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Current Trends in Myxobacteria Research

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Current Trends in Myxobacteria Research Ann Microbiol (2016) 66:17–33 DOI 10.1007/s13213-015-1104-3 REVIEW ARTICLE Current trends in myxobacteria research Wioletta Wrótniak-Drzewiecka1 & Anna Joanna Brzezińska1 & Hanna Dahm1 & Avinash P. Ingle 2 & Mahendra Rai 2 Received: 5 March 2015 /Accepted: 19 May 2015 /Published online: 12 June 2015 # Springer-Verlag Berlin Heidelberg and the University of Milan 2015 Abstract Myxobacteria are fascinating Gram-negative bacte- Keywords Myxobacteria . Ecology . Cytology . Enzymatic ria whose life cycle includes the formation of multicellular activity . Secondary metabolism . Social interactions fruiting bodies that contain about 100,000 cells differentiated as asexual spores for their long-term survival. They move by gliding on surfaces, an activity that helps them carry out their Introduction primitive kind of multicellular development. Myxobacteria have multiple traits that are clearly social in nature; they move Myxobacteria (slime bacteria) are rod-shaped Gram-negative and feed socially. These processes require specific intercellu- bacteria that move by gliding. They typically travel in swarms, lar signals, thereby exhibiting a sophisticated level of the inter- containing many cells kept together by intercellular molecular organismal communication. Myxobacteria are predators. signals. Bacterial gliding is a process whereby a bacterium can Predation is social not only with respect to searching for prey move under its own power. For many bacteria, the mechanism (motility) but also in the killing of prey. Swarming groups of of gliding is unknown or only partially known, and different cells secrete antibiotics and bacteriolytic compounds that kill bacteria (cyanobacteria, cytophaga-flavobacteria) have dis- and lyse their prey, and food is thereby released. Since the last tinct mechanisms of movement. When nutrients are scarce, three decades, myxobacteria are known as valuable producers cells of myxobacteria aggregate by chemotaxis, produce of secondary metabolites exhibiting various biological activi- fruiting bodies and avoid desiccation by forming resistant ties. Myxobacterial metabolites exhibit many unique structur- myxospores. al features as well as rare or novel modes of action, making Myxobacteria occur in at least two morphological types: them attractive lead structures for drug development. Both (1) slender flexible rods with more or less tapering ends, and genome sequencing and metabolic profiling of myxobacterial (2) cylindrical rods with rounded ends. Vegetative cells are strains suggest that the diversity of myxobacterial secondary relatively large, measuring 3–6 μm long and 0.7–1.0 μmwide metabolism is far greater than previously appreciated. The (Krzemieniewska and Krzemieniowski 1928). Different cell present review discusses the structure, cytology, physiology, types with other characters can be used to divide the and ecology of myxobacteria, as well as their secondary me- Myxobacteriales into three sub-orders, the Cytobacterineae, tabolite production and social interactions. Sorangiineae and Nannocystineae (Garcia et al. 2010). For a century, taxonomy and classification of myxobacteria were based on morphological traits such as shape of cell and * Wioletta Wrótniak-Drzewiecka fruiting bodies, size, colour and swarm patterns. However, [email protected] morphological similarity often does not represent genetic sim- ilarity, and morphology-based phylogenies may fail to model 1 Department of Microbiology, Faculty of Biology and Environmental relationships among species (Velicer and Hillesland 2008; Protection, Nicolaus Copernicus University, Lwowska 1, Garcia et al. 2010). 87-100 Torun, Poland The DNA sequence-based classification provides patterns 2 Department of Biotechnology, Sant Gadge Baba Amravati of ancestral relationship among myxobacterial species. In re- University, Amravat 444 602, Maharashtra, India cent years, 16S rRNA studies have shown that the group as a 18 Ann Microbiol (2016) 66:17–33 whole is phylogenetically coherent and belongs to the delta only M. xantus, but is also manifested by other bacteria. The group Proteobacteria, a large taxon of Gram-negative forms. mechanism whereby the bacterium senses the presence of a They are closely related to sulphate-reducing bacteria and physical or biological surface, specifically recognizes it and Bdellovibrio species, which are also predators of bacteria. associates with it is an area of microbiology that remains to be The sub-order Cystobacterinae includes the two most thor- clarified (Dawid et al. 1988). oughly studied species, Myxococcus xanthus and Stigmatella The present review is focused on different aspects of aurantiaca. The sub-order Soranginae includes the family myxobacteria, viz., ecology, cytology, social interactions, sig- Polyangiaceae with the genera Sorangium, an extensively nal transduction, predation, secondary metabolism and enzy- studied cellulose decomposer. The sub-order matic activity. Nannocystineae is a unique mixture of isolates grouped into two clusters: (1) the marine organisms Enhygromyxa and Plesiocystis, which are allied to the terrestrial nonhalophilic Ecology bacterium Nannocystis;and(2)theHaliangium-Kofleria clus- ter (Garcia et al. 2011). Jiang et al. (2007)proposedthatthe The myxobacteria seem to be a ubiquitous group of microor- myxobacteria exist in the environment in two forms — the ganisms that can inhabit very diverse habitats, including de- fruiting and the non-fruiting types. Most of the uncultured sert crust soils (Powell et al. 2015), the surface of the older myxobacteria may represent taxa that rarely form fruiting bod- leaves in grain crops, as well as the surface of wheat and ies, or may lack some or all of the developmental genes need- barley seeds (Leontievskaya and Dobrovol’skaya 2014), the ed for fruiting body formation. fruiting bodies and hyphosphere of several basidiomycetes Many phenomena and concepts originally described with (Zagriadskaia et al. 2014) and sewage sludge (Zhou et al. regard to social interactions among higher organisms have 2014a). Myxobacteria were dominant on the older leaves of equivalents in microorganisms. These include inter- grain crops and in grain of wheat and barley ears; species organismal communication, division of activity, self/non-self composition and structure of epiphytic bacterial communities recognition, kin selection vs. individual selection and social in the grain cereal crops changed in the course of vegetation conflict. Microorganisms offer the opportunity to study the (Leontievskaya and Dobrovol’skaya 2014). Nutrient-rich soils evolution of such social traits with a new level of rigor harbor more myxobacteria species, but these organisms can (Crespi 2001; Velicer and Stredwick 2002). Their rapid also live in rocky soils and pure sand (Dawid 2000). growth allows observations of evolutionary changes in labo- Myxobacteria are capable of bioreduction of water-soluble ratory populations. The social bacterium M. xanthus is a mod- uranium U(VI) to insoluble uranium U(IV). This phenomenon el system for the experimental study of microbial social evo- can be used for bioremediation of ground water contaminated lution. As a group, the myxobacteria produce a large variety of with uranium U(VI) and with other radionuclides (Newsome secondary metabolites, some of which may have medical uses et al. 2014). There is little contribution in the field of marine (Reichenbach and Höfle 1993; Gerth et al. 2003; Weissman myxobacteria (Felder et al. 2013). The marine myxobacteria, and Müller 2009;Diezetal.2012). The reasons why including Enhygromyxa, Plesiocystis, Pseudenhygromyxa, myxobacteria are multi-producers of secondary metabolites and Haliangium, are phylogenetically different from terrestrial are still not well understood. It has been argued that they myxobacteria. Most cultured species prefer mild temperatures confer a competitive advantage in soil environments, which (20–30 °C), neutral pH and high concentrations of organic maybeusedtomodulatecell–cell interactions and as weapons matter, but low ionic concentrations. Marine myxobacteria for predation. Answers to this question remain in the realm of occur in bottom sediments, and thus may have available high speculation. concentration of organic matter (Brinkhoff et al. 2012). Understanding the evolution of social phenotypes remains However, myxobacteria isolated from Antarctica grow at 4 ° a great challenge for the evolutionary biologist. This problem C (Dawid et al. 1988), and those from warm arid climates is daunting in higher organisms for many reasons, including have optimal growth temperatures of 42–44 °C (Gerth and limited knowledge of behavioral genetics and genotype–envi- Müller 2005). Only a few halophilic (Iizuka et al. 1998)or ronment interactions. Microbial social systems may help re- halotolerant (Li et al. 2002) strains of myxobacteria have been veal aspects of social evolution shared across all levels of isolated from coastal areas (Jiang et al. 2010). Many studies biological organization. It is now clear that cell–cell commu- suggest that our knowledge of the particular environments of nications and functional multicellularity among and between myxobacteria is limited by methods of isolation and cultiva- bacteria and eukaryotic cells are commonplace. These take tion. One of the commonly used myxobacteria isolation tech- place as a part of host–parasite interactions, biofilm formation, niques involves use of soil enrichment cultures (Fig. 1). multicellular development, and syntrophic interactions Myxobacteria
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