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Annual Review of Microbiology - Volume 71, 2017
Volume 71, 2017
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Bacterial Cell Division: Nonmodels Poised to Take the Spotlight
Vol. 71 (2017), pp. 393–411More LessThe 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.
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Histone Methylation by SET Domain Proteins in Fungi
Vol. 71 (2017), pp. 413–439More LessHistone-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.
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Predator Versus Pathogen: How Does Predatory Bdellovibrio bacteriovorus Interface with the Challenges of Killing Gram-Negative Pathogens in a Host Setting?
Vol. 71 (2017), pp. 441–457More LessBdellovibrio 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.
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Germination of Spores of the Orders Bacillales and Clostridiales
Vol. 71 (2017), pp. 459–477More LessDormant 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.
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Microbial Expansins
Vol. 71 (2017), pp. 479–497More LessExpansins 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.
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Bacterial Cell Size: Multifactorial and Multifaceted
Vol. 71 (2017), pp. 499–517More LessHow 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.
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Bacterial Membranes: Structure, Domains, and Function
Vol. 71 (2017), pp. 519–538More LessThe 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.
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Outer Membrane Biogenesis
Vol. 71 (2017), pp. 539–556More LessThe 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.
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Rewriting the Genetic Code
Vol. 71 (2017), pp. 557–577More LessThe 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.
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Evolutionary Trajectories to Antibiotic Resistance
Vol. 71 (2017), pp. 579–596More LessThe 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.
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Copper Acquisition and Utilization in Fungi
Vol. 71 (2017), pp. 597–623More LessFungal 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.
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Variant Gene Expression and Antigenic Variation by Malaria Parasites
Vol. 71 (2017), pp. 625–641More LessMalaria 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.
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Syntrophy Goes Electric: Direct Interspecies Electron Transfer
Vol. 71 (2017), pp. 643–664More LessDirect 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.
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Neisseria gonorrhoeae: Drug Resistance, Mouse Models, and Vaccine Development
Vol. 71 (2017), pp. 665–686More LessGonorrhea, 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.
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Rho Protein: Roles and Mechanisms
Vol. 71 (2017), pp. 687–709More LessAt 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.
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Present and Future of Culturing Bacteria
Vol. 71 (2017), pp. 711–730More LessThe 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.
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The Colorful World of Extracellular Electron Shuttles
Vol. 71 (2017), pp. 731–751More LessDescriptions 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.
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Molecular Evolution of Antifungal Drug Resistance
Vol. 71 (2017), pp. 753–775More LessThe 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.
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Previous Volumes
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Volume 77 (2023)
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Volume 76 (2022)
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Volume 75 (2021)
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Volume 74 (2020)
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Volume 73 (2019)
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Volume 72 (2018)
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Volume 71 (2017)
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Volume 70 (2016)
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Volume 69 (2015)
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Volume 68 (2014)
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Volume 67 (2013)
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Volume 66 (2012)
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Volume 65 (2011)
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Volume 64 (2010)
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Volume 63 (2009)
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Volume 62 (2008)
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Volume 61 (2007)
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Volume 60 (2006)
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Volume 59 (2005)
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Volume 58 (2004)
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Volume 57 (2003)
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Volume 56 (2002)
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Volume 55 (2001)
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Volume 54 (2000)
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Volume 53 (1999)
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Volume 52 (1998)
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Volume 51 (1997)
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Volume 50 (1996)
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Volume 49 (1995)
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Volume 48 (1994)
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Volume 47 (1993)
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Volume 46 (1992)
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Volume 45 (1991)
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Volume 44 (1990)
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Volume 43 (1989)
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Volume 42 (1988)
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Volume 41 (1987)
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Volume 40 (1986)
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Volume 39 (1985)
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Volume 38 (1984)
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Volume 37 (1983)
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Volume 36 (1982)
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Volume 35 (1981)
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Volume 34 (1980)
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Volume 33 (1979)
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Volume 32 (1978)
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Volume 31 (1977)
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Volume 30 (1976)
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Volume 29 (1975)
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Volume 28 (1974)
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Volume 27 (1973)
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Volume 26 (1972)
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Volume 25 (1971)
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Volume 24 (1970)
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Volume 23 (1969)
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Volume 22 (1968)
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Volume 21 (1967)
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Volume 20 (1966)
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Volume 19 (1965)
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Volume 18 (1964)
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Volume 17 (1963)
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Volume 16 (1962)
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Volume 15 (1961)
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Volume 14 (1960)
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Volume 13 (1959)
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Volume 12 (1958)
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Volume 11 (1957)
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Volume 10 (1956)
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Volume 9 (1955)
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Volume 8 (1954)
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Volume 7 (1953)
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Volume 6 (1952)
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Volume 5 (1951)
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Volume 4 (1950)
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Volume 3 (1949)
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Volume 2 (1948)
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Volume 1 (1947)
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Volume 0 (1932)