mobile DNA elements. Three families of human retrotransposons remain... (Review)
Review
The human genome is replete with interspersed repetitive sequences derived from the propagation of mobile DNA elements. Three families of human retrotransposons remain active today: LINE1, Alu, and SVA elements. Since 1988, de novo insertions at previously recognized disease loci have been shown to generate highly penetrant alleles in Mendelian disorders. Only recently has the extent of germline-transmitted retrotransposon insertion polymorphism (RIP) in human populations been fully realized. Also exciting are recent studies of somatic retrotransposition in human tissues and reports of tumor-specific insertions, suggesting roles in tissue heterogeneity and tumorigenesis. Here we discuss mobile elements in human disease with an emphasis on exciting developments from the last several years.
Topics: Alleles; Alu Elements; Carcinogenesis; Genetic Diseases, Inborn; Genome, Human; Humans; Long Interspersed Nucleotide Elements; Neoplasms; Polymorphism, Genetic
PubMed: 23523050
DOI: 10.1016/j.gde.2013.02.007 -
Philosophical Transactions of the Royal... Aug 2009Comparative whole-genome analyses have demonstrated that horizontal gene transfer (HGT) provides a significant contribution to prokaryotic genome innovation. The... (Review)
Review
Comparative whole-genome analyses have demonstrated that horizontal gene transfer (HGT) provides a significant contribution to prokaryotic genome innovation. The evolution of specific prokaryotes is therefore tightly linked to the environment in which they live and the communal pool of genes available within that environment. Here we use the term supergenome to describe the set of all genes that a prokaryotic 'individual' can draw on within a particular environmental setting. Conjugative plasmids can be considered particularly successful entities within the communal pool, which have enabled HGT over large taxonomic distances. These plasmids are collections of discrete regions of genes that function as 'backbone modules' to undertake different aspects of overall plasmid maintenance and propagation. Conjugative plasmids often carry suites of 'accessory elements' that contribute adaptive traits to the hosts and, potentially, other resident prokaryotes within specific environmental niches. Insight into the evolution of plasmid modules therefore contributes to our knowledge of gene dissemination and evolution within prokaryotic communities. This communal pool provides the prokaryotes with an important mechanistic framework for obtaining adaptability and functional diversity that alleviates the need for large genomes of specialized 'private genes'.
Topics: Evolution, Molecular; Gene Transfer, Horizontal; Genome, Archaeal; Genome, Bacterial; Interspersed Repetitive Sequences; Plasmids
PubMed: 19571247
DOI: 10.1098/rstb.2009.0037