Annual Review of Microbiology - Volume 61, 2007

Plants support a diverse array of bacteria, including parasites, mutualists, and commensals on and around their roots, in the vasculature, and on aerial tissues. These microbes have a profound influence on plant health and productivity. Bacteria physically interact with surfaces to form complex multicellular and often multispecies assemblies, including biofilms and smaller aggregates. There is growing appreciation that the intensity, duration, and outcome of plant-microbe interactions are significantly influenced by the conformation of adherent microbial populations. Biofilms on different tissues have unique properties, reflecting the prevailing conditions at those sites. Attachment is required for biofilm formation, and bacteria interact with plant tissues through adhesins including polysaccharides and surface proteins, with initial contact often mediated by active motility. Recognition between lectins and their cognate carbohydrates is a common means of specificity. Biofilm development and the resulting intimate interactions with plants often require cell-cell communication between colonizing bacteria.

Filamentous fungi are multicellular eukaryotic organisms known for nutrient recycling as well as for antibiotic and food production. This group of organisms also contains the most devastating plant pathogens and several important human pathogens. Since the first report of heterotrimeric G proteins in filamentous fungi in 1993, it has been demonstrated that G proteins are essential for growth, asexual and sexual development, and virulence in both animal and plant pathogenic filamentous species. Numerous G protein subunit and G protein–coupled receptor genes have been identified, many from whole-genome sequences. Several regulatory pathways have now been delineated, including those for nutrient sensing, pheromone response and mating, and pathogenesis. This review provides a comparative analysis of G protein pathways in several filamentous species, with discussion of both unifying themes and important unique signaling paradigms.

Data from protist genomes suggest that eukaryotes show enormous variability in their gene complements, especially of genes coding regulatory proteins. Overall counts of eukaryotic signaling proteins show weak nonlinear scaling with proteome size, but individual superfamilies of signaling domains might show vast expansions in certain protists. Alteration of domain architectural complexity of signaling proteins and repeated lineage-specific reshaping of architectures might have played a major role in the emergence of new signaling interactions in different eukaryotes. Lateral transfer of various signaling domains from bacteria or from hosts, in parasites such as apicomplexans, appears to also have played a major role in the origin of new functional networks. Lineage-specific expansion of regulatory proteins, particularly of transcription factors, has played a critical role in the adaptive radiation of different protist lineages. Comparative genomics allows objective reconstruction of the ancestral conditions and subsequent diversification of several regulatory systems involved in phosphorylation, cyclic nucleotide signaling, Ubiquitin conjugation, chromatin remodeling, and posttranscriptional gene silencing.

The current need for antibiotics with novel target molecules has coincided with advances in technical approaches for the structural and functional analysis of the lantibiotics, which are ribosomally synthesized peptides produced by gram-positive bacteria. These peptides have antibiotic or morphogenetic activity and are structurally defined by the presence of unusual amino acids introduced by posttranslational modification. Lantibiotics are complex polycyclic molecules formed by the dehydration of select Ser and Thr residues and the intramolecular addition of Cys thiols to the resulting unsaturated amino acids to form lanthionine and methyllanthionine bridges, respectively. Importantly, the structural and functional diversity of the lantibiotics is much broader than previously imagined. Here we discuss this growing collection of molecules and introduce some recently discovered peptides, review advances in enzymology and protein engineering, and discuss the regulatory networks that govern the synthesis of the lantibiotics by the producing organisms.

The availability of whole-genome sequences for ammonia-oxidizing bacteria (AOB) has led to dramatic increases in our understanding of these environmentally important microorganisms. Their genomes are smaller than many other members of the proteobacteria and may indicate genome reductions consistent with their limited lifestyle. The genomes have a surprising level of gene repetition including genes for ammonia catabolism, iron acquisition, and insertion sequences. The gene profiles reveal limited genes for catabolism and transport of complex organic compounds, but complete pathways for some other compounds. This led to the observation of chemolithoheterotrophic growth of Nitrosomonas europaea. Genes for sucrose synthesis/degradation were identified. The core metabolic module of aerobic ammonia oxidation, the extraction of electrons from hydroxylamine to generate proton-motive force and reductant, has evolutionary roots in the denitrification inventory of anaerobic sulfur-dependent bacteria. The extension by ammonia monooxygenase provides a mechanism to feed this module using ammonia and O2.

Candida albicans is termed a dimorphic fungus because it proliferates in either a yeast form or a hyphal form. The switch between these forms is the result of a complex interplay of external and internal factors and is coordinated in part by polarity-regulating proteins that are conserved among eukaryotic cells. However, yeast and hyphal cells are not the only morphological states of C. albicans. The opaque form required for mating, the pseudohyphal cell, and the chlamydospore represent distinct cell types that form in response to specific genetic or environmental conditions. In addition, hyperextended buds can form as a result of various cell cycle–related stresses. Recent studies are beginning to shed light on some of the molecular controls regulating the various morphogenetic forms of this fascinating human pathogen.

Endospores formed by Bacillus, Clostridia, and related genera are encased in a protein shell called the coat. In many species, including B. subtilis, the coat is the outermost spore structure, and in other species, such as the pathogenic organisms B. anthracis and B. cereus, the spore is encased in an additional layer called the exosporium. Both the coat and the exosporium have roles in protection of the spore and in its environmental interactions. Assembly of both structures is a function of the mother cell, one of two cellular compartments of the developing sporangium. Studies in B. subtilis have revealed that the timing of coat protein production, the guiding role of a small group of morphogenetic proteins, and several types of posttranslational modifications are essential for the fidelity of the assembly process. Assembly of the exosporium requires a set of novel proteins as well as homologues of proteins found in the outermost layers of the coat and of some of the coat morphogenetic factors, suggesting that the exosporium is a more specialized structure of a multifunctional coat. These and other insights into the molecular details of spore surface morphogenesis provide avenues for exploitation of the spore surface layers in applications for biotechnology and medicine.

All cytoskeletal elements known from eukaryotic cells are also present in bacteria, where they perform vital tasks in many aspects of the physiology of the cell. Bacterial tubulin (FtsZ), actin (MreB), and intermediate filament (IF) proteins are key elements in cell division, chromosome and plasmid segregation, and maintenance of proper cell shape, as well as in maintenance of cell polarity and assembly of intracellular organelle-like structures. Although similar tasks are performed by eukaryotic cytoskeletal elements, the individual functions of FtsZ, MreBs, and IFs are different from those performed by their eukaryotic orthologs, revealing a striking evolutional plasticity of cytoskeletal proteins. However, similar to the functions of their eukaryotic counterparts, the functions conferred by bacterial cytoskeletal proteins are driven by their ability to form dynamic filamentous structures. Therefore, the cytoskeleton was a prokaryotic invention, and additional bacteria-specific cytoskeletal elements, such as fibril and MinD-type ATPases, that confer various functions in cell morphology and during the cell cycle have been observed in prokaryotes. The investigation of these elements will give fundamental information for all types of cells and can reveal the molecular mode of action of cytoskeletal, filament-forming proteins.