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- Volume 69, 2015
Annual Review of Microbiology - Volume 69, 2015
Volume 69, 2015
- Preface
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My Lifelong Passion for Biochemistry and Anaerobic Microorganisms
Vol. 69 (2015), pp. 1–30More LessEarly parental influence led me first to medical school, but after developing a passion for biochemistry and sensing the need for a deeper foundation, I changed to chemistry. During breaks between semesters, I worked in various biochemistry labs to acquire a feeling for the different areas of investigation. The scientific puzzle that fascinated me most was the metabolism of the anaerobic bacterium Clostridium kluyveri, which I took on in 1965 in Karl Decker's lab in Freiburg, Germany. I quickly realized that little was known about the biochemistry of strict anaerobes such as clostridia, methanogens, acetogens, and sulfate-reducing bacteria and that these were ideal model organisms to study fundamental questions of energy conservation, CO2 fixation, and the evolution of metabolic pathways. My passion for anaerobes was born then and is unabated even after 50 years of study.
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The Pyromaniac Inside You: Salmonella Metabolism in the Host Gut
Vol. 69 (2015), pp. 31–48More LessA metabolically diverse microbial community occupies all available nutrient-niches in the lumen of the mammalian intestine, making it difficult for pathogens to establish themselves in this highly competitive environment. Salmonella serovars sidestep the competition by using their virulence factors to coerce the host into creating a novel nutrient-niche. Inflammation-derived nutrients available in this new niche support a bloom of Salmonella serovars, thereby ensuring transmission of the pathogen to the next susceptible host by the fecal-oral route. Here we review the anaerobic food chain that characterizes resident gut-associated microbial communities along with the winning metabolic strategy Salmonella serovars use to edge out competing microbes in the inflamed intestine.
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Regulation of Transcript Elongation
Vol. 69 (2015), pp. 49–69More LessBacteria lack subcellular compartments and harbor a single RNA polymerase that synthesizes both structural and protein-coding RNAs, which are cotranscriptionally processed by distinct pathways. Nascent rRNAs fold into elaborate secondary structures and associate with ribosomal proteins, whereas nascent mRNAs are translated by ribosomes. During elongation, nucleic acid signals and regulatory proteins modulate concurrent RNA-processing events, instruct RNA polymerase where to pause and terminate transcription, or act as roadblocks to the moving enzyme. Communications among complexes that carry out transcription, translation, repair, and other cellular processes ensure timely execution of the gene expression program and survival under conditions of stress. This network is maintained by auxiliary proteins that act as bridges between RNA polymerase, ribosome, and repair enzymes, blurring boundaries between separate information-processing steps and making assignments of unique regulatory functions meaningless. Understanding the regulation of transcript elongation thus requires genome-wide approaches, which confirm known and reveal new regulatory connections.
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Candida albicans Biofilms and Human Disease
Vol. 69 (2015), pp. 71–92More LessIn humans, microbial cells (including bacteria, archaea, and fungi) greatly outnumber host cells. Candida albicans is the most prevalent fungal species of the human microbiota; this species asymptomatically colonizes many areas of the body, particularly the gastrointestinal and genitourinary tracts of healthy individuals. Alterations in host immunity, stress, resident microbiota, and other factors can lead to C. albicans overgrowth, causing a wide range of infections, from superficial mucosal to hematogenously disseminated candidiasis. To date, most studies of C. albicans have been carried out in suspension cultures; however, the medical impact of C. albicans (like that of many other microorganisms) depends on its ability to thrive as a biofilm, a closely packed community of cells. Biofilms are notorious for forming on implanted medical devices, including catheters, pacemakers, dentures, and prosthetic joints, which provide a surface and sanctuary for biofilm growth. C. albicans biofilms are intrinsically resistant to conventional antifungal therapeutics, the host immune system, and other environmental perturbations, making biofilm-based infections a significant clinical challenge. Here, we review our current knowledge of biofilms formed by C. albicans and closely related fungal species.
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Transcription Factors That Defend Bacteria Against Reactive Oxygen Species
Vol. 69 (2015), pp. 93–108More LessBacteria live in a toxic world in which their competitors excrete hydrogen peroxide or superoxide-generating redox-cycling compounds. They protect themselves by activating regulons controlled by the OxyR, PerR, and SoxR transcription factors. OxyR and PerR sense peroxide when it oxidizes key thiolate or iron moieties, respectively; they then induce overlapping sets of proteins that defend their vulnerable metalloenzymes. An additional role for OxyR in detecting electrophilic compounds is possible. In some nonenteric bacteria, SoxR appears to control the synthesis and export of redox-cycling compounds, whereas in the enteric bacteria it defends the cell against the same agents. When these compounds oxidize its iron-sulfur cluster, SoxR induces proteins that exclude, excrete, or modify them. It also induces enzymes that defend the cell against the superoxide that such compounds make. Recent work has brought new insight into the biochemistry and physiology of these responses, and comparative studies have clarified their evolutionary histories.
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Bacterial Proteasomes
Vol. 69 (2015), pp. 109–127More LessInterest in bacterial proteasomes was sparked by the discovery that proteasomal degradation is required for the pathogenesis of Mycobacterium tuberculosis, one of the world's deadliest pathogens. Although bacterial proteasomes are structurally similar to their eukaryotic and archaeal homologs, there are key differences in their mechanisms of assembly, activation, and substrate targeting for degradation. In this article, we compare and contrast bacterial proteasomes with their archaeal and eukaryotic counterparts, and we discuss recent advances in our understanding of how bacterial proteasomes function to influence microbial physiology.
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The Organellar Genomes of Chromera and Vitrella, the Phototrophic Relatives of Apicomplexan Parasites
Vol. 69 (2015), pp. 129–144More LessApicomplexa are known to contain greatly reduced organellar genomes. Their mitochondrial genome carries only three protein-coding genes, and their plastid genome is reduced to a 35-kb-long circle. The discovery of coral-endosymbiotic algae Chromera velia and Vitrella brassicaformis, which share a common ancestry with Apicomplexa, provided an opportunity to study possibly ancestral forms of organellar genomes, a unique glimpse into the evolutionary history of apicomplexan parasites. The structurally similar mitochondrial genomes of Chromera and Vitrella differ in gene content, which is reflected in the composition of their respiratory chains. Thus, Chromera lacks respiratory complexes I and III, whereas Vitrella and apicomplexan parasites are missing only complex I. Plastid genomes differ substantially between these algae, particularly in structure: The Chromera plastid genome is a linear, 120-kb molecule with large and divergent genes, whereas the plastid genome of Vitrella is a highly compact circle that is only 85 kb long but nonetheless contains more genes than that of Chromera. It appears that organellar genomes have already been reduced in free-living phototrophic ancestors of apicomplexan parasites, and such reduction is not associated with parasitism.
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The Gut Microbiota of Termites: Digesting the Diversity in the Light of Ecology and Evolution
Vol. 69 (2015), pp. 145–166More LessTermite guts harbor a dense and diverse microbiota that is essential for symbiotic digestion. The major players in lower termites are unique lineages of cellulolytic flagellates, whereas higher termites harbor only bacteria and archaea. The functions of the mostly uncultivated lineages and their distribution in different diet groups are slowly emerging. Patterns in community structure match changes in the biology of different host groups and reflect the availability of microbial habitats provided by flagellates, wood fibers, and the increasing differentiation of the intestinal tract, which also creates new niches for microbial symbionts. Whereas the intestinal communities in the closely related cockroaches seem to be shaped primarily by the selective forces of microhabitat and functional niche, the social behavior of termites reduces the stochastic element of community assembly, which facilitates coevolution and may ultimately result in cospeciation.
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Microsporidia: Eukaryotic Intracellular Parasites Shaped by Gene Loss and Horizontal Gene Transfers
Vol. 69 (2015), pp. 167–183More LessMicrosporidia are eukaryotic parasites of many animals that appear to have adapted to an obligate intracellular lifestyle by modifying the morphology and content of their cells. Living inside other cells, they have lost many, or all, metabolic functions, resulting in genomes that are always gene poor and often very small. The minute content of microsporidian genomes led many to assume that these parasites are biochemically static and uninteresting. However, recent studies have demonstrated that these organisms can be surprisingly complex and dynamic. In this review I detail the most significant recent advances in microsporidian genomics and discuss how these have affected our understanding of many biological aspects of these peculiar eukaryotic intracellular pathogens.
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Anthrax Pathogenesis*
Vol. 69 (2015), pp. 185–208More LessAnthrax is caused by the spore-forming, gram-positive bacterium Bacillus anthracis. The bacterium's major virulence factors are (a) the anthrax toxins and (b) an antiphagocytic polyglutamic capsule. These are encoded by two large plasmids, the former by pXO1 and the latter by pXO2. The expression of both is controlled by the bicarbonate-responsive transcriptional regulator, AtxA. The anthrax toxins are three polypeptides—protective antigen (PA), lethal factor (LF), and edema factor (EF)—that come together in binary combinations to form lethal toxin and edema toxin. PA binds to cellular receptors to translocate LF (a protease) and EF (an adenylate cyclase) into cells. The toxins alter cell signaling pathways in the host to interfere with innate immune responses in early stages of infection and to induce vascular collapse at late stages. This review focuses on the role of anthrax toxins in pathogenesis. Other virulence determinants, as well as vaccines and therapeutics, are briefly discussed.
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CRISPR-Cas: New Tools for Genetic Manipulations from Bacterial Immunity Systems
Vol. 69 (2015), pp. 209–228More LessProkaryotic CRISPR-Cas loci encode proteins that function as an adaptive immune system against infectious viruses and plasmids. Immunity is mediated by Cas nucleases and small RNA guides, which specify a cleavage site within the genome of the invader. In type II CRISPR-Cas systems, the RNA-guided Cas9 nuclease cleaves the DNA. Cas9 can be reprogrammed to create double-strand DNA breaks in the genomes of a variety of organisms, from bacteria to human cells. Repair of Cas9 lesions by homologous recombination or nonhomologous end joining mechanisms can lead to the introduction of specific nucleotide substitutions or indel mutations, respectively. Furthermore, a nuclease-null Cas9 has been developed to regulate endogenous gene expression and to label genomic loci in living cells. Targeted genome editing and gene regulation mediated by Cas9 are easy to program, scale, and multiplex, allowing researchers to decipher the causal link between genetic and phenotypic variation. In this review, we describe the most notable applications of Cas9 in basic biology, translational medicine, synthetic biology, biotechnology, and other fields.
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Perception and Homeostatic Control of Iron in the Rhizobia and Related Bacteria
Vol. 69 (2015), pp. 229–245More LessIron is an essential nutrient, but it can also be toxic. Therefore, iron homeostasis must be strictly regulated. Transcriptional control of iron-dependent gene expression in the rhizobia and other taxa of the Alphaproteobacteria is fundamentally different from the Fur paradigm in Escherichia coli and other model systems. Rather than sense iron directly, the rhizobia employ the iron response regulator (Irr) to monitor and respond to the status of an iron-dependent process, namely, heme biosynthesis. This novel control mechanism allows iron homeostasis to be integrated with other cellular processes, and it permits differential control of iron regulon genes in a manner not readily achieved by Fur. Moreover, studies of Irr have defined a role for heme in conditional protein stability that has been subsequently described in eukaryotes. Finally, Irr-mediated control of iron metabolism may reflect a cellular strategy that accommodates a greater reliance on manganese.
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Thymineless Death Lives On: New Insights into a Classic Phenomenon
Vol. 69 (2015), pp. 247–263More LessThe primary mechanisms by which bacteria lose viability when deprived of thymine have been elusive for over half a century. Early research focused on stalled replication forks and the deleterious effects of uracil incorporation into DNA from thymidine-deficient nucleotide pools. The initiation of the replication cycle and origin-proximal DNA degradation during thymine starvation have now been quantified via whole-genome microarrays and other approaches. These advances have fostered innovative models and informative experiments in bacteria since this topic was last reviewed. Given that thymineless death is similar in mammalian cells and that certain antibacterial and chemotherapeutic drugs elicit thymine deficiency, a mechanistic understanding of this phenomenon might have valuable biomedical applications.
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Membrane-Coupled mRNA Trafficking in Fungi
Vol. 69 (2015), pp. 265–281More LessIntracellular logistics are essential for delivery of newly synthesized material during polar growth of fungal hyphae. Proteins and lipids are actively transported throughout the cell by motor-dependent movement of small vesicles or larger units such as endosomes and the endoplasmic reticulum. A remarkably tight link is emerging between active membrane trafficking and mRNA transport, a process that determines the precise subcellular localization of translation products within the cell. Here, we report on recent insights into the mechanism and biological role of these intricate cotransport processes in fungal models such as Saccharomyces cerevisiae, Candida albicans, and Ustilago maydis. In the latter, we focus on the new finding of endosomal mRNA transport and its implications for protein targeting, complex assembly, and septin biology.
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Molecular Pathogenesis of Ehrlichia chaffeensis Infection
Vol. 69 (2015), pp. 283–304More LessEhrlichia chaffeensis is an obligatory intracellular and cholesterol-dependent bacterium that has evolved special proteins and functions to proliferate inside leukocytes and cause disease. E. chaffeensis has a multigene family of major outer membrane proteins with porin activity and induces infectious entry using its entry-triggering protein to bind the human cell surface protein DNase X. During intracellular replication, three functional pairs of two-component systems are sequentially expressed to regulate metabolism, aggregation, and the development of stress-resistance traits for transmission. A type IV secretion effector of E. chaffeensis blocks mitochondrion-mediated host cell apoptosis. Several type I secretion proteins are secreted at the Ehrlichia–host interface. E. chaffeensis strains induce strikingly variable inflammation in mice. The central role of MyD88, but not Toll-like receptors, suggests that Ehrlichia species have unique inflammatory molecules. A recent report about transient targeted mutagenesis and random transposon mutagenesis suggests that stable targeted knockouts may become feasible in Ehrlichia.
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Microbiology Meets Big Data: The Case of Gut Microbiota–Derived Trimethylamine
Vol. 69 (2015), pp. 305–321More LessDuring the past decade, meta-omics approaches have revolutionized microbiology, allowing for a cultivation-free assessment of the composition and functional properties of entire microbial ecosystems. On the one hand, a phylogenetic and functional interpretation of such data relies on accumulated genetic, biochemical, metabolic, and phenotypic characterization of microbial variation. On the other hand, the increasing availability of extensive microbiome data sets and corresponding metadata provides a vast, underused resource for the microbiology field as a whole. To demonstrate the potential for integrating big data into a functional microbiology workflow, we review literature on trimethylamine (TMA), a microbiota-generated metabolite linked to atherosclerosis development. Translating recently elucidated microbial pathways resulting in TMA production into genomic orthologs, we demonstrate how to mine for their presence in public (meta-) genomic databases and link findings to associated metadata. Reviewing pathway abundance in public data sets shows that TMA production potential is associated with symptomatic atherosclerosis and allows identification of currently uncharacterized TMA-producing bacteria.
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The Unique Molecular Choreography of Giant Pore Formation by the Cholesterol-Dependent Cytolysins of Gram-Positive Bacteria
Vol. 69 (2015), pp. 323–340More LessThe mechanism by which the cholesterol-dependent cytolysins (CDCs) assemble their giant β-barrel pore in cholesterol-rich membranes has been the subject of intense study in the past two decades. A combination of structural, biophysical, and biochemical analyses has revealed deep insights into the series of complex and highly choreographed secondary and tertiary structural transitions that the CDCs undergo to assemble their β-barrel pore in eukaryotic membranes. Our knowledge of the molecular details of these dramatic structural changes in CDCs has transformed our understanding of how giant pore complexes are assembled and has been critical to our understanding of the mechanisms of other important classes of pore-forming toxins and proteins across the kingdoms of life. Finally, there are tantalizing hints that the CDC pore-forming mechanism is more sophisticated than previously imagined and that some CDCs are employed in pore-independent processes.
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Ion Regulation in the Malaria Parasite
Vol. 69 (2015), pp. 341–359More LessSome hours after invading the erythrocytes of its human host, the malaria parasite Plasmodium falciparum induces an increase in the permeability of the erythrocyte membrane to monovalent ions. The resulting net influx of Na+ and net efflux of K+, down their respective concentration gradients, converts the erythrocyte cytosol from an initially high-K+, low-Na+ solution to a high-Na+, low-K+ solution. The intraerythrocytic parasite itself exerts tight control over its internal Na+, K+, Cl−, and Ca2+ concentrations and its intracellular pH through the combined actions of a range of membrane transport proteins. The molecular mechanisms underpinning ion regulation in the parasite are receiving increasing attention, not least because PfATP4, a P-type ATPase postulated to be involved in Na+ regulation, has emerged as a potential antimalarial drug target, susceptible to inhibition by a wide range of chemically unrelated compounds.
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Physics of Intracellular Organization in Bacteria
Vol. 69 (2015), pp. 361–379More LessWith the realization that bacteria achieve exquisite levels of spatiotemporal organization has come the challenge of discovering the underlying mechanisms. In this review, we describe three classes of such mechanisms, each of which has physical origins: the use of landmarks, the creation of higher-order structures that enable geometric sensing, and the emergence of length scales from systems of chemical reactions coupled to diffusion. We then examine the diversity of geometric cues that exist even in cells with relatively simple geometries, and end by discussing both new technologies that could drive further discovery and the implications of our current knowledge for the behavior, fitness, and evolution of bacteria. The organizational strategies described here are employed in a wide variety of systems and in species across all kingdoms of life; in many ways they provide a general blueprint for organizing the building blocks of life.
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Previous Volumes
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Volume 78 (2024)
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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)