A Life in Bacillus subtilis Signal Transduction Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 James A. Hoch
This is a tale of how technology drove the discovery of the molecular basis for signal transduction in the initiation of sporulation in Bacillus subtilis and in bacterial two-component systems. It progresses from genetics to cloning and sequencing to biochemistry to structural biology to an understanding of how proteins evolve interaction specificity and to identification of interaction surfaces by statistical physics. This is about how the people in my laboratory accomplished this feat; without them little would have been done.
Metabolic Diversity and Novelties in the Oomycetes Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Howard S. Judelson
The eukaryotic microbes called oomycetes include many important saprophytes and pathogens, with the latter exhibiting necrotrophy, biotrophy, or obligate biotrophy. Understanding oomycete metabolism is fundamental to understanding these lifestyles. Genome mining and biochemical studies have shown that oomycetes, which belong to the kingdom Stramenopila, secrete suites of carbohydrate- and protein-degrading enzymes adapted to their environmental niches and produce unusual lipids and energy storage compounds. Despite having limited secondary metabolism, many oomycetes make chemicals for communicating within their species or with their hosts. Horizontal and endosymbiotic gene transfer events have diversified oomycete metabolism, resulting in biochemical pathways that often depart from standard textbook descriptions by amalgamating enzymes from multiple sources. Gene fusions and duplications have further shaped the composition and expression of the enzymes. Current research is helping us learn how oomycetes interact with host and environment, understand eukaryotic diversity and evolution, and identify targets for drugs and crop protection chemicals.
Early Diverging Fungi: Diversity and Impact at the Dawn of Terrestrial Life Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Mary L. Berbee, Timothy Y. James, Christine Strullu-Derrien
As decomposers or plant pathogens, fungi deploy invasive growth and powerful carbohydrate active enzymes to reduce multicellular plant tissues to humus and simple sugars. Fungi are perhaps also the most important mutualistic symbionts in modern ecosystems, transporting poorly soluble mineral nutrients to plants and thus enhancing the growth of vegetation. However, at their origin over a billion years ago, fungi, like plants and animals, were unicellular marine microbes. Like the other multicellular kingdoms, Fungi evolved increased size, complexity, and metabolic functioning. Interactions of fungi with plants changed terrestrial ecology and geology and modified the Earth's atmosphere. In this review, we discuss the diversification and ecological roles of the fungi over their first 600 million years, from their origin through their colonization of land, drawing on phylogenomic evidence for their relationships and metabolic capabilities and on molecular dating, fossils, and modeling of Earth's paleoclimate.
Regulation of Cell Polarity in Motility and Cell Division in Myxococcus xanthus Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Dominik Schumacher, Lotte Søgaard-Andersen
Rod-shaped Myxococcus xanthus cells are polarized with proteins asymmetrically localizing to specific positions. This spatial organization is important for regulation of motility and cell division and changes over time. Dedicated protein modules regulate motility independent of the cell cycle, and cell division dependent on the cell cycle. For motility, a leading-lagging cell polarity is established that is inverted during cellular reversals. Establishment and inversion of this polarity are regulated hierarchically by interfacing protein modules that sort polarized motility proteins to the correct cell poles or cause their relocation between cell poles during reversals akin to a spatial toggle switch. For division, a novel self-organizing protein module that incorporates a ParA ATPase positions the FtsZ-ring at midcell. This review covers recent findings concerning the spatiotemporal regulation of motility and cell division in M. xanthus and illustrates how the study of diverse bacteria may uncover novel mechanisms involved in regulating bacterial cell polarity.
Assembly and Function of the Bacillus anthracis S-Layer Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Dominique Missiakas, Olaf Schneewind
Bacillus anthracis, the anthrax agent, is a member of the Bacillus cereus sensu lato group, which includes invasive pathogens of mammals or insects as well as nonpathogenic environmental strains. The genes for anthrax pathogenesis are located on two large virulence plasmids. Similar virulence plasmids have been acquired by other B. cereus strains and enable the pathogenesis of anthrax-like diseases. Among the virulence factors of B. anthracis is the S-layer-associated protein BslA, which endows bacilli with invasive attributes for mammalian hosts. BslA surface display and function are dependent on the bacterial S-layer, whose constituents assemble by binding to the secondary cell wall polysaccharide (SCWP) via S-layer homology (SLH) domains. B. anthracis and other pathogenic B. cereus isolates harbor genes for the secretion of S-layer proteins, for S-layer assembly, and for synthesis of the SCWP. We review here recent insights into the assembly and function of the S-layer and the SCWP.
The Cell Wall of the Human Fungal Pathogen Aspergillus fumigatus: Biosynthesis, Organization, Immune Response, and Virulence Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Jean-Paul Latgé, Anne Beauvais, Georgios Chamilos
More than 90% of the cell wall of the filamentous fungus Aspergillus fumigatus comprises polysaccharides. Biosynthesis of the cell wall polysaccharides is under the control of three types of enzymes: transmembrane synthases, which are anchored to the plasma membrane and use nucleotide sugars as substrates, and cell wall–associated transglycosidases and glycosyl hydrolases, which are responsible for remodeling the de novo synthesized polysaccharides and establishing the three-dimensional structure of the cell wall. For years, the cell wall was considered an inert exoskeleton of the fungal cell. The cell wall is now recognized as a living organelle, since the composition and cellular localization of the different constitutive cell wall components (especially of the outer layers) vary when the fungus senses changes in the external environment. The cell wall plays a major role during infection. The recognition of the fungal cell wall by the host is essential in the initiation of the immune response. The interactions between the different pattern-recognition receptors (PRRs) and cell wall pathogen-associated molecular patterns (PAMPs) orientate the host response toward either fungal death or growth, which would then lead to disease development. Understanding the molecular determinants of the interplay between the cell wall and host immunity is fundamental to combatting Aspergillus diseases.
Elongation Factor P and the Control of Translation Elongation Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Andrei Rajkovic, Michael Ibba
Elongation factor P (EF-P) binds to ribosomes requiring assistance with the formation of oligo-prolines. In order for EF-P to associate with paused ribosomes, certain tRNAs with specific d-arm residues must be present in the peptidyl site, e.g., tRNAPro. Once EF-P is accommodated into the ribosome and bound to Pro-tRNAPro, productive synthesis of the peptide bond occurs. The underlying mechanism by which EF-P facilitates this reaction seems to have entropic origins. Maximal activity of EF-P requires a posttranslational modification in Escherichia coli, Pseudomonas aeruginosa, and Bacillus subtilis. Each of these modifications is distinct and ligated onto its respective EF-P through entirely convergent means. Here we review the facets of translation elongation that are controlled by EF-P, with a particular focus on the purpose behind the many different modifications of EF-P.
Genetics and Epigenetics of Mating Type Determination in Paramecium and Tetrahymena Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Eduardo Orias, Deepankar Pratap Singh, Eric Meyer
While sex is an ancient and highly conserved eukaryotic invention, self-incompatibility systems such as mating types or sexes appear to be derived limitations that show considerable evolutionary plasticity. Within a single class of ciliates, Paramecium and Tetrahymena species have long been known to present a wide variety of mating type numbers and modes of inheritance, but only recently have the genes involved been identified. Although similar transmembrane proteins mediate self/nonself recognition in both ciliates, the mechanisms of mating type determination differ widely, ranging from Mendelian systems to developmental nuclear differentiation, either stochastic or maternally inherited. The non-Mendelian systems rely on programmed editing of the germline genome that occurs during differentiation of the somatic nucleus, and they have co-opted different DNA recombination mechanisms—some previously unknown. Here we review the recent molecular advances and some remaining unsolved questions and discuss the possible implications of these diverse mechanisms for inbreeding/outbreeding balance regulation.
Microbiota-Based Therapies for Clostridium difficile and Antibiotic-Resistant Enteric Infections Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Brittany B. Lewis, Eric G. Pamer
Bacterial pathogens are increasingly antibiotic resistant, and development of clinically effective antibiotics is lagging. Curing infections increasingly requires antimicrobials that are broader spectrum, more toxic, and more expensive, and mortality attributable to antibiotic-resistant pathogens is rising. The commensal microbiota, comprising microbes that colonize the mammalian gastrointestinal tract, can provide high levels of resistance to infection, and the contributions of specific bacterial species to resistance are being discovered and characterized. Microbiota-mediated mechanisms of colonization resistance and pathogen clearance include bactericidal activity, nutrient depletion, immune activation, and manipulation of the gut's chemical environment. Current research is focusing on development of microbiota-based therapies to reduce intestinal colonization with antibiotic-resistant pathogens, with the goal of reducing pathogen transmission and systemic dissemination.
A Symphony of Cyclases: Specificity in Diguanylate Cyclase Signaling Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Kurt M. Dahlstrom, George A. O'Toole
Cyclic diguanylate (c-di-GMP) is a near universal signaling molecule produced by diguanylate cyclases that can direct a variety of bacterial behaviors. A major area of research over the last several years has been aimed at understanding how a cell with dozens of diguanylate cyclases can deploy a given subset of them to produce a desired phenotypic outcome without undesired cross talk between c-di-GMP-dependent systems. Several models have been put forward to address this question, including specificity of cyclase activation, tuned binding constants of effector proteins, and physical interaction between cyclases and effectors. Additionally, recent evidence has suggested that there may be a link between the catalytic state of a cyclase and its physical contact with an effector. This review highlights several key studies, examines the proposed global and local models of c-di-GMP signaling specificity in bacteria, and attempts to identify the most fruitful steps that can be taken to better understand how dynamic networks of sibling cyclases and effector proteins result in sensible outputs that govern cellular behavior.
Evolution of Mating in the Saccharomycotina Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Kenneth H. Wolfe, Geraldine Butler
The fungal phylum Ascomycota comprises three subphyla: Saccharomycotina, Pezizomycotina, and Taphrinomycotina. In many Saccharomycotina species, cell identity is determined by genes at the MAT (mating-type) locus; mating occurs between MATa and MATα cells. Some species can switch between MATa and MATα mating types. Switching in the Saccharomycotina originated in the common ancestor of the Saccharomycetaceae, Pichiaceae, and Metschnikowiaceae families, as a flip/flop mechanism that inverted a section of chromosome. Switching was subsequently lost in the Metschnikowiaceae, including Candida albicans, but became more complex in the Saccharomycetaceae when the mechanism changed from inversion to copy-and-paste between HML/HMR and MAT. Based on their phylogenetic closeness and the similarity of their MTL (mating-type like) loci, some Metschnikowia species may provide useful models for the sexual cycles of Candida species. Conservation of synteny demonstrates that, despite changes in its gene content, a single orthologous locus (MAT/MTL) has controlled cell type throughout ascomycete evolution.
“Fleaing” the Plague: Adaptations of Yersinia pestis to Its Insect Vector That Lead to Transmission* Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 B. Joseph Hinnebusch, Clayton O. Jarrett, David M. Bland
Interest in arthropod-borne pathogens focuses primarily on how they cause disease in humans. How they produce a transmissible infection in their arthropod host is just as critical to their life cycle, however. Yersinia pestis adopts a unique life stage in the digestive tract of its flea vector, characterized by rapid formation of a bacterial biofilm that is enveloped in a complex extracellular polymeric substance. Localization and adherence of the biofilm to the flea foregut is essential for transmission. Here, we review the molecular and genetic mechanisms of these processes and present a comparative evaluation and updated model of two related transmission mechanisms.
Evolutionary Genomics of Defense Systems in Archaea and Bacteria* Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Eugene V. Koonin, Kira S. Makarova, Yuri I. Wolf
Evolution of bacteria and archaea involves an incessant arms race against an enormous diversity of genetic parasites. Accordingly, a substantial fraction of the genes in most bacteria and archaea are dedicated to antiparasite defense. The functions of these defense systems follow several distinct strategies, including innate immunity; adaptive immunity; and dormancy induction, or programmed cell death. Recent comparative genomic studies taking advantage of the expanding database of microbial genomes and metagenomes, combined with direct experiments, resulted in the discovery of several previously unknown defense systems, including innate immunity centered on Argonaute proteins, bacteriophage exclusion, and new types of CRISPR-Cas systems of adaptive immunity. Some general principles of function and evolution of defense systems are starting to crystallize, in particular, extensive gain and loss of defense genes during the evolution of prokaryotes; formation of genomic defense islands; evolutionary connections between mobile genetic elements and defense, whereby genes of mobile elements are repeatedly recruited for defense functions; the partially selfish and addictive behavior of the defense systems; and coupling between immunity and dormancy induction/programmed cell death.
Regulating Bacterial Virulence with RNA Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Juan J. Quereda, Pascale Cossart
Noncoding RNAs (ncRNAs) regulating virulence have been identified in most pathogens. This review discusses RNA-mediated mechanisms exploited by bacterial pathogens to successfully infect and colonize their hosts. It discusses the most representative RNA-mediated regulatory mechanisms employed by two intracellular [Listeria monocytogenes and Salmonella enterica serovar Typhimurium (S. Typhimurium)] and two extracellular (Vibrio cholerae and Staphylococcus aureus) bacterial pathogens. We review the RNA-mediated regulators (e.g., thermosensors, riboswitches, cis- and trans-encoded RNAs) used for adaptation to the specific niches colonized by these bacteria (intestine, blood, or the intracellular environment, for example) in the framework of the specific pathophysiological aspects of the diseases caused by these microorganisms. A critical discussion of the newest findings in the field of bacterial ncRNAs shows how examples in model pathogens could pave the way for the discovery of new mechanisms in other medically important bacterial pathogens.
Clostridium difficile Toxin Biology Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Klaus Aktories, Carsten Schwan, Thomas Jank
Clostridium difficile is the cause of antibiotics-associated diarrhea and pseudomembranous colitis. The pathogen produces three protein toxins: C. difficile toxins A (TcdA) and B (TcdB), and C. difficile transferase toxin (CDT). The single-chain toxins TcdA and TcdB are the main virulence factors. They bind to cell membrane receptors and are internalized. The N-terminal glucosyltransferase and autoprotease domains of the toxins translocate from low-pH endosomes into the cytosol. After activation by inositol hexakisphosphate (InsP6), the autoprotease cleaves and releases the glucosyltransferase domain into the cytosol, where GTP-binding proteins of the Rho/Ras family are mono-O-glucosylated and, thereby, inactivated. Inactivation of Rho proteins disturbs the organization of the cytoskeleton and affects multiple Rho-dependent cellular processes, including loss of epithelial barrier functions, induction of apoptosis, and inflammation. CDT, the third C. difficile toxin, is a binary actin-ADP-ribosylating toxin that causes depolymerization of actin, thereby inducing formation of the microtubule-based protrusions. Recent progress in understanding of the toxins’ actions include insights into the toxin structures, their interaction with host cells, and functional consequences of their actions.
Lessons from the Environmental Antibiotic Resistome Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Matthew D. Surette, Gerard D. Wright
Antibiotic resistance is a global public health issue of growing proportions. All antibiotics are susceptible to resistance. The evidence is now clear that the environment is the single largest source and reservoir of resistance. Soil, aquatic, atmospheric, animal-associated, and built ecosystems are home to microbes that harbor antibiotic resistance elements and the means to mobilize them. The diversity and abundance of resistance in the environment is consistent with the ancient origins of antibiotics and a variety of studies support a long natural history of associated resistance. The implications are clear: Understanding the evolution of resistance in the environment, its diversity, and mechanisms is essential to the management of our existing and future antibiotic resources.
Evolutionary Origins of Two-Barrel RNA Polymerases and Site-Specific Transcription Initiation Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Thomas Fouqueau, Fabian Blombach, Finn Werner
Evolution-related multisubunit RNA polymerases (RNAPs) carry out RNA synthesis in all domains life. Although their catalytic cores and fundamental mechanisms of transcription elongation are conserved, the initiation stage of the transcription cycle differs substantially in bacteria, archaea, and eukaryotes in terms of the requirements for accessory factors and details of the molecular mechanisms. This review focuses on recent insights into the evolution of the transcription apparatus with regard to (a) the surprisingly pervasive double-Ψ β-barrel active-site configuration among different nucleic acid polymerase families, (b) the origin and phylogenetic distribution of TBP, TFB, and TFE transcription factors, and (c) the functional relationship between transcription and translation initiation mechanisms in terms of transcription start site selection and RNA structure.
The Critical Roles of Polysaccharides in Gut Microbial Ecology and Physiology Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Nathan T. Porter, Eric C. Martens
The human intestine harbors a dense microbial ecosystem (microbiota) that is different between individuals, dynamic over time, and critical for aspects of health and disease. Dietary polysaccharides directly shape the microbiota because of a gap in human digestive physiology, which is equipped to assimilate only proteins, lipids, simple sugars, and starch, leaving nonstarch polysaccharides as major nutrients reaching the microbiota. A mutualistic role of gut microbes is to digest dietary complex carbohydrates, liberating host-absorbable energy via fermentation products. Emerging data indicate that polysaccharides play extensive roles in host–gut microbiota symbiosis beyond dietary polysaccharide digestion, including microbial interactions with endogenous host glycans and the importance of microbial polysaccharides. In this review, we consider multiple mechanisms through which polysaccharides mediate aspects of host-microbe symbiosis in the gut, including some affecting health. As host and microbial metabolic pathways are intimately connected with diet, we highlight the potential to manipulate this system for health.
The RNAi Universe in Fungi: A Varied Landscape of Small RNAs and Biological Functions Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Santiago Torres-Martínez, Rosa M. Ruiz-Vázquez
RNA interference (RNAi) is a conserved eukaryotic mechanism that uses small RNA molecules to suppress gene expression through sequence-specific messenger RNA degradation, translational repression, or transcriptional inhibition. In filamentous fungi, the protective function of RNAi in the maintenance of genome integrity is well known. However, knowledge of the regulatory role of RNAi in fungi has had to wait until the recent identification of different endogenous small RNA classes, which are generated by distinct RNAi pathways. In addition, RNAi research on new fungal models has uncovered the role of small RNAs and RNAi pathways in the regulation of diverse biological functions. In this review, we give an up-to-date overview of the different classes of small RNAs and RNAi pathways in fungi and their roles in the defense of genome integrity and regulation of fungal physiology and development, as well as in the interaction of fungi with biotic and abiotic environments.
Bacterial Cell Division: Nonmodels Poised to Take the Spotlight Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Prahathees J. Eswara, Kumaran S. Ramamurthi
The last three decades have witnessed an explosion of discoveries about the mechanistic details of binary fission in model bacteria such as Escherichia coli, Bacillus subtilis, and Caulobacter crescentus. This was made possible not only by advances in microscopy that helped answer questions about cell biology but also by clever genetic manipulations that directly and easily tested specific hypotheses. More recently, research using understudied organisms, or nonmodel systems, has revealed several alternate mechanistic strategies that bacteria use to divide and propagate. In this review, we highlight new findings and compare these strategies to cell division mechanisms elucidated in model organisms.
Histone Methylation by SET Domain Proteins in Fungi Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Michael Freitag
Histone-modifying enzymes are responsible for regulating transcription, recombination, DNA repair, DNA replication, chromatid cohesion, and chromosome segregation. Fungi are ideally suited for comparative chromatin biology because sequencing of numerous genomes from many clades is coupled to existing rich methodology that allows truly holistic approaches, integrating evolutionary biology with mechanistic molecular biology and ecology, promising applications in medicine or plant pathology. While genome information is rich, mechanistic studies on histone modifications are largely restricted to two yeasts, Saccharomyces cerevisiae and Schizosaccharomyces pombe, and one filamentous fungus, Neurospora crassa—three species that arguably are not representative of this diverse kingdom. Here, histone methylation serves as a paradigm to illustrate the roles chromatin modifications may play in more complex fungal life cycles. This review summarizes recent advances in our understanding of histone H3 methylation at two sites associated with active transcription, lysine 4 and lysine 36 (H3K4, H3K36); a site associated with the formation of constitutive heterochromatin, lysine 9 (H3K9); and a site associated with the formation of facultative heterochromatin, lysine 27 (H3K27). Special attention is paid to differences in how methylation marks interact in different taxa.
Predator Versus Pathogen: How Does Predatory Bdellovibrio bacteriovorus Interface with the Challenges of Killing Gram-Negative Pathogens in a Host Setting? Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 David Negus, Chris Moore, Michelle Baker, Dhaarini Raghunathan, Jess Tyson, R. Elizabeth Sockett
Bdellovibrio bacteriovorus is a small deltaproteobacterial predator that has evolved to invade, reseal, kill, and digest other gram-negative bacteria in soils and water environments. It has a broad host range and kills many antibiotic-resistant, clinical pathogens in vitro, a potentially useful capability if it could be translated to a clinical setting. We review relevant mechanisms of B. bacteriovorus predation and the physiological properties that would influence its survival in a mammalian host. Bacterial pathogens increasingly display conventional antibiotic resistance by expressing and varying surface and soluble biomolecules. Predators coevolved alongside prey bacteria and so encode diverse predatory enzymes that are hard for pathogens to resist by simple mutation. Predators do not replicate outside pathogens and thus express few transport proteins and thus few surface epitopes for host immune recognition. We explain these features, relating them to the potential of predatory bacteria as cellular medicines.
Germination of Spores of the Orders Bacillales and Clostridiales Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Peter Setlow, Shiwei Wang, Yong-Qing Li
Dormant Bacillales and Clostridiales spores begin to grow when small molecules (germinants) trigger germination, potentially leading to food spoilage or disease. Germination-specific proteins sense germinants, transport small molecules, and hydrolyze specific bonds in cortex peptidoglycan and specific proteins. Major events in germination include (a) germinant sensing; (b) commitment to germinate; (c) release of spores’ depot of dipicolinic acid (DPA); (d) hydrolysis of spores’ peptidoglycan cortex; and (e) spore core swelling and water uptake, cell wall peptidoglycan remodeling, and restoration of core protein and inner spore membrane lipid mobility. Germination is similar between Bacillales and Clostridiales, but some species differ in how germinants are sensed and how cortex hydrolysis and DPA release are triggered. Despite detailed knowledge of the proteins and signal transduction pathways involved in germination, precisely what some germination proteins do and how they do it remain unclear.
Microbial Expansins Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Daniel J. Cosgrove
Expansins are small proteins that loosen plant cell walls and cellulosic materials without lytic activity. First discovered in plants, expansin genes are found in the genomes of numerous bacteria and fungi that interact with plants in pathogenic and mutualistic patterns, as well as in microbes that feed on plant debris. Horizontal gene transfer from plants to microbes and between microbes accounts for expansins’ irregular taxonomic distribution. Expansins facilitate plant colonization by Bacillus, Clavibacter, and Trichoderma species, a list likely to grow as knowledge of microbial expansin function deepens. Studies have documented a synergistic action of expansins for cellulose digestion by cellulases, but only rarely to an extent that is commercially relevant. Expansins’ biophysical actions remain enigmatic because of limited understanding of cell wall structure. Deeper understanding of microbial expansins may lead to novel approaches for biomass deconstruction and biocontrol of plant diseases.
Bacterial Cell Size: Multifactorial and Multifaceted Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Corey S. Westfall, Petra Anne Levin
How cells establish, maintain, and modulate size has always been an area of great interest and fascination. Until recently, technical limitations curtailed our ability to understand the molecular basis of bacterial cell size control. In the past decade, advances in microfluidics, imaging, and high-throughput single-cell analysis, however, have led to a flurry of work revealing size to be a highly complex trait involving the integration of three core aspects of bacterial physiology: metabolism, growth, and cell cycle progression.
Bacterial Membranes: Structure, Domains, and Function Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Henrik Strahl, Jeff Errington
The bacterial cytoplasmic membrane is composed of roughly equal proportions of lipids and proteins. The main lipid components are phospholipids, which vary in acyl chain length, saturation, and branching and carry head groups that vary in size and charge. Phospholipid variants determine membrane properties such as fluidity and charge that in turn modulate interactions with membrane-associated proteins. We summarize recent advances in understanding bacterial membrane structure and function, focusing particularly on the possible existence and significance of specialized membrane domains. We review the role of membrane curvature as a spatial cue for recruitment and regulation of proteins involved in morphogenic functions, especially elongation and division. Finally, we examine the role of the membrane, especially regulation of synthesis and fluid properties, in the life cycle of cell wall–deficient L-form bacteria.
Outer Membrane Biogenesis Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Anna Konovalova, Daniel E. Kahne, Thomas J. Silhavy
The hallmark of gram-negative bacteria and organelles such as mitochondria and chloroplasts is the presence of an outer membrane. In bacteria such as Escherichia coli, the outer membrane is a unique asymmetric lipid bilayer with lipopolysaccharide in the outer leaflet. Integral transmembrane proteins assume a β-barrel structure, and their assembly is catalyzed by the heteropentameric Bam complex containing the outer membrane protein BamA and four lipoproteins, BamB–E. How the Bam complex assembles a great diversity of outer membrane proteins into a membrane without an obvious energy source is a particularly challenging problem, because folding intermediates are predicted to be unstable in either an aqueous or a hydrophobic environment. Two models have been put forward: the budding model, based largely on structural data, and the BamA assisted model, based on genetic and biochemical studies. Here we offer a critical discussion of the pros and cons of each.
Rewriting the Genetic Code Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Takahito Mukai, Marc J. Lajoie, Markus Englert, Dieter Söll
The genetic code—the language used by cells to translate their genomes into proteins that perform many cellular functions—is highly conserved throughout natural life. Rewriting the genetic code could lead to new biological functions such as expanding protein chemistries with noncanonical amino acids (ncAAs) and genetically isolating synthetic organisms from natural organisms and viruses. It has long been possible to transiently produce proteins bearing ncAAs, but stabilizing an expanded genetic code for sustained function in vivo requires an integrated approach: creating recoded genomes and introducing new translation machinery that function together without compromising viability or clashing with endogenous pathways. In this review, we discuss design considerations and technologies for expanding the genetic code. The knowledge obtained by rewriting the genetic code will deepen our understanding of how genomes are designed and how the canonical genetic code evolved.
Evolutionary Trajectories to Antibiotic Resistance Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Diarmaid Hughes, Dan I. Andersson
The ability to predict the evolutionary trajectories of antibiotic resistance would be of great value in tailoring dosing regimens of antibiotics so as to maximize the duration of their usefulness. Useful prediction of resistance evolution requires information about (a) the mutation supply rate, (b) the level of resistance conferred by the resistance mechanism, (c) the fitness of the antibiotic-resistant mutant bacteria as a function of drug concentration, and (d) the strength of selective pressures. In addition, processes including epistatic interactions and compensatory evolution, coselection of drug resistances, and population bottlenecks and clonal interference can strongly influence resistance evolution and thereby complicate attempts at prediction. Currently, the very limited quantitative data on most of these parameters severely limit attempts to accurately predict trajectories of resistance evolution.
Copper Acquisition and Utilization in Fungi Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Aaron D. Smith, Brandon L. Logeman, Dennis J. Thiele
Fungal cells colonize and proliferate in distinct niches, from soil and plants to diverse tissues in human hosts. Consequently, fungi are challenged with the goal of obtaining nutrients while simultaneously elaborating robust regulatory mechanisms to cope with a range of availability of nutrients, from scarcity to excess. Copper is essential for life but also potentially toxic. In this review we describe the sophisticated homeostatic mechanisms by which fungi acquire, utilize, and control this biochemically versatile trace element. Fungal pathogens, which can occupy distinct host tissues that have their own intrinsic requirements for copper homeostasis, have evolved mechanisms to acquire copper to successfully colonize the host, disseminate to other tissues, and combat host copper bombardment mechanisms that would otherwise mitigate virulence.
Variant Gene Expression and Antigenic Variation by Malaria Parasites Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Kirk W. Deitsch, Ron Dzikowski
Malaria is a significant threat throughout the developing world. Among the most fascinating aspects of the protozoan parasites responsible for this disease are the methods they employ to avoid the immune system and perpetuate chronic infections. Key among these is antigenic variation: By systematically altering antigens that are displayed to the host's immune system, the parasite renders the adaptive immune response ineffective. For Plasmodium falciparum, the species responsible for the most severe form of human malaria, this process involves a complicated molecular mechanism that results in continuously changing patterns of variant-antigen-encoding gene expression. Although many features of this process remain obscure, significant progress has been made in recent years to decipher various molecular aspects of the regulatory cascade that causes chronic infection.
Syntrophy Goes Electric: Direct Interspecies Electron Transfer Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Derek R. Lovley
Direct interspecies electron transfer (DIET) has biogeochemical significance, and practical applications that rely on DIET or DIET-based aspects of microbial physiology are growing. Mechanisms for DIET have primarily been studied in defined cocultures in which Geobacter species are one of the DIET partners. Electrically conductive pili (e-pili) can be an important electrical conduit for DIET. However, there may be instances in which electrical contacts are made between electron transport proteins associated with the outer membranes of the partners. Alternatively, DIET partners can plug into conductive carbon materials, such as granular activated carbon, carbon cloth, and biochar, for long-range electron exchange without the need for e-pili. Magnetite promotes DIET, possibly by acting as a substitute for outer-surface c-type cytochromes. DIET is the primary mode of interspecies electron exchange in some anaerobic digesters converting wastes to methane. Promoting DIET with conductive materials shows promise for stabilizing and accelerating methane production in digesters, permitting higher organic loading rates. Various lines of evidence suggest that DIET is important in terrestrial wetlands, which are an important source of atmospheric methane. DIET may also have a role in anaerobic methane oxidation coupled to sulfate reduction, an important control on methane releases. The finding that DIET can serve as the source of electrons for anaerobic photosynthesis further broadens its potential environmental significance. Microorganisms capable of DIET are good catalysts for several bioelectrochemical technologies and e-pili are a promising renewable source of electronic materials. The study of DIET is in its early stages, and additional investigation is required to better understand the diversity of microorganisms that are capable of DIET, the importance of DIET to carbon and electron flow in anaerobic environments, and the biochemistry and physiology of DIET.
Neisseria gonorrhoeae: Drug Resistance, Mouse Models, and Vaccine Development Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Peter A. Rice, William M. Shafer, Sanjay Ram, Ann E. Jerse
Gonorrhea, an obligate human infection, is on the rise worldwide and gonococcal strains resistant to many antibiotics are emerging. Appropriate antimicrobial treatment and prevention, including effective vaccines, are urgently needed. To guide investigation, an experimental model of genital tract infection has been developed in female mice to study mechanisms by which Neisseria gonorrhoeae evades host-derived antimicrobial factors and to identify protective and immunosuppressive pathways. Refinements of the animal model have also improved its use as a surrogate host of human infection and accelerated the testing of novel therapeutic and prophylactic compounds against gonococcal infection. Reviewed herein are the (a) history of antibiotic usage and resistance against gonorrhea and the consequences of resistance mechanisms that may increase gonococcal fitness and therefore the potential for spread, (b) use of gonococcal infection in the animal model system to study mechanisms of pathogenesis and host defenses, and (c) current status of vaccine development.
Rho Protein: Roles and Mechanisms Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Pallabi Mitra, Gairika Ghosh, Md. Hafeezunnisa, Ranjan Sen
At the end of the multistep transcription process, the elongating RNA polymerase (RNAP) is dislodged from the DNA template either at specific DNA sequences, called the terminators, or by a nascent RNA-dependent helicase, Rho. In Escherichia coli, about half of the transcription events are terminated by the Rho protein. Rho utilizes its RNA-dependent ATPase activities to translocate along the mRNA and eventually dislodges the RNAP via an unknown mechanism. The transcription elongation factor NusG facilitates this termination process by directly interacting with Rho. In this review, we discuss current models describing the mechanism of action of this hexameric transcription terminator, its regulation by different cis and trans factors, and the effects of the termination process on physiological processes in bacterial cells, particularly E. coli and Salmonella enterica Typhimurium.
Present and Future of Culturing Bacteria Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Jörg Overmann, Birte Abt, Johannes Sikorski
The cultivation of bacteria is highly biased toward a few phylogenetic groups. Many of the currently underexplored bacterial lineages likely have novel biosynthetic pathways and unknown biochemical features. New cultivation concepts have been developed based on an improved understanding of the ecology of previously not-cultured bacteria. Particularly successful were improved media that mimic the natural types and concentrations of substrates and nutrients, high-throughput cultivation techniques, and approaches that exploit biofilm formation and bacterial interactions. Metagenomics and single-cell genomics can reveal unknown metabolic features of not-yet-cultured bacteria and, if complemented by culture-independent physiological analyses, will help to target functional novelty more efficiently. However, numerous novel types of bacteria that were initially enriched subsequently escaped isolation. Future cultivation work will therefore need to focus on improved subcultivation, purification, and preservation techniques to recover and utilize a larger fraction of microbial diversity.
The Colorful World of Extracellular Electron Shuttles Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Nathaniel R. Glasser, Scott H. Saunders, Dianne K. Newman
Descriptions of the changeable, striking colors associated with secreted natural products date back well over a century. These molecules can serve as extracellular electron shuttles (EESs) that permit microbes to access substrates at a distance. In this review, we argue that the colorful world of EESs has been too long neglected. Rather than simply serving as a diagnostic attribute of a particular microbial strain, redox-active natural products likely play fundamental, underappreciated roles in the biology of their producers, particularly those that inhabit biofilms. Here, we describe the chemical diversity and potential distribution of EES producers and users, discuss the costs associated with their biosynthesis, and critically evaluate strategies for their economical usage. We hope this review will inspire efforts to identify and explore the importance of EES cycling by a wide range of microorganisms so that their contributions to shaping microbial communities can be better assessed and exploited.
Molecular Evolution of Antifungal Drug Resistance Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2017-09-08 Nicole Robbins, Tavia Caplan, Leah E. Cowen
The fungal pathogens Candida albicans, Cryptococcus neoformans, and Aspergillus fumigatus have transitioned from a rare curiosity to a leading cause of human mortality. The management of infections caused by these organisms is intimately dependent on the efficacy of antifungal agents; however, fungi that are resistant to these treatments are regularly isolated in the clinic, impeding our ability to control infections. Given the significant impact fungal pathogens have on human health, it is imperative to understand the molecular mechanisms that govern antifungal drug resistance. This review describes our current knowledge of the mechanisms by which antifungal drug resistance evolves in experimental populations and clinical settings. We explore current antifungal treatment options and discuss promising strategies to impede the evolution of drug resistance. By tackling antifungal drug resistance as an evolutionary problem, there is potential to improve the utility of current treatments and accelerate the development of novel therapeutic strategies.
The Power of Asymmetry: Architecture and Assembly of the Gram-Negative Outer Membrane Lipid Bilayer Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 Jeremy C. Henderson, Shawn M. Zimmerman, Alexander A. Crofts, Joseph M. Boll, Lisa G. Kuhns, Carmen M. Herrera, M. Stephen Trent
Determining the chemical composition of biological materials is paramount to the study of natural phenomena. Here, we describe the composition of model gram-negative outer membranes, focusing on the predominant assembly, an asymmetrical bilayer of lipid molecules. We also give an overview of lipid biosynthetic pathways and molecular mechanisms that organize this material into the outer membrane bilayer. An emphasis is placed on the potential of these pathways as targets for antibiotic development. We discuss deviations in composition, through bacterial cell surface remodeling, and alternative modalities to the asymmetric lipid bilayer. Outer membrane lipid alterations of current microbiological interest, such as lipid structures found in commensal bacteria, are emphasized. Additionally, outer membrane components could potentially be engineered to develop vaccine platforms. Observations related to composition and assembly of gram-negative outer membranes will continue to generate novel discoveries, broaden biotechnologies, and reveal profound mysteries to compel future research.
The Modern Synthesis in the Light of Microbial Genomics Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 Austin Booth, Carlos Mariscal, W. Ford Doolittle
We review the theoretical implications of findings in genomics for evolutionary biology since the Modern Synthesis. We examine the ways in which microbial genomics has influenced our understanding of the last universal common ancestor, the tree of life, species, lineages, and evolutionary transitions. We conclude by advocating a piecemeal toolkit approach to evolutionary biology, in lieu of any grand unified theory updated to include microbial genomics.
Staphylococcus aureus RNAIII and Its Regulon Link Quorum Sensing, Stress Responses, Metabolic Adaptation, and Regulation of Virulence Gene Expression Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 Delphine Bronesky, Zongfu Wu, Stefano Marzi, Philippe Walter, Thomas Geissmann, Karen Moreau, François Vandenesch, Isabelle Caldelari, Pascale Romby
Staphylococcus aureus RNAIII is one of the main intracellular effectors of the quorum-sensing system. It is a multifunctional RNA that encodes a small peptide, and its noncoding parts act as antisense RNAs to regulate the translation and/or the stability of mRNAs encoding transcriptional regulators, major virulence factors, and cell wall metabolism enzymes. In this review, we explain how regulatory proteins and RNAIII are embedded in complex regulatory circuits to express virulence factors in a dynamic and timely manner in response to stress and environmental and metabolic changes.
Insights into the Coral Microbiome: Underpinning the Health and Resilience of Reef Ecosystems Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 David G. Bourne, Kathleen M. Morrow, Nicole S. Webster
Corals are fundamental ecosystem engineers, creating large, intricate reefs that support diverse and abundant marine life. At the core of a healthy coral animal is a dynamic relationship with microorganisms, including a mutually beneficial symbiosis with photosynthetic dinoflagellates (Symbiodinium spp.) and enduring partnerships with an array of bacterial, archaeal, fungal, protistan, and viral associates, collectively termed the coral holobiont. The combined genomes of this coral holobiont form a coral hologenome, and genomic interactions within the hologenome ultimately define the coral phenotype. Here we integrate contemporary scientific knowledge regarding the ecological, host-specific, and environmental forces shaping the diversity, specificity, and distribution of microbial symbionts within the coral holobiont, explore physiological pathways that contribute to holobiont fitness, and describe potential mechanisms for holobiont homeostasis. Understanding the role of the microbiome in coral resilience, acclimation, and environmental adaptation is a new frontier in reef science that will require large-scale collaborative research efforts.
Biological Diversity and Molecular Plasticity of FIC Domain Proteins Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 Alexander Harms, Frédéric V. Stanger, Christoph Dehio
The ubiquitous proteins with FIC (filamentation induced by cyclic AMP) domains use a conserved enzymatic machinery to modulate the activity of various target proteins by posttranslational modification, typically AMPylation. Following intensive study of the general properties of FIC domain catalysis, diverse molecular activities and biological functions of these remarkably versatile proteins are now being revealed. Here, we review the biological diversity of FIC domain proteins and summarize the underlying structure-function relationships. The original and most abundant genuine bacterial FIC domain proteins are toxins that use diverse molecular activities to interfere with bacterial physiology in various, yet ill-defined, biological contexts. Host-targeted virulence factors have evolved repeatedly out of this pool by exaptation of the enzymatic FIC domain machinery for the manipulation of host cell signaling in favor of bacterial pathogens. The single human FIC domain protein HypE (FICD) has a specific function in the regulation of protein stress responses.
Riboswitch-Mediated Gene Regulation: Novel RNA Architectures Dictate Gene Expression Responses Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 Anna V. Sherwood, Tina M. Henkin
Riboswitches are RNA elements that act on the mRNA with which they are cotranscribed to modulate expression of that mRNA. These elements are widely found in bacteria, where they have a broad impact on gene expression. The defining feature of riboswitches is that they directly recognize a physiological signal, and the resulting shift in RNA structure affects gene regulation. The majority of riboswitches respond to cellular metabolites, often in a feedback loop to repress synthesis of the enzymes used to produce the metabolite. Related elements respond to the aminoacylation status of a specific tRNA or to a physical parameter, such as temperature or pH. Recent studies have identified new classes of riboswitches and have revealed new insights into the molecular mechanisms of signal recognition and gene regulation. Application of structural and biophysical approaches has complemented previous genetic and biochemical studies, yielding new information about how different riboswitches operate.
Lessons from Digestive-Tract Symbioses Between Bacteria and Invertebrates Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 Joerg Graf
In most animals, digestive tracts harbor the greatest number of bacteria in the animal that contribute to its health: by aiding in the digestion of nutrients, provisioning essential nutrients and protecting against colonization by pathogens. Invertebrates have been used to enhance our understanding of metabolic processes and microbe-host interactions owing to experimental advantages. This review describes how advances in DNA sequencing technologies have dramatically altered how researchers investigate microbe-host interactions, including 16S rRNA gene surveys, metagenome experiments, and metatranscriptome studies. Advantages and challenges of each of these approaches are described herein. Hypotheses generated through omics studies can be directly tested using site-directed mutagenesis, and findings from transposon studies and site-directed experiments are presented. Finally, unique structural aspects of invertebrate digestive tracts that contribute to symbiont specificity are presented. The combination of omics approaches with genetics and microscopy allows researchers to move beyond correlations to identify conserved mechanisms of microbe-host interactions.
Gut Microbiota, Inflammation, and Colorectal Cancer Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 Caitlin A. Brennan, Wendy S. Garrett
Colorectal cancer is the second-leading cause of cancer-related deaths in the United States and fourth-leading cause of cancer-related deaths worldwide. While cancer is largely considered to be a disease of genetic and environmental factors, increasing evidence has demonstrated a role for the microbiota (the microorganisms associated with the human body) in shaping inflammatory environments and promoting tumor growth and spread. Herein, we discuss both human data from meta'omics analyses and data from mechanistic studies in cell culture and animal models that support specific bacterial agents as potentiators of tumorigenesis—including Fusobacterium nucleatum, enterotoxigenic Bacteroides fragilis, and colibactin-producing Escherichia coli. Further, we consider how microbes can be used in diagnosing colorectal cancer and manipulating the tumor environment to encourage better patient outcomes in response to immunotherapy treatments.
Autophagy Evasion and Endoplasmic Reticulum Subversion: The Yin and Yang of Legionella Intracellular Infection Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 Racquel Kim Sherwood, Craig R. Roy
The gram-negative bacterial pathogen Legionella pneumophila creates a novel organelle inside of eukaryotic host cells that supports intracellular replication. The L. pneumophila–containing vacuole evades fusion with lysosomes and interacts intimately with the host endoplasmic reticulum (ER). Although the natural hosts for L. pneumophila are free-living protozoa that reside in freshwater environments, the mechanisms that enable this pathogen to replicate intracellularly also function when mammalian macrophages phagocytose aerosolized bacteria, and infection of humans by L. pneumophila can result in a severe pneumonia called Legionnaires' disease. A bacterial type IVB secretion system called Dot/Icm is essential for intracellular replication of L. pneumophila. The Dot/Icm apparatus delivers over 300 different bacterial proteins into host cells during infection. These bacterial proteins have biochemical activities that target evolutionarily conserved host factors that control membrane transport processes, which results in the formation of the ER-derived vacuole that supports L. pneumophila replication. This review highlights research discoveries that have defined interactions between vacuoles containing L. pneumophila and the host ER. These studies reveal how L. pneumophila creates a vacuole that supports intracellular replication by subverting host proteins that control biogenesis and fusion of early secretory vesicles that exit the ER and host proteins that regulate the shape and dynamics of the ER. In addition to recruiting ER-derived membranes for biogenesis of the vacuole in which L. pneumophila replicates, these studies have revealed that this pathogen has a remarkable ability to interfere with the host's cellular process of autophagy, which is an ancient cell autonomous defense pathway that utilizes ER-derived membranes to target intracellular pathogens for destruction. Thus, this intracellular pathogen has evolved multiple mechanisms to control membrane transport processes that center on the involvement of the host ER.
(Per)chlorate in Biology on Earth and Beyond Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 Matthew D. Youngblut, Ouwei Wang, Tyler P. Barnum, John D. Coates
Respiration of perchlorate and chlorate [collectively, (per)chlorate] was only recognized in the last 20 years, yet substantial advances have been made in our understanding of the underlying metabolisms. Although it was once considered solely anthropogenic, pervasive natural sources, both terrestrial and extraterrestrial, indicate an ancient (per)chlorate presence across our solar system. These discoveries stimulated interest in (per)chlorate microbiology, and the application of advanced approaches highlights exciting new facets. Forward and reverse genetics revealed new information regarding underlying molecular biology and associated regulatory mechanisms. Structural and functional analysis characterized core enzymes and identified novel reaction sequences. Comparative genomics elucidated evolutionary aspects, and stress analysis identified novel response mechanisms to reactive chlorine species. Finally, systems biology identified unique metabolic versatility and novel mechanisms of (per)chlorate respiration, including symbiosis and a hybrid enzymatic-abiotic metabolism. While many published studies focus on (per)chlorate and their basic metabolism, this review highlights seminal advances made over the last decade and identifies new directions and potential novel applications.
Genomics of Natural Populations of Staphylococcus aureus Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 J. Ross Fitzgerald, Matthew T.G. Holden
Staphylococcus aureus is a major human pathogen and an important cause of livestock infections. The first S. aureus genomes to be published, 15 years ago, provided the first view of genome structure and gene content. Since then, thousands of genomes from a wide array of strains from different sources have been sequenced. Comparison of these sequences has resulted in broad insights into population structure, bacterial evolution, clone emergence and expansion, and the molecular basis of niche adaptation. Furthermore, this information is now being applied clinically in outbreak investigations to inform infection control measures and to determine appropriate treatment regimens. In this review, we summarize some of the broad insights into S. aureus biology gained from the analysis of genomes and discuss future directions and opportunities in this dynamic field of research.
Strolling Toward New Concepts Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 Koreaki Ito
For more than four decades now, I have been studying how genetic information is transformed into protein-based cellular functions. This has included investigations into the mechanisms supporting cellular localization of proteins, disulfide bond formation, quality control of membranes, and translation. I tried to extract new principles and concepts that are universal among living organisms from our observations of Escherichia coli. While I wanted to distill complex phenomena into basic principles, I also tried not to overlook any serendipitous observations. In the first part of this article, I describe personal experiences during my studies of the Sec pathway, which have centered on the SecY translocon. In the second part, I summarize my views of the recent revival of translation studies, which has given rise to the concept that nonuniform polypeptide chain elongation is relevant for the subsequent fates of newly synthesized proteins. Our studies of a class of regulatory nascent polypeptides advance this concept by showing that the dynamic behaviors of the extraribosomal part of the nascent chain affect the ongoing translation process. Vibrant and regulated molecular interactions involving the ribosome, mRNA, and nascent polypeptidyl-tRNA are based, at least partly, on their autonomously interacting properties.
Regulation of mRNA Decay in Bacteria Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 Bijoy K. Mohanty, Sidney R. Kushner
Gram-negative and gram-positive bacteria use a variety of enzymatic pathways to degrade mRNAs. Although several recent reviews have outlined these pathways, much less attention has been paid to the regulation of mRNA decay. The functional half-life of a particular mRNA, which affects how much protein is synthesized from it, is determined by a combination of multiple factors. These include, but are not necessarily limited to, (a) stability elements at either the 5′ or the 3′ terminus, (b) posttranscriptional modifications, (c) ribosome density on individual mRNAs, (d) small regulatory RNA (sRNA) interactions with mRNAs, (e) regulatory proteins that alter ribonuclease binding affinities, (f) the presence or absence of endonucleolytic cleavage sites, (g) control of intracellular ribonuclease levels, and (h) physical location within the cell. Changes in physiological conditions associated with environmental alterations can significantly alter the impact of these factors in the decay of a particular mRNA.
The Role of Microbial Electron Transfer in the Coevolution of the Biosphere and Geosphere Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 Benjamin I. Jelen, Donato Giovannelli, Paul G. Falkowski
All life on Earth is dependent on biologically mediated electron transfer (i.e., redox) reactions that are far from thermodynamic equilibrium. Biological redox reactions originally evolved in prokaryotes and ultimately, over the first ∼2.5 billion years of Earth's history, formed a global electronic circuit. To maintain the circuit on a global scale requires that oxidants and reductants be transported; the two major planetary wires that connect global metabolism are geophysical fluids—the atmosphere and the oceans. Because all organisms exchange gases with the environment, the evolution of redox reactions has been a major force in modifying the chemistry at Earth's surface. Here we briefly review the discovery and consequences of redox reactions in microbes with a specific focus on the coevolution of life and geochemical phenomena.
Genetic Mapping of Pathogenesis Determinants in Toxoplasma gondii Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 Michael S. Behnke, J.P. Dubey, L. David Sibley
Toxoplasma gondii is a widespread parasite of warm-blooded vertebrates that also causes opportunistic infections in humans. Rodents are a natural host for asexually replicating forms, whereas cats serve as the definitive host for sexual development. The laboratory mouse provides a model to study pathogenesis. Strains of T. gondii are globally diverse, with more than 16 distinct haplogroups clustered into 6 major clades. Forward genetic analysis of genetic crosses between different lineages has been used to define the molecular basis of acute virulence in the mouse. These studies have identified a family of secretory serine/threonine rhoptry kinases that target innate immune pathways to protect intracellular parasites from destruction. Rhoptry kinases target immunity-related GTPases, a family of immune effectors that is expanded in rodents. Similar forward genetic studies may be useful to define the basis of pathogenesis in other hosts, including humans, where infections of different strains present with variable clinical severity.
The Phage Shock Protein Response Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 Josué Flores-Kim, Andrew J. Darwin
The phage shock protein (Psp) system was identified as a response to phage infection in Escherichia coli, but rather than being a specific response to a phage, it detects and mitigates various problems that could increase inner-membrane (IM) permeability. Interest in the Psp system has increased significantly in recent years due to appreciation that Psp-like proteins are found in all three domains of life and because the bacterial Psp response has been linked to virulence and other important phenotypes. In this article, we summarize our current understanding of what the Psp system detects and how it detects it, how four core Psp proteins form a signal transduction cascade between the IM and the cytoplasm, and current ideas that explain how the Psp response keeps bacterial cells alive. Although recent studies have significantly improved our understanding of this system, it is an understanding that is still far from complete.
Feedback Control of Two-Component Regulatory Systems Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 Eduardo A. Groisman
Two-component systems are a dominant form of bacterial signal transduction. The prototypical two-component system consists of a sensor that responds to a specific input(s) by modifying the output of a cognate regulator. Because the output of a two-component system is the amount of phosphorylated regulator, feedback mechanisms may alter the amount of regulator, and/or modify the ability of a sensor or other proteins to alter the phosphorylation state of the regulator. Two-component systems may display intrinsic feedback whereby the amount of phosphorylated regulator changes under constant inducing conditions and without the participation of additional proteins. Feedback control allows a two-component system to achieve particular steady-state levels, to reach a given steady state with distinct dynamics, to express coregulated genes in a given order, and to activate a regulator to different extents, depending on the signal acting on the sensor.
Metagenomics and the Human Virome in Asymptomatic Individuals Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 Nicolás Rascovan, Raja Duraisamy, Christelle Desnues
High-throughput sequencing technologies have revolutionized how we think about viruses. Investigators can now go beyond pathogenic viruses and have access to the thousands of viruses that inhabit our bodies without causing clinical symptoms. By studying their interactions with each other, with other microbes, and with host genetics and immune systems, we can learn how they affect health and disease. This article reviews current knowledge of the composition and diversity of the human virome in physiologically healthy individuals. It focuses on recent results from metagenomics studies and discusses the contribution of bacteriophages and eukaryotic viruses to human health.
Kin Recognition in Bacteria Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 Daniel Wall
The ability of bacteria to recognize kin provides a means to form social groups. In turn these groups can lead to cooperative behaviors that surpass the ability of the individual. Kin recognition involves specific biochemical interactions between a receptor(s) and an identification molecule(s). Recognition specificity, ensuring that nonkin are excluded and kin are included, is critical and depends on the number of loci and polymorphisms involved. After recognition and biochemical perception, the common ensuing cooperative behaviors include biofilm formation, quorum responses, development, and swarming motility. Although kin recognition is a fundamental mechanism through which cells might interact, microbiologists are only beginning to explore the topic. This review considers both molecular and theoretical aspects of bacterial kin recognition. Consideration is also given to bacterial diversity, genetic relatedness, kin selection theory, and mechanisms of recognition.
Protists and the Wild, Wild West of Gene Expression: New Frontiers, Lawlessness, and Misfits Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 David Roy Smith, Patrick J. Keeling
The DNA double helix has been called one of life's most elegant structures, largely because of its universality, simplicity, and symmetry. The expression of information encoded within DNA, however, can be far from simple or symmetric and is sometimes surprisingly variable, convoluted, and wantonly inefficient. Although exceptions to the rules exist in certain model systems, the true extent to which life has stretched the limits of gene expression is made clear by nonmodel systems, particularly protists (microbial eukaryotes). The nuclear and organelle genomes of protists are subject to the most tangled forms of gene expression yet identified. The complicated and extravagant picture of the underlying genetics of eukaryotic microbial life changes how we think about the flow of genetic information and the evolutionary processes shaping it. Here, we discuss the origins, diversity, and growing interest in noncanonical protist gene expression and its relationship to genomic architecture.
Molecular Genetic Analysis of Chlamydia Species Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 Barbara S. Sixt, Raphael H. Valdivia
Species of Chlamydia are the etiologic agent of endemic blinding trachoma, the leading cause of bacterial sexually transmitted diseases, significant respiratory pathogens, and a zoonotic threat. Their dependence on an intracellular growth niche and their peculiar developmental cycle are major challenges to elucidating their biology and virulence traits. The last decade has seen tremendous advances in our ability to perform a molecular genetic analysis of Chlamydia species. Major achievements include the generation of large collections of mutant strains, now available for forward- and reverse-genetic applications, and the introduction of a system for plasmid-based transformation enabling complementation of mutations; expression of foreign, modified, or reporter genes; and even targeted gene disruptions. This review summarizes the current status of the molecular genetic toolbox for Chlamydia species and highlights new insights into their biology and new challenges in the nascent field of Chlamydia genetics.
Xenogeneic Silencing and Its Impact on Bacterial Genomes Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 Kamna Singh, Joshua N. Milstein, William Wiley Navarre
The H-NS (heat-stable nucleoid structuring) protein affects both nucleoid compaction and global gene regulation. H-NS appears to act primarily as a silencer of AT-rich genetic material acquired by horizontal gene transfer. As such, it is key in the regulation of most genes involved in virulence and in adaptation to new environmental niches. Here we review recent progress in understanding the biochemistry of H-NS and how xenogeneic silencing affects bacterial evolution. We highlight the strengths and weaknesses of some of the models proposed in H-NS-mediated nucleoprotein complex formation. Based on recent single-molecule studies, we also propose a novel mode of DNA compaction by H-NS termed intrabridging to explain over two decades of observations of the H-NS molecule.
The Atacama Desert: Technical Resources and the Growing Importance of Novel Microbial Diversity Annu. Rev. Microbiol. (IF 9.415) Pub Date : 2016-09-08 Alan T. Bull, Juan A. Asenjo, Michael Goodfellow, Benito Gómez-Silva
The Atacama Desert of northern Chile is the oldest and most arid nonpolar environment on Earth. It is a coastal desert covering approximately 180,000 km2, and together with the greater Atacama region it comprises a dramatically wide range of ecological niches. Long known and exploited for its mineral resources, the Atacama Desert harbors a rich microbial diversity that has only recently been discovered; the great majority of it has not yet been recovered in culture or even taxonomically identified. This review traces the progress of microbiology research in the Atacama and dispels the popular view that this region is virtually devoid of life. We examine reasons for such research activity and demonstrate that microbial life is the latest recognized and least explored resource in this inspiring biome.
Some contents have been Reproduced by permission of The Royal Society of Chemistry.
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