Myxobacteria: Genomics, Cellular and Molecular Biology | Book
Caister Academic Press
Zhaomin Yang and Penelope I. Higgs Biological Sciences, Virginia Tech, Blacksburg, VA 24061-0910, USA; Dept. of Ecophysiology, Max Planck Institute for Terrestrial Microbiology, Marburg, Germany (respectively)
x + 236 (plus colour plates)
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Myxobacteria have fascinated generations of scientists since their discovery over a century ago. These bacteria represent the epitome of complex prokaryotic behaviour. Their predatory swarms move over solid surfaces utilizing two distinct motility machineries: one driven by retractable pili, and the other by a novel gliding machinery. Furthermore, under nutrient limitation, myxobacteria enter a developmental program featuring distinct cell fates and culminating in the formation of multicellular fruiting bodies filled with dormant spores.
In this book, expert myxobiologists describe important recent advances in understanding the behaviour of these bacteria at a molecular and cellular level. The book covers ecology, genomics and cell biology as well as modelling and simulation on topics including motility, development and their associated genetic regulatory networks. Authors provide the most up-to-date overview on myxobacteria and highlight open questions in the active areas of research. The book will serve as an essential reference for everyone working with myxobacteria. Chapters have been written and structured to be accessible to teachers, graduate and advanced undergraduate students new to myxobacteria, as well as experts in other fields including physical and computational sciences.
Whence Comes Social Diversity? Ecological and Evolutionary Analysis of the Myxobacteria
Gregory J. Velicer, Helena Mendes-Soares and Sébastien Wielgoss
Recent discoveries have found the myxobacteria to be much more diverse - both across and within species - than previously known, from global to micrometer spatial scales. Evolutionary analysis of such extant diversity promises to reveal much about how myxobacteria have adapted to natural ecological habitats in the past and continue to evolve in the present, particularly with regard to their intriguing social phenotypes. Experimental populations propagated under defined laboratory conditions undergo very rapid evolution at cooperative traits in a manner that radically changes their social composition. Analysis of such experimentally evolved populations allows detailed characterization of social evolutionary dynamics in real time. Moreover, traditional genetic tools and new genome sequencing technologies together allow deep investigation of the molecular basis of adaptation by experimental populations to known ecological habitats, which in turn can lead to new discoveries regarding the molecular mechanisms governing social behavior.
Genome Evolution and Content in the Myxobacteria
Stuart Huntley, Kristin Wuichet and Lotte Søgaard-Andersen
Nearly 2000 microbial genomes have been completely sequenced since the first bacterial genome sequence was released in 1995. Since then, comparative and functional genomics in combination with advances in sequencing techniques have significantly changed the way (micro)biological research is done. Intra- and inter-genome comparisons are now common practice to understand possible evolutionary trajectories and for identifying genes of interest. Similarly, functional genomics approaches such as transcriptome and proteome analyses, which rely on genome sequences, have been developed in many model organisms including Myxococcus xanthus. Here, we present a summary of the myxobacteria genome sequences available to date (July 2012) as well as an overall comparison of these genomes. Most members of the myxobacteria have large genome with sizes of approximately 10 Mb or even larger. We explore hypotheses for myxobacteria genome evolution, including genome size, genome organization with conserved synteny and genetic content with a special emphasis on genes for signal transduction proteins. Moreover, we discuss the level of shared genetic content of the hallmark characteristic of the myxobacteria, i.e. fruiting body formation. Finally, we look at what is on the near horizon for the future of myxobacteria genomics.
Myxococcus xanthus Vegetative and Developmental Cell Heterogeneity
Penelope I. Higgs, Patricia L. Hartzell, Carina Holkenbrink and Egbert Hoiczyk
The myxobacteria have long been considered model organisms for complex multicellular behavior and Gram-negative differentiation. To effectively compete for nutrients in soil or aquatic environments, these bacteria have evolved multicellular hunting strategies and phenotypic heterogeneity within the population, such as phase variation and cell clustering, which likely contribute to the success of these organisms. To survive periods of nutrient limitation, most myxobacteria enter a complex developmental program culminating in the formation of multicellular fruiting bodies filled with environmentally resistant spores. The developmental program of Myxococcus xanthus, the model myxobacterium, involves segregation of the starving population into at least three distinct fates: aggregation into multicellular mounds followed by differentiation into spores, differentiation into a persister-like state termed peripheral rods, and developmentally-induced cell lysis. This chapter describes what is currently known about the role of phenotypic heterogeneity and developmental cell fate differentiation in the M. xanthus lifecycle. We describe the physiological characteristics as well as regulatory mechanisms involved in generating phenotypic heterogeneity and cell fate differentiation during both vegetative and developmental stages of these remarkably adaptable bacteria.
Cell Cycle Regulation in Myxoccocus xanthus During Vegetative Growth and Development: Regulatory Links between DNA Replication and Cell Division
Anke Treuner-Lange, Lotte Søgaard-Andersen and Mitchell Singer
In response to starvation M. xanthus cells initiate a developmental program that culminates in the formation of multicellular fruiting bodies inside which the rod-shaped cells differentiate into spherical myxospores. Whereas the rod-shaped vegetative cells contain 1 to 2 chromosomes, depending on the stage of the cell cycle, mature myxospores contain two chromosomes and peripheral rods, a differentiated cell type localized outside fruiting bodies, contain one chromosome. Moreover, during development, DNA replication occurs in the pre-aggregation stage and a new round of replication and termination of replication in the pre-aggregation stage are essential for fruiting body formation and myxospore differentiation. These observations suggest that the cell cycle is strictly regulated during fruiting body formation. Here, we describe the current understanding of the M. xanthus cell cycle with special emphasis on replication and chromosome organization as well as cell division. It is currently unknown how myxospores with two chromosomes and peripheral rods with one chromosome arise during development. Importantly, with the recent introduction of cell biology methods, the tools are now available to address how DNA replication, chromosome organization, cell division and cell fate determination are coupled during M. xanthus fruiting body formation.
Social Interactions Mediated by Outer Membrane Exchange
Myxobacteria are unusual because they exhibit complex social behaviors that involve cooperative cell-cell interactions to coordinate multicellular processes. The complexity of their social behaviors is mirrored by their genetic complexity; myxobacteria contain some of the largest known bacterial genomes. Other chapters in this book review cooperative behaviors of myxobacteria, include gliding motility and development. In this chapter, I will review our current understanding of a newly discovered social interaction whereby myxobacteria exchange their outer membrane (OM) proteins and lipids. The mechanism of transfer requires physical contact between aligned cells on hard surfaces. Transfer is mediated by OM fusion in which membrane contents laterally diffuse and are exchanged bidirectionally between cells. TraA and TraB are recently identified proteins that are required in donor and recipient cells for transfer to occur. OM exchange has phenotypic consequences that can alter cellular behaviors, including motility and development. Here I argue that OM exchange represents a new microbial platform whereby cells interact and communicate to coordinate multicellular activities.
Developmental Gene Regulation
Ramya Rajagopalan, Zaara Sarwar, Anthony G. Garza and Lee Kroos
Starvation induces Myxococcus xanthus cells to glide into aggregates and form multicellular fruiting bodies in which some cells differentiate from rods to spores. The gene regulatory network controlling this developmental process involves three interconnected modules. The first module is a cascade of eukaryotic-like enhancer binding proteins that activate early genes in response to starvation, although products of some of those genes function later in development. The second module depends on the first, linking it indirectly to starvation, but other pathways directly link the second module to starvation, and govern accumulation of MrpC and its truncated form MrpC2, which directly activate transcription of fruA, the gene encoding the key component of the third module. Activity of FruA is governed by short-range C-signaling between cells, which is believed to increase as cells become aligned in aggregates. FruA and MrpC2 bind cooperatively to promoter regions of several late genes, subjecting them to control by the Mrp and FruA modules. Among these late genes is the dev operon, whose products somehow control expression of genes required for spore formation. Feedback loops within modules and between modules reinforce developmental progression. Interestingly, some of the key regulators appear to have been acquired by lateral gene transfer and are not conserved in distantly-related mxyobacteria that form fruiting bodies.
Abundance and Complexity of Signalling Mechanisms in Myxobacteria
José Muñoz-Dorado, Penelope I. Higgs and Montserrat Elías-Arnanz
The complex lifestyle of myxobacteria depends on a vast array of signaling mechanisms. Cells must not only monitor their environment and induce adaptive responses, but they must also communicate in order to coordinate and successfully complete their multicellular life cycle. Recent genomics data have revealed that the signaling potential of myxobacteria is far greater than predicted, since the number of two-component systems, extracytoplasmic function σ factors, and eukaryotic-like protein kinases and phosphatases encoded in their genomes is very high. Characterization of some of these signal-transduction systems has revealed unusual complexity, featuring multiple components and interconnections which suggests that many myxobacterial signaling mechanisms function as intricate networks, rather than as linear pathways. Undoubtedly, a comprehensive elucidation of these signaling mechanisms will be one of the main future goals in order to understand the life cycle of these bacteria.
Computational Biology: From Observation to Statistical Image Analysis to Modelling and Back to Biology
Cameron W. Harvey, Oleg A. Igoshin, Roy D. Welch, Mark Alber and Lawrence J. Shimkets
Emergence refers to the manner in which complex behaviors self-organize from a multitude of relatively simple events. Myxococcus xanthus is one of the premier organisms for studying emergence as genetic and biochemical approaches can be wielded in equal measure with computational approaches. Computational modeling has been successfully used to study a range of topics related to myxobacterial self-organization. By reviewing a number of modeling studies from the myxobacteria literature, this chapter aims to demonstrate the cycle of computational modeling. The path from experimental observations to modeling and predictions is traced for three emergent behaviors: swarming, formation of ripples, and fruiting body development. A number of important questions regarding emergent behavior can potentially benefit from computational modeling including the motility mechanisms, signaling during development and biochemical pathways driving direction reversals. Computational models can provide critical insight and predictive power, and are becoming important tools in the study of bacterial behavior.
The Mechanism of A-Motility
Jennifer Luciano, Beiyan Nan, David R. Zusman and Tâm Mignot
Myxococcus xanthus is able to move over solid surfaces as large coordinated groups (Social motility) or as single isolated cells (Adventurous motility). While S-motility was shown to rely on polar Type-IV pili in the early 2000s, the mechanism of A-motility has long remained mysterious because it occurs in absence of detectable extracellular organelles. In the past, many models have been proposed to explain A-motility. In recent years, with the advent of high-resolution fluorescence microscopy and phylogenomics, it has been possible to identify the A-motility machinery and propose a motility mechanism. In this chapter, we discuss the state-of-the-art in A-motility research and future directions to decipher this long mystery of modern bacteriology.
Type IV Pili and Exopolysaccharide-dependent Motility in Myxococcus xanthus
Zhaomin Yang, Chengyun Li, Carmen Friedrich and Lotte Søgaard-Andersen
Social (S) motility of Myxococcus xanthus was discovered in the late 1970's. In the last few decades, especially since the mid-1990's, great strides have been made in our understanding of the molecular mechanisms underlying this form of motility. It is now well established that M. xanthus S-motility as well as twitching motility in other bacteria rely on the retraction of the type IV pilus (T4P) to bring about cell translocation. In fact, T4P retraction generates the strongest force ever measured for a biological motor. In this chapter, we review the landmark studies leading to the conclusion that T4P retraction powers these forms of bacterial surface locomotion. The structure of the T4P system in comparison with the type II secretion system is discussed as they are evolutionally related. We additionally describe the requirement of of M. xanthus S-motility for exopolysaccharides. We will conclude by highlighting some of the unanswered questions, with special attention to M. xanthus T4P-dependent motility.
Sensory Regulation of Myxococcus xanthus Motility
Emilia M.F. Mauriello, Beiyan Nan and David R. Zusman
Myxococcus xanthus cells grow vegetatively on organic nutrients and by killing and digesting prey microorganisms. On hard surfaces, efficient food gathering requires cells to be able to move without flagella. When nutrients become scarce, cells respond by adjusting their movement in order to aggregate into fruiting bodies containing resistant spores. These activities require M. xanthus cells to perceive and respond to many signals. To this purpose, M. xanthus evolved multiple sensory transduction pathways, including one-component, two-component and complex chemosensory systems. In this chapter, we focus on the M. xanthus chemosensory systems and how they control individual cell and group movements, since environmental sensing is essential for survival, permitting bacteria to react to continuously changing external conditions.
The Biophysics of Myxococcus xanthus Motility
Fabian Czerwinski and Joshua Shaevitz
Biophysical approaches have become increasingly important to the study of Myxococcus xanthus from the generation of force during motility to the statistical mechanics of multi-cell pattern formation. In this chapter, we introduce a number of relevant biophysical concepts and techniques, focusing on their relevance for bacterial cells. Biophysical measurements have played a major role in the study of the Escherichia coli flagellar motor. Through analogy with this well-studied system, we hope to highlight current work in the field of M. xanthus biophysics and inspire the next generation of scientists interested in understanding the amazing behaviors of this fascinating organism.
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(EAN: 9781908230348 Subjects: [microbiology] [bacteriology] [molecular microbiology] [environmental microbiology] )