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- Volume 74, 2020
Annual Review of Microbiology - Volume 74, 2020
Volume 74, 2020
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A Tale of Good Fortune in the Era of DNA
Vol. 74 (2020), pp. 1–19More LessTwo strains of good fortune in my career were to stumble upon the Watson–Gilbert laboratory at Harvard when I entered graduate school in 1964, and to study gene regulation in bacteriophage λ when I was there. λ was almost entirely a genetic item a few years before, awaiting biochemical incarnation. Throughout my career I was a relentless consumer of the work of previous and current generations of λ geneticists. Empowered by this background, my laboratory made contributions in two areas. The first was regulation of early gene transcription in λ, the study of which began with the discovery of the Rho transcription termination factor, and the regulatory mechanism of transcription antitermination by the λ N protein, subjects of my thesis work. This was developed into a decades-long program during my career at Cornell, studying the mechanism of transcription termination and antitermination. The second area was the classic problem of prophage induction in response to cellular DNA damage, the study of which illuminated basic cellular processes to survive DNA damage.
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Structures and Strategies of Anti-CRISPR-Mediated Immune Suppression
Vol. 74 (2020), pp. 21–37More LessMore than 50 protein families have been identified that inhibit CRISPR (clustered regularly interspaced short palindromic repeats)-Cas-mediated adaptive immune systems. Here, we analyze the available anti-CRISPR (Acr) structures and describe common themes and unique mechanisms of stoichiometric and enzymatic suppressors of CRISPR-Cas. Stoichiometric inhibitors often function as molecular decoys of protein-binding partners or nucleic acid targets, while enzymatic suppressors covalently modify Cas ribonucleoprotein complexes or degrade immune signaling molecules. We review mechanistic insights that have been revealed by structures of Acrs, discuss some of the trade-offs associated with each of these strategies, and highlight how Acrs are regulated and deployed in the race to overcome adaptive immunity.
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Ape Origins of Human Malaria
Vol. 74 (2020), pp. 39–63More LessAfrican apes harbor at least twelve Plasmodium species, some of which have been a source of human infection. It is now well established that Plasmodium falciparum emerged following the transmission of a gorilla parasite, perhaps within the last 10,000 years, while Plasmodium vivax emerged earlier from a parasite lineage that infected humans and apes in Africa before the Duffy-negative mutation eliminated the parasite from humans there. Compared to their ape relatives, both human parasites have greatly reduced genetic diversity and an excess of nonsynonymous mutations, consistent with severe genetic bottlenecks followed by rapid population expansion. A putative new Plasmodium species widespread in chimpanzees, gorillas, and bonobos places the origin of Plasmodium malariae in Africa. Here, we review what is known about the origins and evolutionary history of all human-infective Plasmodium species, the time and circumstances of their emergence, and the diversity, host specificity, and zoonotic potential of their ape counterparts.
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Archaeal DNA Replication
Vol. 74 (2020), pp. 65–80More LessIt is now well recognized that the information processing machineries of archaea are far more closely related to those of eukaryotes than to those of their prokaryotic cousins, the bacteria. Extensive studies have been performed on the structure and function of the archaeal DNA replication origins, the proteins that define them, and the macromolecular assemblies that drive DNA unwinding and nascent strand synthesis. The results from various archaeal organisms across the archaeal domain of life show surprising levels of diversity at many levels—ranging from cell cycle organization to chromosome ploidy to replication mode and nature of the replicative polymerases. In the following, we describe recent advances in the field, highlighting conserved features and lineage-specific innovations.
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The Plant Microbiome: From Ecology to Reductionism and Beyond
Vol. 74 (2020), pp. 81–100More LessMethodological advances over the past two decades have propelled plant microbiome research, allowing the field to comprehensively test ideas proposed over a century ago and generate many new hypotheses. Studying the distribution of microbial taxa and genes across plant habitats has revealed the importance of various ecological and evolutionary forces shaping plant microbiota. In particular, selection imposed by plant habitats strongly shapes the diversity and composition of microbiota and leads to microbial adaptation associated with navigating the plant immune system and utilizing plant-derived resources. Reductionist approaches have demonstrated that the interaction between plant immunity and the plant microbiome is, in fact, bidirectional and that plants, microbiota, and the environment shape a complex chemical dialogue that collectively orchestrates the plantmicrobiome. The next stage in plant microbiome research will require the integration of ecological and reductionist approaches to establish a general understanding of the assembly and function in both natural and managed environments.
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Fungal Volatile Organic Compounds: More Than Just a Funky Smell?
Vol. 74 (2020), pp. 101–116More LessMany volatile organic compounds (VOCs) associated with industry cause adverse health effects, but less is known about the physiological effects of biologically produced volatiles. This review focuses on the VOCs emitted by fungi, which often have characteristic moldy or “mushroomy” odors. One of the most common fungal VOCs, 1-octen-3-ol, is a semiochemical for many arthropod species and also serves as a developmental hormone for several fungal groups. Other fungal VOCs are flavor components of foods and spirits or are assayed in indirect methods for detecting the presence of mold in stored agricultural produce and water-damaged buildings. Fungal VOCs function as antibiotics as well as defense and plant-growth-promoting agents and have been implicated in a controversial medical condition known as sick building syndrome. In this review, we draw attention to the ubiquity, diversity, and toxicological significance of fungal VOCs as well as some of their ecological roles.
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What Is Metagenomics Teaching Us, and What Is Missed?
Vol. 74 (2020), pp. 117–135More LessShotgun metagenomic sequencing has revolutionized our ability to detect and characterize the diversity and function of complex microbial communities. In this review, we highlight the benefits of using metagenomics as well as the breadth of conclusions that can be made using currently available analytical tools, such as greater resolution of species and strains across phyla and functional content, while highlighting challenges of metagenomic data analysis. Major challenges remain in annotating function, given the dearth of functional databases for environmental bacteria compared to model organisms, and the technical difficulties of metagenome assembly and phasing in heterogeneous environmental samples. In the future, improvements and innovation in technology and methodology will lead to lowered costs. Data integration using multiple technological platforms will lead to a better understanding of how to harness metagenomes. Subsequently, we will be able not only to characterize complex microbiomes but also to manipulate communities to achieve prosperous outcomes for health, agriculture, and environmental sustainability.
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The Influence of Bacteria on Animal Metamorphosis
Vol. 74 (2020), pp. 137–158More LessThe swimming larvae of many marine animals identify a location on the seafloor to settle and undergo metamorphosis based on the presence of specific surface-bound bacteria. While bacteria-stimulated metamorphosis underpins processes such as the fouling of ship hulls, animal development in aquaculture, and the recruitment of new animals to coral reef ecosystems, little is known about the mechanisms governing this microbe-animal interaction. Here we review what is known and what we hope to learn about how bacteria and the factors they produce stimulate animal metamorphosis. With a few emerging model systems, including the tubeworm Hydroides elegans, corals, and the hydrozoan Hydractinia, we have begun to identify bacterial cues that stimulate animal metamorphosis and test hypotheses addressing their mechanisms of action. By understanding the mechanisms by which bacteria promote animal metamorphosis, we begin to illustrate how, and explore why, the developmental decision of metamorphosis relies on cues from environmental bacteria.
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Cyclic di-AMP Signaling in Bacteria
Vol. 74 (2020), pp. 159–179More LessThe second messenger molecule cyclic di-AMP (c-di-AMP) is formed by many bacteria and archaea. In many species that produce c-di-AMP, this second messenger is essential for viability on rich medium. Recent research has demonstrated that c-di-AMP binds to a large number of proteins and riboswitches, which are often involved in potassium and osmotic homeostasis. c-di-AMP becomes dispensable if the bacteria are cultivated on minimal media with low concentrations of osmotically active compounds. Thus, the essentiality of c-di-AMP does not result from an interaction with a single essential target but rather from the multilevel control of complex homeostatic processes. This review summarizes current knowledge on the homeostasis of c-di-AMP and its function(s) in the control of cellular processes.
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Assembly and Dynamics of the Bacterial Flagellum
Vol. 74 (2020), pp. 181–200More LessThe bacterial flagellar motor is the most complex structure in the bacterial cell, driving the ion-driven rotation of the helical flagellum. The ordered expression of the regulon and the assembly of the series of interacting protein rings, spanning the inner and outer membranes to form the ∼45–50-nm protein complex, have made investigation of the structure and mechanism a major challenge since its recognition as a rotating nanomachine about 40 years ago. Painstaking molecular genetics, biochemistry, and electron microscopy revealed a tiny electric motor spinning in the bacterial membrane. Over the last decade, new single-molecule and in vivo biophysical methods have allowed investigation of the stability of this and other large protein complexes, working in their natural environment inside live cells. This has revealed that in the bacterial flagellar motor, protein molecules in both the rotor and stator exchange with freely circulating pools of spares on a timescale of minutes, even while motors are continuously rotating. This constant exchange has allowed the evolution of modified components allowing bacteria to keep swimming as the viscosity or the ion composition of the outside environment changes.
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Bacterial Quorum Sensing During Infection
Vol. 74 (2020), pp. 201–219More LessBacteria are highly interactive and possess an extraordinary repertoire of intercellular communication and social behaviors, including quorum sensing (QS). QS has been studied in detail at the molecular level, so mechanistic details are well understood in many species and are often involved in virulence. The use of different animal host models has demonstrated QS-dependent control of virulence determinants and virulence in several human pathogenic bacteria. QS also controls virulence in several plant pathogenic species. Despite the role QS plays in virulence during animal and plant laboratory-engineered infections, QS mutants are frequently isolated from natural infections, demonstrating that the function of QS during infection and its role in pathogenesis remain poorly understood and are fruitful areas for future research. We discuss the role of QS during infection in various organisms and highlight approaches to better understand QS during human infection. This is an important consideration in an era of growing antimicrobial resistance, when we are looking for new ways to target bacterial infections.
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The Yersinia Type III Secretion System as a Tool for Studying Cytosolic Innate Immune Surveillance
Vol. 74 (2020), pp. 221–245More LessMicrobial pathogens have evolved complex mechanisms to interface with host cells in order to evade host defenses and replicate. However, mammalian innate immune receptors detect the presence of molecules unique to the microbial world or sense the activity of virulence factors, activating antimicrobial and inflammatory pathways. We focus on how studies of the major virulence factor of one group of microbial pathogens, the type III secretion system (T3SS) of human pathogenic Yersinia, have shed light on these important innate immune responses. Yersinia are largely extracellular pathogens, yet they insert T3SS cargo into target host cells that modulate the activity of cytosolic innate immune receptors. This review covers both the host pathways that detect the Yersinia T3SS and the effector proteins used by Yersinia to manipulate innate immune signaling.
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Iron-Only and Vanadium Nitrogenases: Fail-Safe Enzymes or Something More?
Vol. 74 (2020), pp. 247–266More LessThe enzyme molybdenum nitrogenase converts atmospheric nitrogen gas to ammonia and is of critical importance for the cycling of nitrogen in the biosphere and for the sustainability of life. Alternative vanadium and iron-only nitrogenases that are homologous to molybdenum nitrogenases are also found in archaea and bacteria, but they have a different transition metal, either vanadium or iron, at their active sites. So far alternative nitrogenases have only been found in microbes that also have molybdenum nitrogenase. They are less widespread than molybdenum nitrogenase in bacteria and archaea, and they are less efficient. The presumption has been that alternative nitrogenases are fail-safe enzymes that are used in situations where molybdenum is limiting. Recent work indicates that vanadium nitrogenase may play a role in the global biological nitrogen cycle and iron-only nitrogenase may contribute products that shape microbial community interactions in nature.
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Chemical Mediators at the Bacterial-Fungal Interface
Vol. 74 (2020), pp. 267–290More LessInteractions among microbes are key drivers of evolutionary progress and constantly shape ecological niches. Microorganisms rely on chemical communication to interact with each other and surrounding organisms. They synthesize natural products as signaling molecules, antibiotics, or modulators of cellular processes that may be applied in agriculture and medicine. Whereas major insight has been gained into the principles of intraspecies interaction, much less is known about the molecular basis of interspecies interplay. In this review, we summarize recent progress in the understanding of chemically mediated bacterial-fungal interrelations. We discuss pairwise interactions among defined species and systems involving additional organisms as well as complex interactions among microbial communities encountered in the soil or defined as microbiota of higher organisms. Finally, we give examples of how the growing understanding of microbial interactions has contributed to drug discovery and hypothesize what may be future directions in studying and engineering microbiota for agricultural or medicinal purposes.
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Toward a Fully Resolved Fungal Tree of Life
Vol. 74 (2020), pp. 291–313More LessIn this review, we discuss the current status and future challenges for fully elucidating the fungal tree of life. In the last 15 years, advances in genomic technologies have revolutionized fungal systematics, ushering the field into the phylogenomic era. This has made the unthinkable possible, namely access to the entire genetic record of all known extant taxa. We first review the current status of the fungal tree and highlight areas where additional effort will be required. We then review the analytical challenges imposed by the volume of data and discuss methods to recover the most accurate species tree given the sea of gene trees. Highly resolved and deeply sampled trees are being leveraged in novel ways to study fungal radiations, species delimitation, and metabolic evolution. Finally, we discuss the critical issue of incorporating the unnamed and uncultured dark matter taxa that represent the vast majority of fungal diversity.
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Structure and Function of the Mycobacterial Type VII Secretion Systems
Vol. 74 (2020), pp. 315–335More LessBacteria have evolved intricate secretion machineries for the successful delivery of large molecules across their cell envelopes. Such specialized secretion systems allow a variety of bacteria to thrive in specific host environments. In mycobacteria, type VII secretion systems (T7SSs) are dedicated protein transport machineries that fulfill diverse and crucial roles, ranging from metabolite uptake to immune evasion and subversion to conjugation. Since the discovery of mycobacterial T7SSs about 15 y ago, genetic, structural, and functional studies have provided insight into the roles and functioning of these secretion machineries. Here, we focus on recent advances in the elucidation of the structure and mechanism of mycobacterial T7SSs in protein secretion. As many of these systems are essential for mycobacterial growth or virulence, they provide opportunities for the development of novel therapies to combat a number of relevant mycobacterial diseases.
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Microbes as Biosensors
Vol. 74 (2020), pp. 337–359More LessThe ability to detect disease early and deliver precision therapy would be transformative for the treatment of human illnesses. To achieve these goals, biosensors that can pinpoint when and where diseases emerge are needed. Rapid advances in synthetic biology are enabling us to exploit the information-processing abilities of living cells to diagnose disease and then treat it in a controlled fashion. For example, living sensors could be designed to precisely sense disease biomarkers, such as by-products of inflammation, and to respond by delivering targeted therapeutics in situ. Here, we provide an overview of ongoing efforts in microbial biosensor design, highlight translational opportunities, and discuss challenges for enabling sense-and-respond precision medicines.
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Shaping an Endospore: Architectural Transformations During Bacillus subtilis Sporulation
Vol. 74 (2020), pp. 361–386More LessEndospore formation in Bacillus subtilis provides an ideal model system for studying development in bacteria. Sporulation studies have contributed a wealth of information about the mechanisms of cell-specific gene expression, chromosome dynamics, protein localization, and membrane remodeling, while helping to dispel the early view that bacteria lack internal organization and interesting cell biological phenomena. In this review, we focus on the architectural transformations that lead to a profound reorganization of the cellular landscape during sporulation, from two cells that lie side by side to the endospore, the unique cell within a cell structure that is a hallmark of sporulation in B. subtilis and other spore-forming Firmicutes. We discuss new insights into the mechanisms that drive morphogenesis, with special emphasis on polar septation, chromosome translocation, and the phagocytosis-like process of engulfment, and also the key experimental advances that have proven valuable in revealing the inner workings of bacterial cells.
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The Bacterial Ro60 Protein and Its Noncoding Y RNA Regulators
Vol. 74 (2020), pp. 387–407More LessRo60 ribonucleoproteins (RNPs), composed of the ring-shaped Ro 60-kDa (Ro60) protein and noncoding RNAs called Y RNAs, are present in all three domains of life. Ro60 was first described as an autoantigen in patients with rheumatic disease, and Ro60 orthologs have been identified in 3% to 5% of bacterial genomes, spanning the majority of phyla. Their functions have been characterized primarily in Deinococcus radiodurans, the first sequenced bacterium with a recognizable ortholog. In D. radiodurans, the Ro60 ortholog enhances the ability of 3′-to-5′ exoribonucleases to degrade structured RNA during several forms of environmental stress. Y RNAs are regulators that inhibit or allow the interactions of Ro60 with other proteins and RNAs. Studies of Ro60 RNPs in other bacteria hint at additional functions, since the most conserved Y RNA contains a domain that is a close tRNA mimic and Ro60 RNPs are often encoded adjacent to components of RNA repair systems.
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Bacterial Volatile Compounds: Functions in Communication, Cooperation, and Competition
Vol. 74 (2020), pp. 409–430More LessBacteria produce a multitude of volatile compounds. While the biological functions of these deceptively simple molecules are unknown in many cases, for compounds that have been characterized, it is clear that they serve impressively diverse purposes. Here, we highlight recent studies that are uncovering the volatile repertoire of bacteria, and the functional relevance and impact of these molecules. We present work showing the ability of volatile compounds to modulate nutrient availability in the environment; alter the growth, development, and motility of bacteria and fungi; influence protist and arthropod behavior; and impact plant and animal health. We further discuss the benefits associated with using volatile compounds for communication and competition, alongside the challenges of studying these molecules and their functional roles. Finally, we address the opportunities these compounds present from commercial, clinical, and agricultural perspectives.
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Molecular Mechanisms of Drug Resistance in Plasmodium falciparum Malaria
Vol. 74 (2020), pp. 431–454More LessUnderstanding and controlling the spread of antimalarial resistance, particularly to artemisinin and its partner drugs, is a top priority. Plasmodium falciparum parasites resistant to chloroquine, amodiaquine, or piperaquine harbor mutations in the P. falciparum chloroquine resistance transporter (PfCRT), a transporter resident on the digestive vacuole membrane that in its variant forms can transport these weak-base 4-aminoquinoline drugs out of this acidic organelle, thus preventing these drugs from binding heme and inhibiting its detoxification. The structure of PfCRT, solved by cryogenic electron microscopy, shows mutations surrounding an electronegative central drug-binding cavity where they presumably interact with drugs and natural substrates to control transport. P. falciparum susceptibility to heme-binding antimalarials is also modulated by overexpression or mutations in the digestive vacuole membrane–bound ABC transporter PfMDR1 (P. falciparum multidrug resistance 1 transporter). Artemisinin resistance is primarily mediated by mutations in P. falciparum Kelch13 protein (K13), a protein involved in multiple intracellular processes including endocytosis of hemoglobin, which is required for parasite growth and artemisinin activation. Combating drug-resistant malaria urgently requires the development of new antimalarial drugs with novel modes of action.
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Prospects and Pitfalls: Next-Generation Tools to Control Mosquito-Transmitted Disease
Vol. 74 (2020), pp. 455–475More LessMosquito-transmitted diseases, including malaria and dengue, are a major threat to human health around the globe, affecting millions each year. A diverse array of next-generation tools has been designed to eliminate mosquito populations or to replace them with mosquitoes that are less capable of transmitting key pathogens. Many of these new approaches have been built on recent advances in CRISPR/Cas9-based genome editing. These initiatives have driven the development of pathogen-resistant lines, new genetics-based sexing methods, and new methods of driving desirable genetic traits into mosquito populations. Many other emerging tools involve microorganisms, including two strategies involving Wolbachia that are achieving great success in the field. At the same time, other mosquito-associated bacteria, fungi, and even viruses represent untapped sources of new mosquitocidal or antipathogen compounds. Although there are still hurdles to be overcome, the prospect that such approaches will reduce the impact of these diseases is highly encouraging.
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Defining and Disrupting Species Boundaries in Saccharomyces
Vol. 74 (2020), pp. 477–495More LessThe genus Saccharomyces is an evolutionary paradox. On the one hand, it is composed of at least eight clearly phylogenetically delineated species; these species are reproductively isolated from each other, and hybrids usually cannot complete their sexual life cycles. On the other hand, Saccharomyces species have a long evolutionary history of hybridization, which has phenotypic consequences for adaptation and domestication. A variety of cellular, ecological, and evolutionary mechanisms are responsible for this partial reproductive isolation among Saccharomyces species. These mechanisms have caused the evolution of diverse Saccharomyces species and hybrids, which occupy a variety of wild and domesticated habitats. In this article, we introduce readers to the mechanisms isolating Saccharomyces species, the circumstances in which reproductive isolation mechanisms are effective and ineffective, and the evolutionary consequences of partial reproductive isolation. We discuss both the evolutionary history of the genus Saccharomyces and the human history of taxonomists and biologists struggling with species concepts in this fascinating genus.
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Polymorphic Toxins and Their Immunity Proteins: Diversity, Evolution, and Mechanisms of Delivery
Vol. 74 (2020), pp. 497–520More LessAll bacteria must compete for growth niches and other limited environmental resources. These existential battles are waged at several levels, but one common strategy entails the transfer of growth-inhibitory protein toxins between competing cells. These antibacterial effectors are invariably encoded with immunity proteins that protect cells from intoxication by neighboring siblings. Several effector classes have been described, each designed to breach the cell envelope of target bacteria. Although effector architectures and export pathways tend to be clade specific, phylogenetically distant species often deploy closely related toxin domains. Thus, diverse competition systems are linked through a common reservoir of toxin-immunity pairs that is shared via horizontal gene transfer. These toxin-immunity protein pairs are extraordinarily diverse in sequence, and this polymorphism underpins an important mechanism of self/nonself discrimination in bacteria. This review focuses on the structures, functions, and delivery mechanisms of polymorphic toxin effectors that mediate bacterial competition.
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Assembly of Bacterial Capsular Polysaccharides and Exopolysaccharides
Vol. 74 (2020), pp. 521–543More LessPolysaccharides are dominant features of most bacterial surfaces and are displayed in different formats. Many bacteria produce abundant long-chain capsular polysaccharides, which can maintain a strong association and form a capsule structure enveloping the cell and/or take the form of exopolysaccharides that are mostly secreted into the immediate environment. These polymers afford the producing bacteria protection from a wide range of physical, chemical, and biological stresses, support biofilms, and play critical roles in interactions between bacteria and their immediate environments. Their biological and physical properties also drive a variety of industrial and biomedical applications. Despite the immense variation in capsular polysaccharide and exopolysaccharide structures, patterns are evident in strategies used for their assembly and export. This review describes recent advances in understanding those strategies, based on a wealth of biochemical investigations of select prototypes, supported by complementary insight from expanding structural biology initiatives. This provides a framework to identify and distinguish new systems emanating from genomic studies.
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Clostridioides difficile Spore Formation and Germination: New Insights and Opportunities for Intervention
Vol. 74 (2020), pp. 545–566More LessSpore formation and germination are essential for the bacterial pathogen Clostridioides difficile to transmit infection. Despite the importance of these developmental processes to the infection cycle of C. difficile, the molecular mechanisms underlying how this obligate anaerobe forms infectious spores and how these spores germinate to initiate infection were largely unknown until recently. Work in the last decade has revealed that C. difficile uses a distinct mechanism for sensing and transducing germinant signals relative to previously characterized spore formers. The C. difficile spore assembly pathway also exhibits notable differences relative to Bacillus spp., where spore formation has been more extensively studied. For both these processes, factors that are conserved only in C. difficile or the related Peptostreptococcaceae family are employed, and even highly conserved spore proteins can have differential functions or requirements in C. difficile compared to other spore formers. This review summarizes our current understanding of the mechanisms controlling C. difficile spore formation and germination and describes strategies for inhibiting these processes to prevent C. difficile infection and disease recurrence.
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Toxoplasma Mechanisms for Delivery of Proteins and Uptake of Nutrients Across the Host-Pathogen Interface
Vol. 74 (2020), pp. 567–586More LessMany intracellular pathogens, including the protozoan parasite Toxoplasma gondii, live inside a vacuole that resides in the host cytosol. Vacuolar residence provides these pathogens with a defined niche for replication and protection from detection by host cytosolic pattern recognition receptors. However, the limiting membrane of the vacuole, which constitutes the host-pathogen interface, is also a barrier for pathogen effectors to reach the host cytosol and for the acquisition of host-derived nutrients. This review provides an update on the specialized secretion and trafficking systems used by Toxoplasma to overcome the barrier of the parasitophorous vacuole membrane and thereby allow the delivery of proteins into the host cell and the acquisition of host-derived nutrients.
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A Bacterial Tower of Babel: Quorum-Sensing Signaling Diversity and Its Evolution
Vol. 74 (2020), pp. 587–606More LessQuorum sensing is a process in which bacteria secrete and sense a diffusible molecule, thereby enabling bacterial groups to coordinate their behavior in a density-dependent manner. Quorum sensing has evolved multiple times independently, utilizing different molecular pathways and signaling molecules. A common theme among many quorum-sensing families is their wide range of signaling diversity—different variants within a family code for different signal molecules with a cognate receptor specific to each variant. This pattern of vast allelic polymorphism raises several questions—How do different signaling variants interact with one another? How is this diversity maintained? And how did it come to exist in the first place? Here we argue that social interactions between signaling variants can explain the emergence and persistence of signaling diversity throughout evolution. Finally, we extend the discussion to include cases where multiple diverse systems work in concert in a single bacterium.
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From Input to Output: The Lap/c-di-GMP Biofilm Regulatory Circuit
Vol. 74 (2020), pp. 607–631More LessBiofilms are the dominant bacterial lifestyle. The regulation of the formation and dispersal of bacterial biofilms has been the subject of study in many organisms. Over the last two decades, the mechanisms of Pseudomonas fluorescens biofilm formation and regulation have emerged as among the best understood of any bacterial biofilm system. Biofilm formation by P. fluorescens occurs through the localization of an adhesin, LapA, to the outer membrane via a variant of the classical type I secretion system. The decision between biofilm formation and dispersal is mediated by LapD, a c-di-GMP receptor, and LapG, a periplasmic protease, which together control whether LapA is retained or released from the cell surface. LapA localization is also controlled by a complex network of c-di-GMP-metabolizing enzymes. This review describes the current understanding of LapA-mediated biofilm formation by P. fluorescens and discusses several emerging models for the regulation and function of this adhesin.
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Membrane Dynamics in Phototrophic Bacteria
Vol. 74 (2020), pp. 633–654More LessPhotosynthetic membranes are typically densely packed with proteins, and this is crucial for their function in efficient trapping of light energy. Despite being crowded with protein, the membranes are fluid systems in which proteins and smaller molecules can diffuse. Fluidity is also crucial for photosynthetic function, as it is essential for biogenesis, electron transport, and protein redistribution for functional regulation. All photosynthetic membranes seem to maintain a delicate balance between crowding, order, and fluidity. How does this work in phototrophic bacteria? In this review, we focus on two types of intensively studied bacterial photosynthetic membranes: the chromatophore membranes of purple bacteria and the thylakoid membranes of cyanobacteria. Both systems are distinct from the plasma membrane, and both have a distinctive protein composition that reflects their specialized roles. Chromatophores are formed from plasma membrane invaginations, while thylakoid membranes appear to be an independent intracellular membrane system. We discuss the techniques that can be applied to study the organization and dynamics of these membrane systems, including electron microscopy techniques, atomic force microscopy, and many variants of fluorescence microscopy. We go on to discuss the insights that havebeen acquired from these techniques, and the role of membrane dynamics in the physiology of photosynthetic membranes. Membrane dynamics on multiple timescales are crucial for membrane function, from electron transport on timescales of microseconds to milliseconds to regulation and biogenesis on timescales of minutes to hours. We emphasize the open questions that remain in the field.
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Epigenetic Regulation of Virulence and Immunoevasion by Phase-Variable Restriction-Modification Systems in Bacterial Pathogens
Vol. 74 (2020), pp. 655–671More LessHuman-adapted bacterial pathogens use a mechanism called phase variation to randomly switch the expression of individual genes to generate a phenotypically diverse population to adapt to challenges within and between human hosts. There are increasing reports of restriction-modification systems that exhibit phase-variable expression. The outcome of phase variation of these systems is global changes in DNA methylation. Analysis of phase-variable Type I and Type III restriction-modification systems in multiple human-adapted bacterial pathogens has demonstrated that global changes in methylation regulate the expression of multiple genes. These systems are called phasevarions (phase-variable regulons). Phasevarion switching alters virulence phenotypes and facilitates evasion of host immune responses. This review describes the characteristics of phasevarions and implications for pathogenesis and immune evasion. We present and discuss examples of phasevarion systems in the major human pathogens Haemophilus influenzae, Neisseria meningitidis, Neisseria gonorrhoeae, Helicobacter pylori, Moraxella catarrhalis, and Streptococcus pneumoniae.
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Amyloid Signaling in Filamentous Fungi and Bacteria
Vol. 74 (2020), pp. 673–691More LessAmyloids are implicated in many protein misfolding diseases. Amyloid folds, however, also display a range of functional roles particularly in the microbial world. The templating ability of these folds endows them with specific properties allowing their self-propagation and protein-to-protein transmission in vivo. This property, the prion principle, is exploited by specific signaling pathways that use transmission of the amyloid fold as a way to convey information from a receptor to an effector protein. I describe here amyloid signaling pathways involving fungal nucleotide binding and oligomerization domain (NOD)-like receptors that were found to control nonself recognition and programmed cell death processes. Studies on these fungal amyloid signaling motifs stem from the characterization of the fungal [Het-s] prion protein and have led to the identification in fungi but also in multicellular bacteria of several distinct families of signaling motifs, one of which is related to RHIM [receptor-interacting protein (RIP) homotypic interaction motif], an amyloid motif regulating mammalian necroptosis.
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Conflict, Competition, and Cooperation Regulate Social Interactions in Filamentous Fungi
Vol. 74 (2020), pp. 693–712More LessSocial cooperation impacts the development and survival of species. In higher taxa, kin recognition occurs via visual, chemical, or tactile cues that dictate cooperative versus competitive interactions. In microbes, the outcome of cooperative versus competitive interactions is conferred by identity at allorecognition loci, so-called kind recognition. In syncytial filamentous fungi, the acquisition of multicellularity is associated with somatic cell fusion within and between colonies. However, such intraspecific cooperation entails risks, as fusion can transmit deleterious genotypes or infectious components that reduce fitness, or give rise to cheaters that can exploit communal goods without contributing to their production. Allorecognition mechanisms in syncytial fungi regulate somatic cell fusion by operating precontact during chemotropic interactions, during cell adherence, and postfusion by triggering programmed cell death reactions. Alleles at fungal allorecognition loci are highly polymorphic, fall into distinct haplogroups, and show evolutionary signatures of balancing selection, similar to allorecognition loci across the tree of life.
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Structural Basis of Hydrogenotrophic Methanogenesis
Vol. 74 (2020), pp. 713–733More LessMost methanogenic archaea use the rudimentary hydrogenotrophic pathway—from CO2 and H2 to methane—as the terminal step of microbial biomass degradation in anoxic habitats. The barely exergonic process that just conserves sufficient energy for a modest lifestyle involves chemically challenging reactions catalyzed by complex enzyme machineries with unique metal-containing cofactors. The basic strategy of the methanogenic energy metabolism is to covalently bind C1 species to the C1 carriers methanofuran, tetrahydromethanopterin, and coenzyme M at different oxidation states. The four reduction reactions from CO2 to methane involve one molybdopterin-based two-electron reduction, two coenzyme F420–based hydride transfers, and one coenzyme F430–based radical process. For energy conservation, one ion-gradient-forming methyl transfer reaction is sufficient, albeit supported by a sophisticated energy-coupling process termed flavin-based electron bifurcation for driving the endergonic CO2 reduction and fixation. Here, we review the knowledge about the structure-based catalytic mechanism of each enzyme of hydrogenotrophic methanogenesis.
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Surface Sensing and Adaptation in Bacteria
Vol. 74 (2020), pp. 735–760More LessBacteria thrive both in liquids and attached to surfaces. The concentration of bacteria on surfaces is generally much higher than in the surrounding environment, offering bacteria ample opportunity for mutualistic, symbiotic, and pathogenic interactions. To efficiently populate surfaces, they have evolved mechanisms to sense mechanical or chemical cues upon contact with solid substrata. This is of particular importance for pathogens that interact with host tissue surfaces. In this review we discuss how bacteria are able to sense surfaces and how they use this information to adapt their physiology and behavior to this new environment. We first survey mechanosensing and chemosensing mechanisms and outline how specific macromolecular structures can inform bacteria about surfaces. We then discuss how mechanical cues are converted to biochemical signals to activate specific cellular processes in a defined chronological order and describe the role of two key second messengers, c-di-GMP and cAMP, in this process.
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Genomic Approaches to Drug Resistance in Malaria
Vol. 74 (2020), pp. 761–786More LessAlthough the last two decades have seen a substantial decline in malaria incidence and mortality due to the use of insecticide-treated bed nets and artemisinin combination therapy, the threat of drug resistance is a constant obstacle to sustainable malaria control. Given that patients can die quickly from this disease, public health officials and doctors need to understand whether drug resistance exists in the parasite population, as well as how prevalent it is so they can make informed decisions about treatment. As testing for drug efficacy before providing treatment to malaria patients is impractical, researchers need molecular markers of resistance that can be more readily tracked in parasite populations. To this end, much work has been done to unravel the genetic underpinnings of drug resistance in Plasmodium falciparum. The aim of this review is to provide a broad overview of common genomic approaches that have been used to discover the alleles that drive drug response phenotypes in the most lethal human malaria parasite.
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How Food Affects Colonization Resistance Against Enteropathogenic Bacteria
Vol. 74 (2020), pp. 787–813More LessFood has a major impact on all aspects of health. Recent data suggest that food composition can also affect susceptibility to infections by enteropathogenic bacteria. Here, we discuss how food may alter the microbiota as well as mucosal defenses and how this can affect infection. Salmonella Typhimurium diarrhea serves as a paradigm, and complementary evidence comes from other pathogens. We discuss the effects of food composition on colonization resistance, host defenses, and the infection process as well as the merits and limitations of mouse models and experimental foods, which are available to decipher the underlying mechanisms.
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The Ingenuity of Bacterial Genomes
Vol. 74 (2020), pp. 815–834More LessThe genomes of bacteria contain fewer genes and substantially less noncoding DNA than those of eukaryotes, and as a result, they have much less raw material to invent new traits. Yet, bacteria are vastly more taxonomically diverse, numerically abundant, and globally successful in colonizing new habitats compared to eukaryotes. Although bacterial genomes are generally considered to be optimized for efficient growth and rapid adaptation, nonadaptive processes have played a major role in shaping the size, contents, and compact organization of bacterial genomes and have allowed the establishment of deleterious traits that serve as the raw materials for genetic innovation.
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Implications of the Evolutionary Trajectory of Centromeres in the Fungal Kingdom
Vol. 74 (2020), pp. 835–853More LessChromosome segregation during the cell cycle is an evolutionarily conserved, fundamental biological process. Dynamic interaction between spindle microtubules and the kinetochore complex that assembles on centromere DNA is required for faithful chromosome segregation. The first artificial minichromosome was constructed by cloning the centromere DNA of the budding yeast Saccharomyces cerevisiae. Since then, centromeres have been identified in >60 fungal species. The DNA sequence and organization of the sequence elements are highly diverse across these fungal centromeres. In this article, we provide a comprehensive view of the evolution of fungal centromeres. Studies of this process facilitated the identification of factors influencing centromere specification, maintenance, and propagation through many generations. Additionally, we discuss the unique features and plasticity of centromeric chromatin and the involvement of centromeres in karyotype evolution. Finally, we discuss the implications of recurrent loss of RNA interference (RNAi) and/or heterochromatin components on the trajectory of the evolution of fungal centromeres and propose the centromere structure of the last common ancestor of three major fungal phyla—Ascomycota, Basidiomycota, and Mucoromycota.
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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)