Abstract
Myxobacteria are fascinating Gram-negative bacteria whose life cycle includes the formation of multicellular 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 primitive kind of multicellular development. Myxobacteria have multiple traits that are clearly social in nature; they move and feed socially. These processes require specific intercellular signals, thereby exhibiting a sophisticated level of the inter-organismal communication. Myxobacteria are predators. Predation is social not only with respect to searching for prey (motility) but also in the killing of prey. Swarming groups of cells secrete antibiotics and bacteriolytic compounds that kill and lyse their prey, and food is thereby released. Since the last three decades, myxobacteria are known as valuable producers of secondary metabolites exhibiting various biological activities. Myxobacterial metabolites exhibit many unique structural features as well as rare or novel modes of action, making them attractive lead structures for drug development. Both genome sequencing and metabolic profiling of myxobacterial strains suggest that the diversity of myxobacterial secondary metabolism is far greater than previously appreciated. The present review discusses the structure, cytology, physiology, and ecology of myxobacteria, as well as their secondary metabolite production and social interactions.
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References
Ahn JW, Jang KH, Chung SC, Oh KB, Shin J (2008) Sorangiadenosine, a new sesquiterpene adenoside from the myxobacterium Sorangium cellulosum. Org Lett 10:1167–1169
Altendorfer M, Irschik H, Menche D (2012) Design, synthesis and biological evaluation of simplified side chains of the macrolide antibiotic etnangien. Bioorg Med Chem Lett 22:5731–5734
Alvarez-Sieiro P, Martin MC, Redruello B, Rio B, Ladero V, Palanski BA, Khosla C, Fernandez M, Alvarez MA (2014) Generation of food-grade recombinant Lactobacillus casei delivering Myxococcus xanthus prolyl endopeptidase. Appl Microbiol Biotechnol 98(15):6689–6700
Barbier J, Jansen R, Irschik H, Benson S, Gerth K, Böhlendorf B, Höfle G, Reichenbach H, Wegner J, Zeilinger C, Kirschning A, Müller R (2012) Isolation and total synthesis of icumazoles and noricumazoles antifungal antibiotics and cation-channel blockers from Sorangium cellulosum. Angew Chem Int Ed 44(42):6828–6846
Behmlander RM, Dworkin M (1994) Biochemical and structural analyses of the extracellular matrix fibrils of Myxococcus xanthus. J Bacteriology 176:6295–6303
Berleman JE, Scott J, Chumley T, Kirby JR (2008) Predataxis behavior in Myxococcus xanthus. Proc Natl Acad Sci U S A 105:17127–17132
Berleman JE, Vicente JJ, Davis AE, Jiang SY, Seo Y-E et al (2011) FrzS regulates social motility in Myxococcus xanthus by controlling exopolysaccharide production. PLoS ONE 6(8):e23920. doi:10.1371/journal.pone.0023920
Beyer S, Kunze B, Silakowski B, Müller R (1999) Metabolic diversity in myxobacteria: identification of the myxalamid and the stigmatellin biosynthetic gene cluster of Stigmatella aurantiaca Sg a15 and a combined polyketide-(poly)peptide gene cluster from the epothilone producing strain Sorangium cellulosum So ce90. Biochim Biophys Acta 1445:185–195
Bode HB, Müller R (2005) The impact of bacterial genomics on natural product research. Angew Chem Int Ed 44(42):6828–6846
Bode HB, Meiser P, Klefisch T, Socorro N, Cortina J, Krug D, Göhring A, Schwär G, Mahmud T, Elnakady YA, Müller R (2007) Mutasynthesis-derived myxalamids and origin of the isobutyryl-CoA starter unit of myxalamid. Chembiochem 8(17):2139–2144
Brinkhoff T, Fischer D, Vollmers J, Voget S, Beardsley C, Thole S, Mussmannn M, Kunze B, Wagner-Dobler I, Daniel R, SImon M (2012) Biogeography and phylogenetic diversity of a cluster of exclusively marine myxobacteria. ISME J 6:1260–1272
Brzezińska AJ (2012) Myxobacteria as a factor bio-controlling of the trees roots. PhD Thesis, Nicolaus Copernicus University, Torun, Poland
Bui NK, Gray J, Schwarz H, Schumann P, Blanot D, Vollmer W (2009) The peptidoglycan sacculus of Myxococcus xanthus has unusual structural features and is degraded during glycerol-induced myxospore development. J Bacteriol 191(2):494–505
Buntin K, Rachid S, Scharfe M, Blöcker H, Weissman KJ, Müller R (2008) Production of the antifungal isochromanone ajudazols A and B in Chondromyces crocatus Cm c5: biosynthetic machinery and cytochrome P450 modifications. Angew Chem Int Ed Engl 47:4595–4599
Carvalho R, Reid R, Viswanathan N, Gramajo H, Julien B (2005) The biosynthetic genes for disorazoles, potent cytotoxic compounds that disrupt microtubule formation. Gene 359:91–98
Chen H, Keseler IM, Shimkets LJ (1990) Genome size of Myxococcus xanthus determined by pulsed-field gel electrophoresis. J Bacteriol 172:4206–4213
Crespi BJ (2001) The evolution of social behavior in microorganisms. Trends Ecol Evol 16:178–183
Curtis PD, Geyer R, White DC, Shimkets LJ (2006) Novel lipids in Myxococcus xanthus and their role in chemotaxis. Environ Microbiol 8:1935–1949
Dahm H, Brzezińska AJ, Wrótniak-Drzewiecka W, Golińska P, Różycki H, Rai M (2015) Myxobacteria as a potential biocontrol agent for control of economically important pathogenic fungi of forest trees. Dendrobiology (in press)
Darnell CL, Wilson JM, Tiwari N, Fuentesc E, Kirby JR (2014) Chemosensory regulation of a HEAT-repeat protein couples aggregation and sporulation in Myxococcus xanthus. J Bacteriol 196(17):3160–3168
Dawid W (2000) Biology and global distribution of myxobacteria in soils. FEMS Microbiol Rev 24:403–427
Dawid W, Galikowski CA, Hirsch P (1988) Psychrophilic myxobacteria from antarctic soils. Polarforschung 58:217–278
Dejon L, Speicher A (2013) Synthesis of aurachin D and isoprenoid analogues from the myxobacterium Stigmatella aurantiaca. Tetrahedron Lett 54:6700–6702
Diez J, Martinez JP, Metres J, Sasse F, Frank R, Meyerhans A (2012) Myxobacteria: natural pharmaceutical factories. Microb Cell Fact 11:52
Ducret A, Valignat MP, Mouhamar F, Mignot T, Theodoly O (2012) Wet-surface-enhanced ellipsometric contrast microscopy identifies slime as a major adhesion factor during bacterial surface motility. Proc Natl Acad Sci U S A 109:10036–10041
Ducret A, Fleuchot B, Bergam P, Mignot T (2013) Direct live imaging of cell–cell protein transfer by transient outer membrane fusion in Myxococcus xanthus. eLife 2:e00868. doi:10.7554/eLife.0086
Dworkin M (1972) Myxobacteria: new directions in studies of prokaryotic development. Crit Rev Microbiol 1:435–452
Dworkin M (1999) Fibrils as extracellular appendages of bacteria: their role in contact-mediated cell–cell interactions in Myxococcus xanthus. BioEssays 21:590–595
Evans K, Hobley L, Lambert C, Sockett RE (2008) Bdellovibrio: lone hunter cousin of the pack hunting myxobacteria. In: Whitworth DE (ed) Myxobacteria, multicellularity and differentiation. ASMPress, Washington, D.C, pp 351–362
Felder S, Dreisigacker S, Kehraus S, Neu E, Bierbaum G, Wright PR, Menche D, Schaberle TF, Kçnig GM (2013) Salimabromide: unexpected chemistry from the obligate marine, myxobacterium Enhygromyxa salina. Chem Eur J 19:9319–9324
Feng Z, Qi J, Tsuge T, Oba Y, Kobayashi T, Suzuki Y, Sakagami Y, Ojika M (2005) Construction of a bacterial artificial chromosome library for a myxobacterium of the genus Cystobacter and characterization of an antibiotic biosynthetic gene cluster. Biosci Biotechnol Biochem 69:1372–1380
Fink JM, Zissler JF (1989) Characterization of lipopolysaccharide from Myxococcus xanthus by use of monoclonal antibodies. J Bacteriol 171:2028–2032
Fleta-Soriano E, Martinez JP, Hinkelmann B, Gerth K, Washausen P, Diez J, Frank R, Sasse F, Meyerhans A (2014) The myxobacterial metabolite ratjadone A inhibits HIV infection by blocking the Rev/CRM1-mediated nuclear export pathway. Microb Cell Fact 13:17. doi:10.1186/1475-2859-13-17
Freese A, Reichenbach H, Lunsdorf H (1997) Further characterization and in situ localization of chain-like aggregates of the gliding bacteria Myxococcus fulvus and Myxococcus xanthus. J Bacteriol 179:1246–1252
Garcia R, Gerth K, Stadler M, Dogma IJ, Müller R (2010) Expanded phylogeny of myxobacteria and evidence for cultivation of the unculturables. Molec Phylogen Evol 57:78–887
Garcia R, Pistorius D, Müller R (2011) Fatty acid-related phylogeny of myxobacteria as an approach to discover polyunsaturated omega-3/6 fatty acids. J Bacteriol 193(8):1930–1942
Gerth K, Müller R (2005) Moderately thermophilic myxobacteria: novel potential for the production of natural products isolation and characterization. Environ Microbiol 7:874–880
Gerth K, Pradella S, Perlova O, Beyer S, Müller R (2003) Myxobacteria: proficient producers of novel natural products with various biological activities - past and future biotechnological aspects with the focus on the genus Sorangium. J Biotechnol 106:233–253
Gill JS, Dworkin M (1986) Cell surface antigens during submerged development of Myxococcus xanthus examined with monoclonal antibodies. J Bacteriol 168:505–511
Gnosspelius G (1978) Myxobacterial slime and proteolytic activity. Arch Microbiol 116:51–59
Goldman BS, Nierman WC, Kaiser D, Slater SC, Durkin AS, Eisen JA, Ronning CM, Barbazuk WB, Blanchard M, Field C, Halling C, Hinkle G, Iartchuk O, Kim HS, Mackenzie C, Madupu R, Miller N, Shvartsbeyn A, Sullivan SA, Vaudin M, Wiegand R, Kaplan HB (2006) Evolution of sensory complexity recorded in a myxobacterial genome. Proc Natl Acad Sci U S A 103:15200–15205
Gong G, Wei X, Huang Y, Chen X (2014) Preparation and regeneration of protoplast from antitumor agent epothilone-producing microbes myxobacteria. J Chem Pharma Res 6(3):472–476
Guerrero R, Esteve I, Pedrosalio C, Gaju N (1987) Predatory bacteria in procaryotic communities—the earliest trophic relationships. Ann NY Acad Sci 503:238–250
Guo WJ, Tao WY (2008) Phoxalone, a novel macrolide from Sorangium cellulosum: structure identification and its anti-tumor bioactivity in vitro. Biotechnol Lett 3:349–356
Harvey CW, Alber M, Tsimring LS, Aranson IS (2013) Continuum modeling of myxobacteria clustering. New J Phys 15:035029
Hou P, Li Y, Wu B, Yan Y, Yan B, Gao B (2006) Cellulolytic complex exist in cellulolytic myxobacterium Sorangium. Enzyme Microb Tech 38:273–278
Huang H, Menefee M, Edgerly M, Zhuang S, Kotz H, Poruchynsky M, Huff LM, Bates S, Fojo T (2010) A phase II clinical trial of ixabepilone (Ixempra; BMS-247550; NSC 710428), an epothilone B analog, in patients with metastatic renal cell carcinoma. Clin Cancer Res 16:1634–1641
Huntley S, Zhang Y, Treuner-Lange A, Kneip S, Sensen CW, Søgaard-Andersen L (2012) Complete genome sequence of the fruiting myxobacterium Corallococcus coralloides DSM 2259. J Bacteriol 194(11):3012–3013
Huntley S, Kneip S, Treuner-Lange A, Søgaard-Andersen L (2013) Complete genome sequence of Myxococcus stipitatus strain DSM 14675, a fruiting myxobacterium. Genome Announc 1(2):e00100–e00113. doi:10.1128/genomeA.00100-13
Hutchings MI, Palmer T, Harrington DJ, Sutcliffe IC (2009) Lipoprotein biogenesis in Gram-positive bacteria: knowing when to hold’em, knowing when to fold’em. Trends Microbiol 17:13–21
Iizuka T, Jojima Y, Fudou R, Yamanaka S (1998) Isolation of myxobacteria from the marine environment. FEMS Microbiol Lett 169:317–322
Irschik H, Jansen R, Gerth K, Hofle G, Reichenbach H (1987) The sorangicins novel and powerful inhibitors of eubacterial RNA polymerase isolated from myxobacteria. J Antibiot (Tokyo) 40:7–13
Irschik H, Schummer D, Höfle G, Reichenbach H, Steinmetz H, Jansen R (2007) Etnangien, a macrolide-polyene antibiotic from Sorangium cellulosum that inhibits nucleic acid polymerase. J Nat Prod 70:1060–1063
Irschik H, Washausen P, Sasse F, Fohrer J, Huch V, Muller R, Prusov EV (2013) Isolation, structure elucidation, and biological activity of maltepolides: Remarkable macrolides from myxobacteria. Angew Chem Int Ed 52:5402–5405
Jansen R, Irschik H, Reichenbach H, Höfle G (1997) Antibiotics from gliding bacteria, LXXXŁ Chivosayoles A-FŁ novel antifungal and cytotoxic macrolides from Sorangium cellulosum (Myxobacteria). Liebigs Ann 1725–1732
Jansen R, Irschik H, Huch V, Schummer D, Steinmetz H, Bock M, Schmidt T, Kirschning A, Müller R (2010) Carolacton—a macrolide ketocarbonic acid reducing biofilm formation by the caries- and endocarditis-associated bacterium Streptococcus mutans. Europ J Org Chem 7:1284–1289
Jiang DM, Wu ZH, Zhao JY, Li YZ (2007) Fruiting and non-fruiting myxobacteria: a phylogenetic perspective of cultured and uncultured members of this group. Mol Phylogenet Evol 44:545–552
Jiang DM, Kato C, Zhou XW, Wu ZH, Sato T, Li YZ (2010) Phylogeographic separation of marine and soil myxobacteria at high levels of classification. ISME J 4:1520–1530
Johnson TA, Sohn J, Vaske YM, White KN, Cohen TL, Vervoort HC, Tenney K, Valeriote FA, Bjeldanes LF, Drews P (2012) Myxobacteria versus sponge-derived alkaloids: the bengamide family identified as potent immune modulating agents by scrutiny of LC-MS/ELSD libraries. Bioorg Med Chem 20:4348–4355
Julien B, Shah S, Ziermann R, Goldman R, Katz L, Khosla C (2000) Isolation and characterization of the epothilone biosynthetic gene cluster from Sorangium cellulosum. Gene 249:153–160
Kaimer C, Berleman JE, Szuman DR (2012) Chemosensory signaling controls motility and subcellular polarity in Myxococcus xanthus. Curr Opin Microbiol 15:751–757
Kaiser D (1998) How and why myxobacteria talk to each other. Curr Opin Microbiol 1:663–668
Kaiser D (2004) Signaling in myxobacteria. Ann Rev Microbiol 58:75–98
Kaiser D (2013) Are myxobacteria intelligent? Frontiers in microbiology, evolutionary and genomic microbiology 4, Article 335. doi:10.3389/fmicb.2013.00335
Kaiser D (2015) Signaling in swarming and aggregating myxobacteria. In: Ruiz-Trillo I, Nedelcu AM, Ruiz-Trillo I, Nedelcu AM (eds) Evolutionary transitions to multicellular life: advances in marine genomics, vol. 2. Springer Science + Business Media, Dordrecht, pp 469–485
Kaiser D, Robinson M, Kroos L (2010) Myxobacteria, polarity, and multicellular morphogenesis. Cold Spring Harb Perspect Biol 2:a000380
Kearns DB, Bonner PJ, Smith DR, Shimkets LJ (2002) An extracellular matrix-associated zinc metalloprotease is required for dilauroyl phosphatidylethanolamine chemotactic excitation in Myxococcus xanthus. J Bacteriol 184:1678–1684
Kim J, Chung J, Cho K, Yi Y (2009) Isolation and characterization of myxobacteria with proteolytic activity. Kor J Microbiol Biotechnol 37(3):183–188
Kim SJ, Lee YJ, Kim JB (2013) Myxobacterial metabolites enhance cell proliferation and reduce intracellular stress in cells from a Parkinson’s disease mouse model. Gene 514:36–40
Kirby JR, Berleman JE, Muller S, Li D, Scott JC, Wilson JM (2008) Chemosensory signal transduction systems in Myxococcus xanthus. In: Whitworth DE (ed) Myxobacteria: multicellularity and differentiation. American Society for Microbiology, Washington, DC, pp 135–147
Konovalova A, Petters T, Sogaard-Andersen L (2010) Extracellular biology of Myxococcus xanthus. FEMS Microbiol Rev 34:89–106
Kopp M, Irschik H, Gemperlein K, Buntin K, Meiser P, Weissman KJ, Bode HB, Müller R (2011) Insights into the complex biosynthesis of the leupyrrins in Sorangium cellulosum So ce690. Mol Biosyst 7(5):1549–1563
Krell T, Busch A, Lacal J, Silva-Jiménez H, Ramos JL (2009) The enigma of cytosolic two-component systems: a hypothesis. Environ Microbiol Rep 1(3):171–176
Kroos L (2007) The Bacillus and Myxococcus developmental networks and their transcriptional regulators. Annu Rev Genet 41:13–39
Krug D, Zurek G, Revermann O, Vos M, Velicer GJ, Müller R (2008) Discovering the hidden secondary metabolome of Myxococcus xanthus: a study of intraspecific diversity. Appl Environ Microbiol 74(10):3058–3068
Kruse T, Lobedanz S, Berthelsen NMS, Søgaard-Andersen L (2001) C-signal: a cell surface-associated morphogen that induces and co-ordinates multicellular fruiting body morphogenesis and sporulation in Myxococcus xanthus. Mol Microbiol 40:156–168
Krzemieniewska H, Krzemieniowski S (1928) Morfologia komórki miksobakteryjnej. Acta Soc Bot Pol 6:46–90
Kudryashev M, Cyrklaff M, Alex B, Lemgruber L, Baumeister W, Wallich R, Frischknecht F (2011) Evidence of direct cell–cell fusion in Borrelia by cryogenic electron tomography. Cell Microbiol 13:731–741
Kulp A, Kuehn MJ (2010) Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 64:163–184
Lancero H, Brofft JE, Downard J, Birren BW, Nusbaum C, Taylor J, Shi W, Shimkets LJ (2002) Mapping of Myxococcus xanthus social motility dsp mutations to the dif genes. J Bacteriol 184:1462–1465
Leonardy S, Bulyha I, Søgaard-Andersen L (2008) Reversing cells and oscillating proteins. Mol Biosyst 4:1009–1014
Leontievskaya FA, Dobrovol’skaya TG (2014) Epiphytic bacterial complexes in grain crops: taxonomic composition and antagonistic properties. Eurasian Soil Sci 47(1):1033–1037
Li YZ, Hu W, Zhang YQ, Qiu ZJ, Zhang Y, Wu BH (2002) A simple method to isolate salt-tolerant myxobacteria from marine samples. J Microbiol Methods 50:205–209
Li Y, Sun H, Ma X, Lu A, Lux R, Zusman D, Shi W (2003) Extracellular polysaccharides mediate pilus retraction during social motility of Myxococcus xanthus. Proc Natl Acad Sci U S A 100:5443–5448
Li Y, Weissman KJ, Müller R (2008) Myxochelin biosynthesis: direct evidence for two- and four-electron reduction of a carrier protein-bound thioester. J Am Chem Soc 130:7554–7555
Li ZF, Li X, Liu H, Han K, Wu ZH, Hu W, Li FF, Li YZ (2011) Genome sequence of the halotolerant marine bacterium Myxoccocus fulvus HW-1. J Bacteriol 193:5015–5016
Ligon J, Hill S, Beck J, Zirkle R, Molnar I, Zawodny J, Money S, Schupp T (2002) Characterization of the biosynthetic gene cluster for the antifungal polyketide soraphen A from Sorangium cellulosum So ce26. Gene 285:257–267
Mashburn-Warren LM, Whiteley M (2006) Special delivery: vesicle trafficking in prokaryotes. Mol Microbiol 61:839–846
Mauriello EMF, Mignot T, Yang Z, Zusman DR (2010) Gliding motility revisited: how do the myxobacteria move without flagella? Microbiol Mol Bio Rev 74(2):229–249
McBride MJ (2001) Bacterial gliding motility: multiple mechanisms for cell movement over surfaces. Annu Rev Microbiol 55:49–75
McBride MJ, Zusman DR (1996) Behavioral analysis of single cells of Myxococcus xanthus in response to prey cells of Escherichia coli. FEMS Microbiol Lett 137:227–231
Merroun ML, Chekroun KB, Arias JM, Gonzales-Munoz MT (2003) Lanthanum fixation by Myxococcus xanthus: cellular location and extracellular polysaccharide observation. Chemosphere 52:113–120
Michałowska M (2009) Prevalence and characteristics of the bacteria in a row Myxococcales isolated from selected Polish soil types. PhD thesis. Warsaw. WAU. Typescript pp. 434
Mogensen JE, Otzen DE (2005) Interactions between folding factors and bacterial outer membrane proteins. Mol Microbiol 57:326–346
Moraleda-Muñoz A, Shimkets LJ (2007) Lipolytic enzymes in Myxococcus xanthus. J Bacteriol 189:3072–3080
Morgan AD, MacLean RC, Hillesland KL, Velicer GJ (2010) Comparative analysis of Myxococcus predation on soil bacteria. Appl Environ Microbiol 76:6920–6927
Mori Y, Kimura Y (2014) Myxococcus xanthus low-molecular-weight protein tyrosine phosphatase homolog, ArsA, possesses arsenate reductase activity. J Biosci Bioeng 118(1):10–13
Muller FD, Schink CW, Hoiczyk E, Cserti E, Higgs PI (2012) Spore formation in Myxococcus xanthus is tied to cytoskeleton functions and polysaccharide spore coat deposition. Mol Microbiol 83:486–505
Muller S, Willet JW, Bahr SM, Darnell CL, Hummels KR, Dong CK, Vlamakis HC, Kirby JR (2013) Draft genome sequence of Myxococcus xanthus wild-type strain DZ2, a model organism for predation and development. Genome Announc 1(3):e00217–13. doi:10.1128/genomeA.00217-13
Mulzer JH (2009) The epothilones—an outstanding family of anti-tumour agents: from soil to the clinic. Springer Verlag, Wien
Nan B, Zusman DR (2011) Uncovering the mystery of gliding motility in the myxobacteria. Annu Rev Genet 45:21–39
Nan B, Chen J, Neu JC, Berry RM, Oster G, Zusman DR (2010) Myxobacteria gliding motility requires cytoskeleton rotation powered by proton motive force. PNAS 106(6):2498–2503
Nan B, McBride MJ, Chen J, Zusman DR, Oster G (2014) Bacteria that glide with helical tracks. Curr Biol 24(4):R169–R173
Newsome L, Morris K, Lloyd JR (2014) The biogeochemistry and remediation of uranium and other priority radionuclides. Chem Geol 363:164–184
O’Connor KA, Zusman DR (1989) Patterns of cellular interactions during fruiting-body formation in Myxococcus xanthus. J Bacteriol 17(1):6013–6024
O’Neill A, Oliva B, Storey C, Hoyle A, Fishwick C, Chopra I (2000) RNA polymerase inhibitors with activity against rifampin - resistant mutants of Staphylococcus aureus. Antimicrob Agents Chemother 44:3163–3166
Pathak DT, Wall D (2012) Identification of the cglC, cglD, cglE, and cglF genes and their role in cell contact-dependent gliding motility in Myxococcus xanthus. J Bacteriol 194(8):1940–1949
Pathak DT, Wei X, Wall D (2012a) Myxobacterial tools for social interactions. Res Microbiol 163:579–591
Pathak DT, Wei X, Bucuvalas A, Haft DH, Gerloff DL, Wall D (2012b) Cell contact-dependent outer membrane exchange in myxobacteria: genetic determinants and mechanism. PLoS Genet 8:e1002626
Perez J, Castaneda-Garcıa A, Jenke-Kodama H, Mullers R, Munoz-Dorado J (2008) Eukaryotic-like protein kinases in the prokaryotes and the myxobacterial kinome. Proc Natl Acad Sci U S A 105(41):15950–15955
Perlova O, Gerth K, Hans A, Kaiser O, Müller R (2006) Identification and analysis of the chivosazol biosynthetic gene cluster from the myxobacterial model strain Sorangium cellulosum Soce56. J Biotechnol 121:174–191
Plaga W, Stamm I, Schairer HU (1998) Intercellular signaling in Stigmatella aurantiaca: purification and characterization of stigmolone, a myxobacterial pheromone. Proc Natl Acad Sci U S A 95(19):11263–11267
Plaza A, Müller R (2014) Myxobacteria: chemical diversity and screening strategies. In Goss R, Carter G, Osbourne A. (eds.), Natural products: Discourse, diversity and design. Wiley-Blackwell, doi:10.1002/9781118794623.ch6
Plaza A, Garcia R, Bifulco G, Martinez JP, Hüttel S, Sasse F, Meyerhans A, Stadler M, Müller R (2012) Aetheramides A and B, potent HIV-inhibitory dep-sipeptides from a myxobacterium of the new genus “Aetherobacter”. Org Lett 14:2854–2857
Powell JT, Chatziefhimiou AD, Banack SA, Cox PA, Metcalf JS (2015) Desert crust microorganisms, their environment and human health. J Arid Environ 112(Part B):127–133
Pradella S, Hans A, Spröer H, Reichenbach H, Gerth K, Beyer S (2002) Characterization, genome size and genetic manipulation of the myxobacterium Sorangium cellulosum Soce 56. Arch Microbiol 178:484–492
Reichenbach H, Höfle G (1993) Biologically active secondary metabolites from myxobacteria. Biotechnol Adv 11(2):219–277
Reichenbach H, Dworkin M (1992) The myxobacteria. In: Trüper HG, Dworkin M, Harder W, Schleifer KH (eds) The prokaryotes, 2nd edn. Spriger-Verlag, Berlin, pp 3418–3487
Reinchenbach H (1999) The ecology of the myxobacteria. Environ Microbiol 1:15–21
Reinchenbach H (2001) Myxobacteria, producers of novel bioactive substances. J Ind Microbiol Biotechnol 27:149–156
Ronning CM, Nierman W (2008) The genomes of Myxococcus xanthus and Stigmatella aurantiaca. In: Whitworth D (ed) Myxobacteria. multicellularity and differentiation. Am Soc Microbiol, Washington DC, pp 17–41
Rosenberg E, Varon M (1984) Antibiotics and lytic enzymes. In: Rosenberg E (ed) Myxobacteria: development and cell interactions. Springer, New York, pp 109–125
Rosenbluh A, Eisenbach M (1992) Effect of mechanical removal of pili on gliding motility of Myxococcus xanthus. J Bacteriol 174:5406–5413
Sandmann A, Sasse F, Muüller R (2004) Identification and analysis of the core biosynthetic machinery of tubulysin, a potent cytotoxin with potential anticancer activity. Chem Biol 11:1071–1079
Saraf M, Pandya U, Thakkar A (2014) Role of allelochemicals in plant growth promotingrhizobacteria for biocontrol of phytopathogens. Microbiol Res 169(1):18–29
Sasaki M, Takegawa K, Kimura Y (2014) Enzymatic characteristics of an Apah-like phosphatase, PrpA, and a diadenosine tetraphosphate hydrolase, ApaH, from Myxococcus xanthus. FEBS Lett 588(18):3395–3402
Sasse F, Steinmetz H, Heil J, Höfle G, Reichenbach H (2000) Tubulysins, new cytostatic peptides from myxobacteria acting on microtubuli. Production, isolation, physico-chemical and biological properties. J Antibiot 53:879–885
Schäberle TF, Schiefer A, Schmitz A, König GM, Hoerauf A, Pfarr K (2014) Corallopyronin A: a promising antibiotic for treatment of filariasis. Int J Med Microbiol 304:72–78
Schierholz JM, Beuth J (2001) Implant infections: a haven for opportunistic bacteria. J Hosp Infect 49:87–93
Schlicker C, Mogk A, Bukan B (2004) A PDZ switch for a cellular stress response. Cell 117:417–419
Schmitz A, Felder S, Höver T, Kehraus S, Neu E, Lohr F, König GM, Schäberle TF (2013) Antibiotics from gliding bacteria. Phytochem Rev 12:507–516
Shimkets LJ (1990) Social and developmental biology of the myxobacteria. Microbiol Rev 54:473–501
Shimkets LJ (1999) Intercellular signaling during fruiting-body development of Myxococcus xanthus. Annu Rev Microbiol 53:525–549
Silakowski B, Nordsiek G, Kunze B, Blöcker H, Müller R (2001) Novel features in a combined polyketide synthase/nonribosomal peptide synthetase: the myxalamid biosynthetic gene cluster of the myxobacterium Stigmatella aurantiaca Sga15. Chem Biol 8:59–69
Simunowic VJ, Yapp S, Rachid S, Krug P, Meiser P, Müller R (2006) Myxovirescin biosynthesis is directed by an intriguing megasynthetase consisting of hybrid polyketide synthases /nonribosomal peptide synthetase, 3-hydroxy-3-methylglutaryl CoA synthases and trans-acting acyltransferases. Chembiochem 7:1206–1220
Singer M, Kaiser D (1995) Ectopic production of guanosine penta- and tetraphosphate can initiate early developmental gene expression in Myxococcus xanthus. Gene Dev 9:1633–1644
Skerker JM, Berg HC (2001) Direct observation of extension and retraction of type IV pili. Proc Natl Acad Sci U S A 98:6901–6904
Spormann AM (1999) Gliding motility in bacteria: insights from studies of Myxococcus xanthus. Microbiol Mol Biol Rev 63:621–641
Steinmetz H, Gerth K, Jansen R, Schläger N, Dehn R, Reinecke S, Kirschning A, Müller R (2011) Elansolid A, a unique macrolide antibiotic from Chitinophaga sancti isolated as two stable atropisomers. Angew Chem Int Ed Engl 50(2):532–536
Steinmetz H, Zander W, Shushni MA, Jansen R, Gerth K, Dehn R, Dräger G, Kirschning A, Müller R (2012) Precursor-directed syntheses and biological evaluation of new elansolid derivatives. Chembiochem 13(12):1813–1817
Stevens DC, Young J, Carmichael R, Tan J, Taylor RE (2014) Draft genome sequence of gephyronic acid producer Cystobacter violaceus strain Cb vi 76. Genome Announc 2(6):e01299–14. doi:10.1128/genomeA.01299-14
Sun M, Wartel M, Cascales E, Shaevitz JW, Mignot T (2011) Motordriven intracellular transport powers bacterial gliding motility. Proc Natl Acad Sci U S A 108:7559–7564
Velicer GJ, Hillesland KL (2008) Why cooperate? the ecology and evolution of myxobacteria. In: Whitworth D (ed) Myxobacteria. multicellularity and differentiation. Am Soc Microbiol, Washington, DC, pp 17–41
Velicer GJ, Stredwick KL (2002) Experimental social evolution with Myxococcus xanthus. A van Leeuw J Microbiol 81:155–164
Villaverde A (2010) Nanotechnology, bionanotechnology and microbial cell factories. Microb Cell Fact 9:53
Vlamakis HC, Kirby JR, Zusman DR (2004) The Che 4 pathway of Myxococcus xanthus regulates type IV pilus- mediated motility. Mol Microbiol 52:1799–1811
Volz C, Kegler C, Müller R (2012) Enhancer binding proteins act as hetero-oligomers and link secondary metabolite production to myxococcal development, motility and predation. Chem Biol 19:1447–1459
Wall D (2014a) Molecular recognition in myxobacterial outer membrane exchange: functional, social and evolutionary implications. Mol Microbiol 91:209–220
Wall D (2014b) Social interactions mediated by outer membrane exchange. In: Yang Z, Higgs PI (eds) Myxobacteria: genomics, cellular and molecular biology. Caister Academic Press, UK
Wall D, Kolenbrander PE, Kaiser D (1999) The Myxococcus xanthus pilQ (sglA) gene encodes a secretin homolog required for type IV pilus biogenesis, social motility and development. J Bacteriol 181:24–33
Wei X, Vassallo CN, Pathak DT, Wall D (2014) Myxobacteria produce outer membrane-enclosed tubes in unstructured environments. J Bacteriol 196(10):1807–1814
Weissman KJ, Müller R (2009) A brief tour of myxobacterial secondary metabolism. Bioorgan Med Chem 17:2121–2136
Weissman KJ, Müller R (2010) Myxobacterial secondary metabolites: bioactivities and modes of action. Nat Prod Rep 27:1276–1295
Wenzel SC, Müller R (2007) For a recent review on the biosynthesis of myxobacterial metabolites. Nat Prod Rep 24:1211
White D, Dworkin M, Tipper DJ (1968) Peptidoglycan of Myxococcus xanthus: structure and relation to morphogenesis. J Bacteriol 95:2186–2197
Whitworth DE, Cock PJA (2007) Myxobacterial two-component systems. In: Whitworth DE (ed) Myxobacteria: multicellularity and differentiation. Am Soc Microbiol, Washington, DC, pp 169–189
Whitworth DE, Cock PJA (2008) Two-component systems of the myxobacteria: structure, diversity and evolutionary relationships. Microbiology 150:360–372
Wiseman JW, Dworkin M (1977) Developmentally induced autolysis during fruiting body formation by Myxococcus xanthus. J Bacteriol 129:796–802
Wrótniak-Drzewiecka W, Laskowski D, Rai M (2013) Microbial synthesis of silver nanoparticles. W: Proceedings of XIV Conference DIAGMOL 2013 Molecular biology in diagnostics of infectious diseases and biotechnology”, 291 October 2013, WULS-SGGW in Warsaw, Poland
Wrótniak-Drzewiecka W, Gaikwad S, Laskowski D, Dahm H, Niedojadało J, Gade A, Rai M (2014) Novel approach towards synthesis of silver nanoparticles from Myxococcus virescens and their lethality on pathogenic bacterial cells. Austin J Biotechnol Bioeng 1(1): id1004: 01–07
Wu SS, Kaiser D (1995) Genetic and functional evidence that type — IV pili are required for social gliding motility in Myxococcus xanthus. Mol Microbiol 18:547–558
Wu Y, Jiang Y, Kaiser D, Alber M (2007) Social interactions in myxobacterial swarming. PLoS Comput Biol 3(12):253. doi:10.1371/journal.pcbi.0030253
Xiao Y, Wei X, Richard E, Wall D (2011) Antibiotic production by myxobacteria plays a role in predation. J Bacteriol 193:4626–4633
Yang C, Kaplan HB (1997) Myxococcus xanthus sasS encodes a sensor histidine kinase required for early developmental gene expression. J Bacteriol 179:7759–7767
Yang Z, Duan X, Esmaeiliyan M, Kaplan H (2008) Composition, structure and function of the Myxococcus xanthus cell envelope. In: Whitworth DE (ed) Myxobacteria. multicellularity and differentiation. Am Soc Microbiol, Washington DC, pp 17–41
Yu R, Kaiser D (2007) Gliding motility and polarized slime secretion. Mol Microbiol 63:454–467
Yu YT, Yuan X, Velicer GJ (2010) Adaptive evolution of an sRNA that controls Myxococcus development. Science 328(5981):993. doi:10.1126/science.1187200
Zafriri D, Rosenberg E, Mirelman D (1981) Mode of action of Myxococcus xanthus antibiotic TA. Antimicrob Agents Chemother 19:349–351
Zagriadskaia Yu A, Lysak LV, Sidorova II, Aleksandrova AV, Voronina E (2014) Bacterial complexes of the fruiting bodies and hyphosphere of certain basidiomycetes. Biology Bull 41(1):12–18
Zander W, Gerth K, Mohr K, Kessler W, Jansen R, Müller R (2011) Roimatacene: an antibiotic against gram-negative bacteria isolated from Cystobacter ferrugineus Cb G35 (myxobacteria). Chemistry 17:7875–7881
Zhou X, Li S, Li W, Jiang D, Han K, Wu Z, Li Y (2014a) Myxobacterial community is a predominant and highly diverse bacterial group in soil niches. Environ Microbiol Rep 6(1):45–56
Zhou Z, Qiao W, Xing C, Shen X, Hu D, Wang L (2014b) A micro-aerobic hydrolysis process for sludge in situ reduction: performance and microbial community structure. Bioresource Technol 173:452–456
Acknowledgments
This work has been supported by Grant from the Polish Ministry of Science and Higher Education (Grant No. 2 PO4 C 040 29). Dr Mahendra Rai is thankful to Nicolaus Copernicus University (Torun, Poland) for fellowships to Visiting Professors within the project “Enhancing Educational Potential of Nicolaus Copernicus University in the Disciplines of Mathematical and Natural Sciences” conducted under Sub-measure 4.1.1 Human Capital Operational Programme – Task 7 (Project No.POKL.04.01.01-00-081/10)”
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Wrótniak-Drzewiecka, W., Brzezińska, A.J., Dahm, H. et al. Current trends in myxobacteria research. Ann Microbiol 66, 17–33 (2016). https://doi.org/10.1007/s13213-015-1104-3
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DOI: https://doi.org/10.1007/s13213-015-1104-3