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Diversity of Myxobacteria—We Only See the Tip of the Iceberg

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Diversity of Myxobacteria—We Only See the Tip of the Iceberg microorganisms Review Diversity of Myxobacteria—We Only See the Tip of the Iceberg Kathrin I. Mohr Microbial Drugs (MWIS), Helmholtz Centre for Infection Research (HZI), 38124 Braunschweig, Germany; [email protected]; Tel.: +49-531-6181-4251 Received: 6 June 2018; Accepted: 8 August 2018; Published: 11 August 2018 Abstract: The discovery of new antibiotics is mandatory with regard to the increasing number of resistant pathogens. One approach is the search for new antibiotic producers in nature. Among actinomycetes, Bacillus species, and fungi, myxobacteria have been a rich source for bioactive secondary metabolites for decades. To date, about 600 substances could be described, many of them with antibacterial, antifungal, or cytostatic activity. But, recent cultivation-independent studies on marine, terrestrial, or uncommon habitats unequivocally demonstrate that the number of uncultured myxobacteria is much higher than would be expected from the number of cultivated strains. Although several highly promising myxobacterial taxa have been identified recently, this so-called Great Plate Count Anomaly must be overcome to get broader access to new secondary metabolite producers. In the last years it turned out that especially new species, genera, and families of myxobacteria are promising sources for new bioactive metabolites. Therefore, the cultivation of the hitherto uncultivable ones is our biggest challenge. Keywords: myxobacteria; diversity; uncultured; secondary metabolites; new antibiotics 1. Introduction We know little about the real diversity of myxobacteria in the environment. How many myxobacteria are cultivable under standard laboratory conditions? How many resist these cultivation efforts and lie undiscovered in the ground? After an introduction to myxobacteria, the status of antibiotics, myxobacterial secondary metabolites, the Great Plate Count Anomaly phenomenon, and microbial biogeography, the diversity of cultivable and uncultivated myxobacteria in different habitats is presented. Therefore, numerous sequences from the NCBI database were analysed. The intent of this review is to draw attention to the high amount of undiscovered myxobacteria and encourage further discovery and isolation of these hidden treasures with regard to their potential as new antibiotic producers. 2. Biology and Phylogeny of Myxobacteria Myxobacteria are soil dwelling deltaproteobacteria and are distributed all over the world. Temperate zones, tropical rain forests, arctic tundra, deserts, acidic soils [1–3], marine and other saline environments [4–7], and even caves [8], for example, are appropriate habitats. Myxobacteria can be isolated from various natural sources as soil, bark, rotting wood, leaves of trees, compost [9], or dung of herbivores [1,10]. They live aerobically, except the only described facultative anaerobic genus and species, Anaeromyxobacter dehalogenans [11]. Nevertheless, it is highly likely that further facultative or even strictly anaerobic myxobacteria exist, which hitherto withstand the common isolation efforts. Currently the monophyletic order Myxococcales comprises 3 suborders, 10 families, 29 genera, and 58 species (Figure1). Microorganisms 2018, 6, 84; doi:10.3390/microorganisms6030084 www.mdpi.com/journal/microorganisms Microorganisms 2018, 6, 84 2 of 23 Molecules 2018, 23, x FOR PEER REVIEW 2 of 23 42 43 FigureFigure 1.1. MonophyleticMonophyletic orderorder MyxococcalesMyxococcales (delta-proteobacteria),(delta-proteobacteria), suborders,suborders,families, families,and and generagenera ofof 44 myxobacteriamyxobacteria (status(status MayMay 2018).2018). TheThe numbernumber ofof speciesspecies withinwithin thethe generagenera isis mentionedmentioned inin bracketsbrackets 45 (original(original graphicgraphic fromfrom Corinna Corinna Wolf, Wolf, modified modified by by K. K. I. I. Mohr). Mohr). 46 Myxobacteria are fascinating because of their extraordinary social lifestyle, which is unique in Myxobacteria are fascinating because of their extraordinary social lifestyle, which is unique in the 47 the bacterial domain. Under appropriate environmental conditions, vegetative cells move in swarms bacterial domain. Under appropriate environmental conditions, vegetative cells move in swarms by 48 by gliding over solid surfaces [12]. Myxobacteria do not have flagella, but two motility systems, used gliding over solid surfaces [12]. Myxobacteria do not have flagella, but two motility systems, used 49 for locomotion, and well studied in Myxococcus xanthus, are known: social (S-) motility, powered by for locomotion, and well studied in Myxococcus xanthus, are known: social (S-) motility, powered 50 retraction of type IV pili is responsible for the movement of cells which travel in groups [13]. In by retraction of type IV pili is responsible for the movement of cells which travel in groups [13]. In 51 addition, extracellular matrix polysaccharide (EPS), also referred to as fibrils, are used. Therefore, the addition, extracellular matrix polysaccharide (EPS), also referred to as fibrils, are used. Therefore, the 52 intrinsic polarity of rod-shaped cells lays the foundation, and each cell uses two polar engines for intrinsic polarity of rod-shaped cells lays the foundation, and each cell uses two polar engines for 53 gliding on surfaces. It sprouts retractile type IV pili from the leading cell pole and secretes capsular gliding on surfaces. It sprouts retractile type IV pili from the leading cell pole and secretes capsular 54 polysaccharide through nozzles from the trailing pole [14]. On the other hand, slime secretion enables polysaccharide through nozzles from the trailing pole [14]. On the other hand, slime secretion enables 55 cell movements, when cells were isolated from the group (adventurous A-motility) [15]. For a cell movements, when cells were isolated from the group (adventurous A-motility) [15]. For a detailed 56 detailed description of myxobacterial gliding mechanisms see Nan et al. [13] and Faure et al. [16]. description of myxobacterial gliding mechanisms see Nan et al. [13] and Faure et al. [16]. 57 Due to their nutritional behavior and based on their specialization in degradation of Due to their nutritional behavior and based on their specialization in degradation of 58 biomacromolecules, members of the order Myxococcales can be divided into two groups: predators biomacromolecules, members of the order Myxococcales can be divided into two groups: predators 59 (the majority), which are able to lyse whole living cells of other microorganisms by exhausting lytic (the majority), which are able to lyse whole living cells of other microorganisms by exhausting 60 enzymes, and cellulose-decomposers, the latter are represented by the genera Sorangium and lytic enzymes, and cellulose-decomposers, the latter are represented by the genera Sorangium and 61 Byssovorax [12]. But, as mentioned for the (facultative) anaerobic myxobacteria, it is also highly likely Byssovorax [12]. But, as mentioned for the (facultative) anaerobic myxobacteria, it is also highly likely 62 that further cellulose-degrading genera exist, which successfully resisted standard cultivation that further cellulose-degrading genera exist, which successfully resisted standard cultivation attempts. 63 attempts. If nutrients become rare, the cells undergo an impressive process of cooperative morphogenesis. 64 If nutrients become rare, the cells undergo an impressive process of cooperative morphogenesis. Cells agglomerate and form species-specific fruiting bodies by directed cell movement [12]. These 65 Cells agglomerate and form species-specific fruiting bodies by directed cell movement [12]. These fruiting bodies consist of one to several sporangioles [1]. The architecture of these fruiting bodies ranges 66 fruiting bodies consist of one to several sporangioles [1]. The architecture of these fruiting bodies from simple, single sporangioles (M. xanthus, Cystobacter spp.), stalked sporangioles (M. stipitatus), or 67 ranges from simple, single sporangioles (M. xanthus, Cystobacter spp.), stalked sporangioles (M. 68 stipitatus), or even delicate tree-like structures of high complexity (Chondromyces spp.; Stigmatella Microorganisms 2018, 6, 84 3 of 23 Molecules 2018, 23, x FOR PEER REVIEW 3 of 23 69 evenspp.) delicate [10]. Colors tree-like of cells/fruiting structures of bodies high complexity vary from (milky,Chondromyces yellow,spp.; orange,Stigmatella red, brownspp.) to [ 10even]. Colors black 70 of(Figure cells/fruiting 2) [1]. bodies vary from milky, yellow, orange, red, brown to even black (Figure2)[1]. 71 72 FigureFigure 2.2. VariationVariation ofof myxobacterialmyxobacterial fruitingfruiting bodies. bodies. Genus/species,Genus/species, strainstrain designation,designation, (agar(agar 73 medium)medium) areare mentioned.mentioned. ((a)a) Myxococcus Myxococcus xanthusxanthusMxx42 Mxx42 (P); (P); ( b(b)) Cystobacter Cystobacter ferrugineus ferrugineusCbfe48 Cbfe48 (VY/2); (VY/2); 74 ((c)c) Archangium Archangiumsp. sp. Ar7747 Ar7747 (VY/2); (VY/2);( d(d)) Chondromyces Chondromycessp. sp. (Stan(Stan 2121 withwith filter);filter);( e(e)) Sorangium Sorangiumsp. sp. SoceSoce 75 14621462 degradingdegrading filterfilter paperpaper onon Stan Stan 21 21 agar; agar; ( f(f)) Polyangium Polyangiumsp. sp. Pl3323 Pl3323 (VY/2); (VY/2); ((g)g) CystobacterCystobacter fuscusfuscus 76 Cbf18Cbf18 (VY/2);(VY/2); ((h)h) Corallococcus coralloides Ccc379 (VY/2). 77 A known function of these mainly carotenoid or melanoid pigments is to provide protection A known function
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