Annual Review of Microbiology - Volume 67, 2013

Asymmetries in cell growth and division occur in eukaryotes and prokaryotes alike. Even seemingly simple and morphologically symmetric cell division processes belie inherent underlying asymmetries in the composition of the resulting daughter cells. We consider the types of asymmetry that arise in various bacterial cell growth and division processes, which include both conditionally activated mechanisms and constitutive, hardwired aspects of bacterial life histories. Although asymmetry disposes some cells to the deleterious effects of aging, it may also benefit populations by efficiently purging accumulated damage and rejuvenating newborn cells. Asymmetries may also generate phenotypic variation required for successful exploitation of variable environments, even when extrinsic changes outpace the capacity of cells to sense and respond to challenges. We propose specific experimental approaches to further develop our understanding of the prevalence and the ultimate importance of asymmetric bacterial growth.

Archaea constitute a considerable fraction of the microbial biomass on Earth. Like Bacteria they have evolved a variety of energy metabolisms using organic and/or inorganic electron donors and acceptors, and many of them are able to fix carbon from inorganic sources. Archaea thus play crucial roles in the Earth's global geochemical cycles and influence greenhouse gas emissions. Methanogenesis and anaerobic methane oxidation are important steps in the carbon cycle; both are performed exclusively by anaerobic archaea. Oxidation of ammonia to nitrite is performed by Thaumarchaeota. They represent the only archaeal group that resides in large numbers in the global aerobic terrestrial and marine environments on Earth. Sulfur-dependent archaea are confined mostly to hot environments, but metal leaching by acidophiles and reduction of sulfate by anaerobic, nonthermophilic methane oxidizers have a potential impact on the environment. The metabolisms of a large number of archaea, in particular those dominating the subsurface, remain to be explored.

The complex and intimate relationship between humans and their gut microbial communities is becoming less obscure, due in part to large-scale gut microbial genome-sequencing projects and culture-independent surveys of the composition and gene content of these communities. These studies build upon, and are complemented by, experimental efforts to define underlying mechanisms of host-microbe interactions in simplified model systems. This review highlights the intersection of these approaches. Experimental studies now leverage the advances in high-throughput DNA sequencing that have driven the explosion of microbial genome and community profiling projects, and the loss-of-function and gain-of-function strategies long employed in model organisms are now being extended to microbial genes, species, and communities from the human gut. These developments promise to deepen our understanding of human gut host–microbiota relationships and are readily applicable to other host-associated and free-living microbial communities.

Plant biomass degradation by fungi requires a diverse set of secreted enzymes and significantly contributes to the global carbon cycle. Recent advances in genomic and systems-level studies have begun to reveal how filamentous ascomycete species exploit carbon sources in different habitats. These studies have laid the groundwork for unraveling new enzymatic strategies for deconstructing the plant cell wall, including the discovery of polysaccharide monooxygenases that enhance the activity of cellulases. The identification of genes encoding proteins lacking functional annotation, but that are coregulated with cellulolytic genes, suggests functions associated with plant biomass degradation remain to be elucidated. Recent research shows that signaling cascades mediating cellulolytic responses often act in a light-dependent manner and show crosstalk with other metabolic pathways. In this review, we cover plant biomass degradation, from sensing, to transmission and modulation of signals, to activation of transcription factors and gene induction, to enzyme complement and function.

Most epithelia in animals are colonized by microbial communities. These resident microbes influence fitness and thus ecologically important traits of their hosts, ultimately forming a metaorganism consisting of a multicellular host and a community of associated microorganisms. Recent discoveries in the cnidarian Hydra show that components of the innate immune system as well as transcriptional regulators of stem cells are involved in maintaining homeostasis between animals and their resident microbiota. Here I argue that components of the innate immune system with its host-specific antimicrobial peptides and a rich repertoire of pattern recognition receptors evolved in early-branching metazoans because of the need to control the resident beneficial microbes, not because of invasive pathogens. I also propose a mutual intertwinement between the stem cell regulatory machinery of the host and the resident microbiota composition, such that disturbances in one trigger a restructuring and resetting of the other.

Are viruses more biologically successful than cellular life? Here we examine many ways of gauging biological success, including numerical abundance, environmental tolerance, type biodiversity, reproductive potential, and widespread impact on other organisms. We especially focus on successful ability to evolutionarily adapt in the face of environmental change. Viruses are often challenged by dynamic environments, such as host immune function and evolved resistance as well as abiotic fluctuations in temperature, moisture, and other stressors that reduce virion stability. Despite these challenges, our experimental evolution studies show that viruses can often readily adapt, and novel virus emergence in humans and other hosts is increasingly problematic. We additionally consider whether viruses are advantaged in evolvability—the capacity to evolve—and in avoidance of extinction. On the basis of these different ways of gauging biological success, we conclude that viruses are the most successful inhabitants of the biosphere.

Prions, or infectious proteins, represent a major frontier in the study of infectious agents. The prions responsible for mammalian transmissible spongiform encephalopathies (TSEs) are due primarily to infectious self-propagation of misfolded prion proteins. TSE prion structures remain ill-defined, other than being highly structured, self-propagating, and often fibrillar protein multimers with the capacity to seed, or template, the conversion of their normal monomeric precursors into a pathogenic form. Purified TSE prions usually take the form of amyloid fibrils, which are self-seeding ultrastructures common to many serious protein misfolding diseases such as Alzheimer's, Parkinson's, Huntington's and Lou Gehrig's (amytrophic lateral sclerosis). Indeed, recent reports have now provided evidence of prion-like propagation of several misfolded proteins from cell to cell, if not from tissue to tissue or individual to individual. These findings raise concerns that various protein misfolding diseases might have spreading, prion-like etiologies that contribute to pathogenesis or prevalence.

This review presents a personal account of research on archaeal viruses and describes many new viral species and families, demonstrating that viruses of Archaea constitute a distinctive part of the virosphere and display morphotypes that are not associated with the other two domains of life, Bacteria and Eukarya. I focus primarily on viruses that infect hyperthermophilic members of the phylum Crenarchaeota. These viruses' distinctiveness extends from their morphotypes to their genome sequences and the structures of the proteins they encode. Moreover, the mechanisms underlying the interactions of these viruses with their hosts also have unique features. Studies of archaeal viruses provide new perspectives concerning the nature, diversity, and evolution of virus-host interactions. Considering these studies, I associate the distinctions between bacterial and archaeal viruses with the fundamental differences in the envelope compositions of their host cells.

Fungal hyphae extend by apical growth. This process involves the polarized traffic of secretory vesicles to the Spitzenkörper (SPK) and their subsequent distribution to specific domains of the plasma membrane, where they fuse to provide all the enzymes and material needed for cell wall expansion. Endocytic recycling and localized translation of specific mRNAs play an important role in hyphal apical growth. The traffic of vesicular carriers from synthesis sites to their destinations is coordinated by the combined action of coats, tethers, Rab GTPases, motors, and SNAREs in a mechanism that is just beginning to be understood. Only recently has it been confirmed that the different-sized vesicles present at the SPK contain distinct cell wall biosynthetic activities and are distributed in a stratified manner.

Symbiosis between Rhizobium bacteria and legumes leads to the formation of the root nodule. The endosymbiotic bacteria reside in polyploid host cells as membrane-surrounded vesicles where they reduce atmospheric nitrogen to support plant growth by supplying ammonia in exchange for carbon sources and energy. The morphology and physiology of endosymbionts, despite their common function, are highly divergent in different hosts. In galegoid plants, the endosymbionts are terminally differentiated, uncultivable polyploid cells, with remarkably elongated and even branched Y-shaped cells. Bacteroid differentiation is controlled by host peptides, many of which have antibacterial activity and require the bacterial function of BacA. Although the precise and combined action of several hundred host peptides and BacA has yet to be discovered, similarities, especially to certain insect-bacterium symbioses involving likewise host peptides for manipulation of endosymbionts, suggest convergent evolution. Rhizobium-legume symbiosis provides a rich source of information for understanding host-controlled endosymbiotic life in eukaryotic cells.

The pathogen Staphylococcus aureus is well adapted to its human host. Neutrophil-mediated killing is a crucial defense system against S. aureus; however, the pathogen has evolved many strategies to resist killing. We first describe the discrete steps of neutrophil activation and migration to the site of infection and the killing of microbes by neutrophils in general. We then highlight the different approaches utilized by S. aureus to resist the different steps of neutrophil attack. Various molecules are discussed in their evolutionary context. Most of the molecules secreted by S. aureus to combat neutrophil attacks at the site of infection show clear human specificity. Many elements of human neutrophil defenses appear redundant, and so the evasion strategies of staphylococci display redundant functions as well. All efforts by S. aureus to resist neutrophil-mediated killing stress the importance of these mechanisms in the pathophysiology of staphylococcal diseases. However, the highly human-specific nature of most host-pathogen interactions hinders the in vivo establishment of their contribution to staphylococcal pathophysiology.