The complex development undergone by Streptomyces encompasses transitions from vegetative mycelial forms to reproductive aerial hyphae that differentiate into chains of single-celled spores. Whereas their mycelial life - connected with spore formation and antibiotic production - is deeply investigated, spore germination as the counterpoint in their life cycle has received much less attention. Still, germination represents a system of transformation from metabolic zero point to a new living lap. There are several aspects of germination that may attract our attention: (1) Dormant spores are strikingly well-prepared for the future metabolic restart; they possess stable transcriptome, hydrolytic enzymes, chaperones, and other required macromolecules stabilized in a trehalose milieu; (2) Germination itself is a specific sequence of events leading to a complete morphological remodeling that include spore swelling, cell wall reconstruction, and eventually germ tube emergences; (3) Still not fully unveiled are the strategies that enable the process, including a single cell's signal transduction and gene expression control, as well as intercellular communication and the probability of germination across the whole population. This review summarizes our current knowledge about the germination process in Streptomyces, while focusing on the aforementioned points.

Chemistry Department Faculty of Science Jan Evangelista Purkyně University in Ústí nad Labem Ústí nad Labem Czechia

Institute of Immunology and Microbiology 1st Faculty of Medicine Charles University Prague Czechia

Institute of Microbiology of the Czech Academy of Sciences Prague Czechia

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Alvarez-Alvarez R., Botas A., Albillos S. M., Rumbero A., Martin J. F., Liras P. (2015). Molecular genetics of naringenin biosynthesis, a typical plant secondary metabolite produced by Streptomyces clavuligerus. Microb. Cell Fact. 14 178. 10.1186/s12934-015-0373-7 PubMed DOI PMC

An T. Z., Iwakiri M., Edashige K., Sakurai T., Kasai M. (2000). Factors affecting the survival of frozen-thawed mouse spermatozoa. Cryobiology 40 237–249. 10.1006/cryo.2000.2245 PubMed DOI

Aoki Y., Matsumoto D., Kawaide H., Natsume M. (2011). Physiological role of germicidins in spore germination and hyphal elongation in Streptomyces coelicolor A3(2). J. Antibiot. 64 607–611. 10.1038/ja.2011.59 PubMed DOI

Aoki Y., Yoshida M., Kawaide H., Abe H., Natsume M. (2007). Isolation and characterization of a spore germination inhibitor from Streptomyces sp. CB-1-1, a phytopathogen causing root tumor of melon. Biosci. Biotechnol. Biochem. 71 986–992. 10.1271/bbb.60649 PubMed DOI

Ausmees N., Wahlstedt H., Bagchi S., Elliot M. A., Buttner M. J., Flardh K. (2007). SmeA, a small membrane protein with multiple functions in Streptomyces sporulation including targeting of a SpoIIIE/FtsK-like protein to cell division septa. Mol. Microbiol. 65 1458–1473. 10.1111/j.1365-2958.2007.05877.x PubMed DOI

Bagchi S., Tomenius H., Belova L. M., Ausmees N. (2008). Intermediate filament-like proteins in bacteria and a cytoskeletal function in Streptomyces. Mol. Microbiol. 70 1037–1050. 10.1111/j.1365-2958.2008.06473.x PubMed DOI PMC

Balaban N. Q., Merrin J., Chait R., Kowalik L., Leibler S. (2004). Bacterial persistence as a phenotypic switch. Science 305 1622–1625. 10.1126/science.1099390 PubMed DOI

Barabas G., Szabo G. (1968). Role of streptomycin in the life of Streptomyces griseus: streptidine-containing fractions in the cell walls of Streptomyces griseus strains. Can. J. Microbiol. 14 1325–1331. 10.1139/m68-222 PubMed DOI

Benaroudj N., Lee D. H., Goldberg A. L. (2001). Trehalose accumulation during cellular stress protects cells and cellular proteins from damage by oxygen radicals. J. Biol. Chem. 276 24261–24267. 10.1074/jbc.M101487200 PubMed DOI

Bentley S. D., Chater K. F., Cerdeno-Tarraga A. M., Challis G. L., Thomson N. R., James K. D., et al. (2002). Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417 141–147. 10.1038/417141a PubMed DOI

Bobek J., Halada P., Angelis J., Vohradsky J., Mikulik K. (2004). Activation and expression of proteins during synchronous germination of aerial spores of Streptomyces granaticolor. Proteomics 4 3864–3880. 10.1002/pmic.200400818 PubMed DOI

Bobek J., Strakova E., Zikova A., Vohradsky J. (2014). Changes in activity of metabolic and regulatory pathways during germination of S. coelicolor. BMC Genomics 15:1173. 10.1186/1471-2164-15-1173 PubMed DOI PMC

Briza P., Breitenbach M., Ellinger A., Segall J. (1990). Isolation of two developmentally regulated genes involved in spore wall maturation in Saccharomyces cerevisiae. Genes Dev. 4 1775–1789. 10.1101/gad.4.10.1775 PubMed DOI

Buerger S., Spoering A., Gavrish E., Leslin C., Ling L., Epstein S. S. (2012). Microbial scout hypothesis, stochastic exit from dormancy, and the nature of slow growers. Appl. Environ. Microbiol. 78 3221–3228. 10.1128/AEM.07307-11 PubMed DOI PMC

Bush M. J., Tschowri N., Schlimpert S., Flardh K., Buttner M. J. (2015). c-di-GMP signalling and the regulation of developmental transitions in streptomycetes. Nat. Rev. Microbiol. 13 749–760. 10.1038/nrmicro3546 PubMed DOI

Ceccarini C. (1967). The biochemical relationship between trehalase and trehalose during growth and differentiation in the cellular slime mold, Dictyostelium discoideum. Biochim. Biophys. Acta 148 114–124. 10.1016/0304-4165(67)90285-1 PubMed DOI

Chen D., Huang S. S., Li Y. Q. (2006). Real-time detection of kinetic germination and heterogeneity of single Bacillus spores by laser tweezers Raman spectroscopy. Anal. Chem. 78 6936–6941. 10.1021/ac061090e PubMed DOI

Chen K. C., Csikasz-Nagy A., Gyorffy B., Val J., Novak B., Tyson J. J. (2000). Kinetic analysis of a molecular model of the budding yeast cell cycle. Mol. Biol. Cell 11 369–391. 10.1091/mbc.11.1.369 PubMed DOI PMC

Claessen D., de Jong W., Dijkhuizen L., Wosten H. A. (2006). Regulation of Streptomyces development: reach for the sky! Trends Microbiol. 14 313–319. 10.1016/j.tim.2006.05.008 PubMed DOI

Claessen D., Rink R., de Jong W., Siebring J., de Vreugd P., Boersma F. G., et al. (2003). A novel class of secreted hydrophobic proteins is involved in aerial hyphae formation in Streptomyces coelicolor by forming amyloid-like fibrils. Genes Dev. 17 1714–1726. 10.1101/gad.264303 PubMed DOI PMC

Claessen D., Stokroos I., Deelstra H. J., Penninga N. A., Bormann C., Salas J. A., et al. (2004). The formation of the rodlet layer of streptomycetes is the result of the interplay between rodlins and chaplins. Mol. Microbiol. 53 433–443. 10.1111/j.1365-2958.2004.04143.x PubMed DOI

Claessen D., Wosten H. A., van Keulen G., Faber O. G., Alves A. M., Meijer W. G., et al. (2002). Two novel homologous proteins of Streptomyces coelicolor and Streptomyces lividans are involved in the formation of the rodlet layer and mediate attachment to a hydrophobic surface. Mol. Microbiol. 44 1483–1492. 10.1046/j.1365-2958.2002.02980.x PubMed DOI

Cohen-Gonsaud M., Keep N. H., Davies A. P., Ward J., Henderson B., Labesse G. (2004). Resuscitation-promoting factors possess a lysozyme-like domain. Trends Biochem. Sci. 29 7–10. 10.1016/j.tibs.2003.10.009 PubMed DOI

Constant P., Poissant L., Villemur R. (2008). Isolation of Streptomyces sp. PCB7, the first microorganism demonstrating high-affinity uptake of tropospheric H2. ISME J. 2 1066–1076. 10.1038/ismej.2008.59 PubMed DOI

Cowan A. E., Koppel D. E., Setlow B., Setlow P. (2003). A soluble protein is immobile in dormant spores of Bacillus subtilis but is mobile in germinated spores: implications for spore dormancy. Proc. Natl. Acad. Sci. U.S.A. 100 4209–4214. 10.1073/pnas.0636762100 PubMed DOI PMC

Crowe J. H., Crowe L. M., Chapman D. (1984). Preservation of membranes in anhydrobiotic organisms: the role of trehalose. Science 223 701–703. 10.1126/science.223.4637.701 PubMed DOI

de Jong W., Manteca A., Sanchez J., Bucca G., Smith C. P., Dijkhuizen L., et al. (2009). NepA is a structural cell wall protein involved in maintenance of spore dormancy in Streptomyces coelicolor. Mol. Microbiol. 71 1591–1603. 10.1111/j.1365-2958.2009.06633.x PubMed DOI

De Virgilio C., Hottiger T., Dominguez J., Boller T., Wiemken A. (1994). The role of trehalose synthesis for the acquisition of thermotolerance in yeast. I. Genetic evidence that trehalose is a thermoprotectant. Eur. J. Biochem. 219 179–186. 10.1111/j.1432-1033.1994.tb19928.x PubMed DOI

Derouaux A., Halici S., Nothaft H., Neutelings T., Moutzourelis G., Dusart J., et al. (2004). Deletion of a cyclic AMP receptor protein homologue diminishes germination and affects morphological development of Streptomyces coelicolor. J. Bacteriol. 186 1893–1897. 10.1128/JB.186.6.1893-1897.2004 PubMed DOI PMC

Diaz-Tielas C., Grana E., Reigosa M. J., Sanchez-Moreiras A. M. (2012). The role of peroxidases on the mode of action of chalcone in Arabidopsis roots. Plant Signal. Behav. 7 1274–1276. 10.4161/psb.21594 PubMed DOI PMC

Ditkowski B., Holmes N., Rydzak J., Donczew M., Bezulska M., Ginda K., et al. (2013). Dynamic interplay of ParA with the polarity protein, Scy, coordinates the growth with chromosome segregation in Streptomyces coelicolor. Open Biol. 3:130006. 10.1098/rsob.130006 PubMed DOI PMC

Eaton D., Ensign J. C. (1980). Streptomyces viridochromogenes spore germination initiated by calcium ions. J. Bacteriol. 143 377–382. PubMed PMC

Elbein A. D. (1974). The metabolism of alpha,alpha-trehalose. Adv. Carbohydr. Chem. Biochem. 30 227–256. 10.1016/S0065-2318(08)60266-8 PubMed DOI

Elbein A. D., Mitchell M. (1973). Levels of glycogen and trehalose in Mycobacterium smegmatis and the purification and properties of the glycogen synthetase. J. Bacteriol. 113 863–873. PubMed PMC

Elbein A. D., Pan Y. T., Pastuszak I., Carroll D. (2003). New insights on trehalose: a multifunctional molecule. Glycobiology 13 17R–27R. 10.1093/glycob/cwg047 PubMed DOI

Elliot M. A., Karoonuthaisiri N., Huang J., Bibb M. J., Cohen S. N., Kao C. M., et al. (2003). The chaplins: a family of hydrophobic cell-surface proteins involved in aerial mycelium formation in Streptomyces coelicolor. Genes Dev. 17 1727–1740. 10.1101/gad.264403 PubMed DOI PMC

Elliot M. A., Talbot N. J. (2004). Building filaments in the air: aerial morphogenesis in bacteria and fungi. Curr. Opin. Microbiol. 7 594–601. 10.1016/j.mib.2004.10.013 PubMed DOI

Ensign J. C. (1978). Formation, properties, and germination of actinomycete spores. Annu. Rev. Microbiol. 32 185–219. 10.1146/annurev.mi.32.100178.001153 PubMed DOI

Epstein S. S. (2009). Microbial awakenings. Nature 457:1083. 10.1038/4571083a PubMed DOI

Fillinger S., Chaveroche M. K., van Dijck P., de Vries R., Ruijter G., Thevelein J., et al. (2001). Trehalose is required for the acquisition of tolerance to a variety of stresses in the filamentous fungus Aspergillus nidulans. Microbiology 147(Pt 7) 1851–1862. 10.1099/00221287-147-7-1851 PubMed DOI

Flardh K. (2003a). Essential role of DivIVA in polar growth and morphogenesis in Streptomyces coelicolor A3(2). Mol. Microbiol. 49 1523–1536. 10.1046/j.1365-2958.2003.03660.x PubMed DOI

Flardh K. (2003b). Growth polarity and cell division in Streptomyces. Curr. Opin. Microbiol. 6 564–571. 10.1016/j.mib.2003.10.011 PubMed DOI

Flardh K., Buttner M. J. (2009). Streptomyces morphogenetics: dissecting differentiation in a filamentous bacterium. Nat. Rev. Microbiol. 7 36–49. 10.1038/nrmicro1968 PubMed DOI

Flardh K., Richards D. M., Hempel A. M., Howard M., Buttner M. J. (2012). Regulation of apical growth and hyphal branching in Streptomyces. Curr. Opin. Microbiol. 15 737–743. 10.1016/j.mib.2012.10.012 PubMed DOI

Foster J. W., Mc D. L., Woodruff H.B., Stokes J. L. (1945). Microbiological aspects of penicillin; conidiospore formation in submerged cultures of Penicillium notatum. J. Bacteriol. 50 365–368. PubMed PMC

Galperin M. Y., Mekhedov S. L., Puigbo P., Smirnov S., Wolf Y. I., Rigden D. J. (2012). Genomic determinants of sporulation in Bacilli and Clostridia: towards the minimal set of sporulation-specific genes. Environ. Microbiol. 14 2870–2890. 10.1111/j.1462-2920.2012.02841.x PubMed DOI PMC

Ghorbel S., Smirnov A., Chouayekh H., Sperandio B., Esnault C., Kormanec J., et al. (2006). Regulation of ppk expression and in vivo function of Ppk in Streptomyces lividans TK24. J. Bacteriol. 188 6269–6276. 10.1128/JB.00202-06 PubMed DOI PMC

Glauert A. M., Hopwood D. A. (1961). The fine structure of Streptomyces violaceoruber (S. coelicolor). III. The walls of the mycelium and spores. J. Biophys. Biochem. Cytol. 10 505–516. 10.1083/jcb.10.4.505 PubMed DOI PMC

Grantcharova N., Lustig U., Flardh K. (2005). Dynamics of FtsZ assembly during sporulation in Streptomyces coelicolor A3(2). J. Bacteriol. 187 3227–3237. 10.1128/JB.187.9.3227-3237.2005 PubMed DOI PMC

Grund A. D., Ensign J. C. (1985). Properties of the germination inhibitor of Streptomyces viridochromogenes spores. J. Gen. Microbiol. 131 833–847. 10.1099/00221287-131-4-833 PubMed DOI

Haiser H. J., Yousef M. R., Elliot M. A. (2009). Cell wall hydrolases affect germination, vegetative growth, and sporulation in Streptomyces coelicolor. J. Bacteriol. 191 6501–6512. 10.1128/JB.00767-09 PubMed DOI PMC

Hardisson C., Manzanal M. B., Salas J. A., Suarez J. E. (1978). Fine structure, physiology and biochemistry of arthrospore germination in Streptomyces antibioticus. J. Gen. Microbiol. 105 203–214. 10.1099/00221287-105-2-203 PubMed DOI

Heichlinger A., Ammelburg M., Kleinschnitz E. M., Latus A., Maldener I., Flardh K., et al. (2011). The MreB-like protein Mbl of Streptomyces coelicolor A3(2) depends on MreB for proper localization and contributes to spore wall synthesis. J. Bacteriol. 193 1533–1542. 10.1128/JB.01100-10 PubMed DOI PMC

Helmann J. D. (2006). Deciphering a complex genetic regulatory network: the Bacillus subtilis sigmaW protein and intrinsic resistance to antimicrobial compounds. Sci. Prog. 89(Pt 3–4) 243–266. 10.3184/003685006783238290 PubMed DOI PMC

Hempel A. M., Cantlay S., Molle V., Wang S. B., Naldrett M. J., Parker J. L., et al. (2012). The Ser/Thr protein kinase AfsK regulates polar growth and hyphal branching in the filamentous bacteria Streptomyces. Proc. Natl. Acad. Sci. U.S.A. 109 E2371–E2379. 10.1073/pnas.1207409109 PubMed DOI PMC

Henriques A. O., Moran C. P., Jr. (2007). Structure, assembly, and function of the spore surface layers. Annu. Rev. Microbiol. 61 555–588. 10.1146/annurev.micro.61.080706.093224 PubMed DOI

Hett E. C., Chao M. C., Deng L. L., Rubin E. J. (2008). A mycobacterial enzyme essential for cell division synergizes with resuscitation-promoting factor. PLOS Pathog. 4:e1000001. 10.1371/journal.ppat.1000001 PubMed DOI PMC

Hey-Ferguson A., Mitchell M., Elbein A. D. (1973). Trehalose metabolism in germinating spores of Streptomyces hygroscopicus. J. Bacteriol. 116 1084–1085. PubMed PMC

Hirsch C. F., Ensign J. C. (1976a). Heat activation of Streptomyces viridochromogenes spores. J. Bacteriol. 126 24–30. PubMed PMC

Hirsch C. F., Ensign J. C. (1976b). Nutritionally defined conditions for germination of Streptomyces viridochromogenes spores. J. Bacteriol. 126 13–23. PubMed PMC

Hirsch C. F., Ensign J. C. (1978). Some properties of Streptomyces viridochromogenes spores. J. Bacteriol. 134 1056–1063. PubMed PMC

Hong H. J., Paget M. S., Buttner M. J. (2002). A signal transduction system in Streptomyces coelicolor that activates the expression of a putative cell wall glycan operon in response to vancomycin and other cell wall-specific antibiotics. Mol. Microbiol. 44 1199–1211. 10.1046/j.1365-2958.2002.02960.x PubMed DOI

Hottiger T., Boller T., Wiemken A. (1989). Correlation of trehalose content and heat resistance in yeast mutants altered in the RAS/adenylate cyclase pathway: is trehalose a thermoprotectant? FEBS Lett. 255 431–434. 10.1016/0014-5793(89)81139-1 PubMed DOI

Jain N. K., Roy I. (2010). Trehalose and protein stability. Curr. Protoc. Protein Sci. 59 4.9.1–4.9.12. 10.1002/0471140864.ps0409s59 PubMed DOI

Jakimowicz D., van Wezel G. P. (2012). Cell division and DNA segregation in Streptomyces: how to build a septum in the middle of nowhere? Mol. Microbiol. 85 393–404. 10.1111/j.1365-2958.2012.08107.x PubMed DOI

Jang M. S., Mouri Y., Uchida K., Aizawa S., Hayakawa M., Fujita N., et al. (2016). Genetic and transcriptional analyses of the flagellar gene cluster in Actinoplanes missouriensis. J. Bacteriol. 198 2219–2227. 10.1128/JB.00306-16 PubMed DOI PMC

Jyothikumar V., Tilley E. J., Wali R., Herron P. R. (2008). Time-lapse microscopy of Streptomyces coelicolor growth and sporulation. Appl. Environ. Microbiol. 74 6774–6781. 10.1128/AEM.01233-08 PubMed DOI PMC

Kalakoutskii L. V., Agre N. S. (1976). Comparative aspects of development and differentiation in actinomycetes. Bacteriol. Rev. 40 469–524. PubMed PMC

Kallifidas D., Thomas D., Doughty P., Paget M. S. (2010). The sigmaR regulon of Streptomyces coelicolor A32 reveals a key role in protein quality control during disulphide stress. Microbiology 156(Pt 6) 1661–1672. 10.1099/mic.0.037804-0 PubMed DOI

Kandror O., DeLeon A., Goldberg A. L. (2002). Trehalose synthesis is induced upon exposure of Escherichia coli to cold and is essential for viability at low temperatures. Proc. Natl. Acad. Sci. U.S.A. 99 9727–9732. 10.1073/pnas.142314099 PubMed DOI PMC

Keep N. H., Ward J. M., Robertson G., Cohen-Gonsaud M., Henderson B. (2006). Bacterial resuscitation factors: revival of viable but non-culturable bacteria. Cell Mol. Life Sci. 63 2555–2559. 10.1007/s00018-006-6188-2 PubMed DOI PMC

Keijser B. J., Noens E. E., Kraal B., Koerten H. K., van Wezel G. P. (2003). The Streptomyces coelicolor ssgB gene is required for early stages of sporulation. FEMS Microbiol. Lett. 225 59–67. 10.1016/S0378-1097(03)00481-6 PubMed DOI

Kelemen G. H. (2017). Intermediate filaments supporting cell shape and growth in bacteria. Subcell. Biochem. 84 161–211. 10.1007/978-3-319-53047-5_6 PubMed DOI

Kelemen G. H., Brian P., Flardh K., Chamberlin L., Chater K. F., Buttner M. J. (1998). Developmental regulation of transcription of whiE, a locus specifying the polyketide spore pigment in Streptomyces coelicolor A3 (2). J. Bacteriol. 180 2515–2521. PubMed PMC

Kelemen G. H., Viollier P. H., Tenor J., Marri L., Buttner M. J., Thompson C. J. (2001). A connection between stress and development in the multicellular prokaryote Streptomyces coelicolor A3(2). Mol. Microbiol. 40 804–814. 10.1046/j.1365-2958.2001.02417.x PubMed DOI

Kleinschnitz E. M., Heichlinger A., Schirner K., Winkler J., Latus A., Maldener I., et al. (2011). Proteins encoded by the mre gene cluster in Streptomyces coelicolor A3(2) cooperate in spore wall synthesis. Mol. Microbiol. 79 1367–1379. 10.1111/j.1365-2958.2010.07529.x PubMed DOI

Kormanec J., Sevcikova B., Halgasova N., Knirschova R., Rezuchova B. (2000). Identification and transcriptional characterization of the gene encoding the stress-response sigma factor sigma(H) in Streptomyces coelicolor A3(2). FEMS Microbiol. Lett. 189 31–38. PubMed

Lederer E. (1976). Cord factor and related trehalose esters. Chem. Phys. Lipids 16 91–106. 10.1016/0009-3084(76)90001-3 PubMed DOI

Liot Q., Constant P. (2016). Breathing air to save energy–new insights into the ecophysiological role of high-affinity [NiFe]-hydrogenase in Streptomyces avermitilis. Microbiologyopen 5 47–59. 10.1002/mbo3.310 PubMed DOI PMC

Ma M., Rateb M. E., Yang D., Rudolf J. D., Zhu X., Huang Y., et al. (2017). Germicidins H-J from Streptomyces sp. CB00361. J. Antibiot. (Tokyo) 70 200–203. 10.1038/ja.2016.100 PubMed DOI

Martin M. C., Diaz L. A., Manzanal M. B., Hardisson C. (1986). Role of trehalose in the spores of Streptomyces. FEMS Microbiol. Lett. 35 49–54. 10.1016/0378-1097(86)90160-6 DOI

Maxwell C. A., Hartwig U. A., Joseph C. M., Phillips D. A. (1989). A chalcone and two related flavonoids released from alfalfa roots induce nod genes of Rhizobium meliloti. Plant Physiol. 91 842–847. 10.1104/pp.91.3.842 PubMed DOI PMC

Mazza P., Noens E. E., Schirner K., Grantcharova N., Mommaas A. M., Koerten H. K., et al. (2006). MreB of Streptomyces coelicolor is not essential for vegetative growth but is required for the integrity of aerial hyphae and spores. Mol. Microbiol. 60 838–852. 10.1111/j.1365-2958.2006.05134.x PubMed DOI

McBride M. J., Ensign J. C. (1987a). Effects of intracellular trehalose content on Streptomyces griseus spores. J. Bacteriol. 169 4995–5001. 10.1128/jb.169.11.4995-5001.1987 PubMed DOI PMC

McBride M. J., Ensign J. C. (1987b). Metabolism of endogenous trehalose by Streptomyces griseus spores and by spores or cells of other actinomycetes. J. Bacteriol. 169 5002–5007. 10.1128/jb.169.11.5002-5007.1987 PubMed DOI PMC

McBride M. J., Ensign J. C. (1990). Regulation of trehalose metabolism by Streptomyces griseus spores. J. Bacteriol. 172 3637–3643. 10.1128/jb.172.7.3637-3643.1990 PubMed DOI PMC

McBride M. J., Zusman D. R. (1989). Trehalose accumulation in vegetative cells and spores of Myxococcus xanthus. J. Bacteriol. 171 6383–6386. 10.1128/jb.171.11.6383-6386.1989 PubMed DOI PMC

Miguelez E. M., Martin C., Hardisson C., Manzanal M. B. (1993). Synchronous germination of Streptomyces antibioticus spores: tool for the analysis of hyphal growth in liquid cultures. FEMS Microbiol. Lett. 109 123–129. 10.1111/j.1574-6968.1993.tb06156.x PubMed DOI

Mikulik K., Bobek J., Bezouskova S., Benada O., Kofronova O. (2002). Expression of proteins and protein kinase activity during germination of aerial spores of Streptomyces granaticolor. Biochem. Biophys. Res. Commun. 299 335–342. 10.1016/S0006-291X(02)02606-2 PubMed DOI

Mikulik K., Bobek J., Zikova A., Smetakova M., Bezouskova S. (2011). Phosphorylation of ribosomal proteins influences subunit association and translation of poly (U) in Streptomyces coelicolor. Mol. Biosyst. 7 817–823. 10.1039/c0mb00174k PubMed DOI

Mikulik K., Janda I., Maskova H., Stastna J., Jiranova A. (1977). Macromolecular synthesis accompanying the transition from spores to vegetative forms of Streptomyces granaticolor. Folia Microbiol. 22 252–261. 10.1007/BF02877654 PubMed DOI

Mikulik K., Janda I., Weiser J., Stastna J., Jiranova A. (1984). RNA and ribosomal protein patterns during aerial spore germination in Streptomyces granaticolor. Eur. J. Biochem. 145 381–388. 10.1111/j.1432-1033.1984.tb08565.x PubMed DOI

Mikulik K., Paleckova P., Felsberg J., Bobek J., Zidkova J., Halada P. (2008). SsrA genes of streptomycetes and association of proteins to the tmRNA during development and cellular differentiation. Proteomics 8 1429–1441. 10.1002/pmic.200700560 PubMed DOI

Mukamolova G. V., Kaprelyants A. S., Young D. I., Young M., Kell D. B. (1998a). A bacterial cytokine. Proc. Natl. Acad. Sci. U.S.A. 95 8916–8921. 10.1073/pnas.95.15.8916 PubMed DOI PMC

Mukamolova G. V., Yanopolskaya N. D., Kell D. B., Kaprelyants A. S. (1998b). On resuscitation from the dormant state of Micrococcus luteus. Antonie Van Leeuwenhoek 73 237–243. 10.1023/A:1000881918216 PubMed DOI

Mukamolova G. V., Murzin A. G., Salina E. G., Demina G. R., Kell D. B., Kaprelyants A. S., et al. (2006). Muralytic activity of Micrococcus luteus Rpf and its relationship to physiological activity in promoting bacterial growth and resuscitation. Mol. Microbiol. 59 84–98. 10.1111/j.1365-2958.2005.04930.x PubMed DOI

Mukamolova G. V., Turapov O. A., Kazarian K., Telkov M., Kaprelyants A. S., Kell D. B., et al. (2002). The rpf gene of Micrococcus luteus encodes an essential secreted growth factor. Mol. Microbiol. 46 611–621. 10.1046/j.1365-2958.2002.03183.x PubMed DOI

Neiman A. M. (2005). Ascospore formation in the yeast Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 69 565–584. 10.1128/MMBR.69.4.565-584.2005 PubMed DOI PMC

Noens E. E., Mersinias V., Traag B. A., Smith C. P., Koerten H. K., van Wezel G. P. (2005). SsgA-like proteins determine the fate of peptidoglycan during sporulation of Streptomyces coelicolor. Mol. Microbiol. 58 929–944. 10.1111/j.1365-2958.2005.04883.x PubMed DOI

Noens E. E., Mersinias V., Willemse J., Traag B. A., Laing E., Chater K. F., et al. (2007). Loss of the controlled localization of growth stage-specific cell-wall synthesis pleiotropically affects developmental gene expression in an ssgA mutant of Streptomyces coelicolor. Mol. Microbiol. 64 1244–1259. 10.1111/j.1365-2958.2007.05732.x PubMed DOI

Nwaka S., Holzer H. (1998). Molecular biology of trehalose and the trehalases in the yeast Saccharomyces cerevisiae. Prog. Nucleic Acid Res. Mol. Biol. 58 197–237. 10.1016/S0079-6603(08)60037-9 PubMed DOI

Onaka H., Mori Y., Igarashi Y., Furumai T. (2011). Mycolic acid-containing bacteria induce natural-product biosynthesis in Streptomyces species. Appl. Environ. Microbiol. 77 400–406. 10.1128/AEM.01337-10 PubMed DOI PMC

Paget M. S., Chamberlin L., Atrih A., Foster S. J., Buttner M. J. (1999). Evidence that the extracytoplasmic function sigma factor sigmaE is required for normal cell wall structure in Streptomyces coelicolor A3(2). J. Bacteriol. 181 204–211. PubMed PMC

Paidhungat M., Setlow P. (2000). Role of ger proteins in nutrient and nonnutrient triggering of spore germination in Bacillus subtilis. J. Bacteriol. 182 2513–2519. 10.1128/JB.182.9.2513-2519.2000 PubMed DOI PMC

Paleckova P., Bobek J., Felsberg J., Mikulik K. (2006). Activity of translation system and abundance of tmRNA during development of Streptomyces aureofaciens producing tetracycline. Folia Microbiol. 51 517–524. 10.1007/BF02931615 PubMed DOI

Palleroni N. J. (1976). Chemotaxis in Actinoplanes. Arch. Microbiol. 110 13–18. 10.1007/BF00416963 PubMed DOI

Pammer M., Briza P., Ellinger A., Schuster T., Stucka R., Feldmann H., et al. (1992). DIT101 (CSD2 CAL1), a cell cycle-regulated yeast gene required for synthesis of chitin in cell walls and chitosan in spore walls. Yeast 8 1089–1099. 10.1002/yea.320081211 PubMed DOI

Paredes-Sabja D., Setlow P., Sarker M. R. (2011). Germination of spores of Bacillales and Clostridiales species: mechanisms and proteins involved. Trends Microbiol. 19 85–94. 10.1016/j.tim.2010.10.004 PubMed DOI

Petersen F., Zahner H., Metzger J. W., Freund S., Hummel R. P. (1993). Germicidin, an autoregulative germination inhibitor of Streptomyces viridochromogenes NRRL B-1551. J. Antibiot. 46 1126–1138. 10.7164/antibiotics.46.1126 PubMed DOI

Piette A., Derouaux A., Gerkens P., Noens E. E., Mazzucchelli G., Vion S., et al. (2005). From dormant to germinating spores of Streptomyces coelicolor A3(2): new perspectives from the crp null mutant. J. Proteome Res. 4 1699–1708. 10.1021/pr050155b PubMed DOI

Ranade N., Vining L. C. (1993). Accumulation of intracellular carbon reserves in relation to chloramphenicol biosynthesis by Streptomyces venezuelae. Can. J. Microbiol. 39 377–383. 10.1139/m93-055 PubMed DOI

Richards D. M., Hempel A. M., Flardh K., Buttner M. J., Howard M. (2012). Mechanistic basis of branch-site selection in filamentous bacteria. PLOS Comput. Biol. 8:e1002423. 10.1371/journal.pcbi.1002423 PubMed DOI PMC

Roth R., Sussman M. (1966). Trehalose synthesis in the cellular slime mold Dictyostelium discoideum. Biochim. Biophys. Acta 122 225–231. 10.1016/0926-6593(66)90064-6 PubMed DOI

Ruban-Osmialowska B., Jakimowicz D., Smulczyk-Krawczyszyn A., Chater K. F., Zakrzewska-Czerwinska J. (2006). Replisome localization in vegetative and aerial hyphae of Streptomyces coelicolor. J. Bacteriol. 188 7311–7316. 10.1128/JB.00940-06 PubMed DOI PMC

Rueda B., Miguelez E. M., Hardisson C., Manzanal M. B. (2001). Changes in glycogen and trehalose content of Streptomyces brasiliensis hyphae during growth in liquid cultures under sporulating and non-sporulating conditions. FEMS Microbiol. Lett. 194 181–185. 10.1111/j.1574-6968.2001.tb09466.x PubMed DOI

Ruggiero A., Tizzano B., Pedone E., Pedone C., Wilmanns M., Berisio R. (2009). Crystal structure of the resuscitation-promoting factor (DeltaDUF)RpfB from M. tuberculosis. J. Mol. Biol. 385 153–162. 10.1016/j.jmb.2008.10.042 PubMed DOI

Salas J. A., Guijarro J. A., Hardisson C. (1983). High calcium content in Streptomyces spores and its release as an early event during spore germination. J. Bacteriol. 155 1316–1323. PubMed PMC

Sanchez L., Brana A. F. (1996). Cell density influences antibiotic biosynthesis in Streptomyces clavuligerus. Microbiology 142(Pt 5) 1209–1220. 10.1099/13500872-142-5-1209 PubMed DOI

Sapir L., Harries D. (2011). Linking trehalose self-association with binary aqueous solution equation of state. J. Phys. Chem. B 115 624–634. 10.1021/jp109780n PubMed DOI

Setlow B., Atluri S., Kitchel R., Koziol-Dube K., Setlow P. (2006). Role of dipicolinic acid in resistance and stability of spores of Bacillus subtilis with or without DNA-protective alpha/beta-type small acid-soluble proteins. J. Bacteriol. 188 3740–3747. 10.1128/JB.00212-06 PubMed DOI PMC

Setlow P. (2003). Spore germination. Curr. Opin. Microbiol. 6 550–556. 10.1016/j.mib.2003.10.001 PubMed DOI

Setlow P. (2007). I will survive: DNA protection in bacterial spores. Trends Microbiol. 15 172–180. 10.1016/j.tim.2007.02.004 PubMed DOI

Sevcikova B., Kormanec J. (2003). The ssgB gene, encoding a member of the regulon of stress-response sigma factor sigmaH, is essential for aerial mycelium septation in Streptomyces coelicolor A3(2). Arch. Microbiol. 180 380–384. 10.1007/s00203-003-0603-y PubMed DOI

Sevcikova B., Rezuchova B., Homerova D., Kormanec J. (2010). The anti-anti-sigma factor BldG is involved in activation of the stress response sigma factor sigma(H) in Streptomyces coelicolor A3(2). J. Bacteriol. 192 5674–5681. 10.1128/JB.00828-10 PubMed DOI PMC

Sexton D. L., St-Onge R. J., Haiser H. J., Yousef M. R., Brady L., Gao C., et al. (2015). Resuscitation-promoting factors are cell wall-lytic enzymes with important roles in the germination and growth of Streptomyces coelicolor. J. Bacteriol. 197 848–860. 10.1128/JB.02464-14 PubMed DOI PMC

Shah I. M., Laaberki M. H., Popham D. L., Dworkin J. (2008). A eukaryotic-like Ser/Thr kinase signals bacteria to exit dormancy in response to peptidoglycan fragments. Cell 135 486–496. 10.1016/j.cell.2008.08.039 PubMed DOI PMC

Shleeva M. O., Trutneva K. A., Demina G. R., Zinin A. I., Sorokoumova G. M., Laptinskaya P. K., et al. (2017). Free trehalose accumulation in dormant Mycobacterium smegmatis cells and its breakdown in early resuscitation phase. Front. Microbiol. 8:524. 10.3389/fmicb.2017.00524 PubMed DOI PMC

Shu D., Chen L., Wang W., Yu Z., Ren C., Zhang W., et al. (2009). afsQ1-Q2-sigQ is a pleiotropic but conditionally required signal transduction system for both secondary metabolism and morphological development in Streptomyces coelicolor. Appl. Microbiol. Biotechnol. 81 1149–1160. 10.1007/s00253-008-1738-1 PubMed DOI

Sigle S., Ladwig N., Wohlleben W., Muth G. (2015). Synthesis of the spore envelope in the developmental life cycle of Streptomyces coelicolor. Int. J. Med. Microbiol. 305 183–189. 10.1016/j.ijmm.2014.12.014 PubMed DOI

Singer M. A., Lindquist S. (1998). Multiple effects of trehalose on protein folding in vitro and in vivo. Mol. Cell 1 639–648. 10.1016/S1097-2765(00)80064-7 PubMed DOI

Sola-Penna M., Meyer-Fernandes J. R. (1998). Stabilization against thermal inactivation promoted by sugars on enzyme structure and function: why is trehalose more effective than other sugars? Arch. Biochem. Biophys. 360 10–14. 10.1006/abbi.1998.0906 PubMed DOI

Song L., Barona-Gomez F., Corre C., Xiang L., Udwary D. W., Austin M. B., et al. (2006). Type III polyketide synthase beta-ketoacyl-ACP starter unit and ethylmalonyl-CoA extender unit selectivity discovered by Streptomyces coelicolor genome mining. J. Am. Chem. Soc. 128 14754–14755. 10.1021/ja065247w PubMed DOI PMC

Stastna J. (1977). A method of rapid wetting and synchronous germination of streptomycete spores. Folia Microbiol. 22 137–138. 10.1007/BF02881639 PubMed DOI

St-Onge R. J., Haiser H. J., Yousef M. R., Sherwood E., Tschowri N., Al-Bassam M., et al. (2015). Nucleotide second messenger-mediated regulation of a muralytic enzyme in Streptomyces. Mol. Microbiol. 96 779–795. 10.1111/mmi.12971 PubMed DOI

Strakova E., Bobek J., Zikova A., Rehulka P., Benada O., Rehulkova H., et al. (2013a). Systems insight into the spore germination of Streptomyces coelicolor. J. Proteome Res. 12 525–536. 10.1021/pr300980v PubMed DOI

Strakova E., Bobek J., Zikova A., Vohradsky J. (2013b). Global features of gene expression on the proteome and transcriptome levels in S. coelicolor during germination. PLOS ONE 8:e72842. 10.1371/journal.pone.0072842 PubMed DOI PMC

Strakova E., Zikova A., Vohradsky J. (2014). Inference of sigma factor controlled networks by using numerical modeling applied to microarray time series data of the germinating prokaryote. Nucleic Acids Res. 42 748–763. 10.1093/nar/gkt917 PubMed DOI PMC

Sturm A., Dworkin J. (2015). Phenotypic diversity as a mechanism to exit cellular dormancy. Curr. Biol. 25 2272–2277. 10.1016/j.cub.2015.07.018 PubMed DOI PMC

Sussman A. S. (1961). The role of trehalose in the activation of dormant ascospores of neurospora. Q. Rev. Biol. 36 109–116. 10.1086/403332 PubMed DOI

Sussman A. S., Lingappa B. T. (1959). Role of trehalose in ascospores of neurospora tetrasperma. Science 130:1343. 10.1126/science.130.3385.1343 PubMed DOI

Susstrunk U., Pidoux J., Taubert S., Ullmann A., Thompson C. J. (1998). Pleiotropic effects of cAMP on germination, antibiotic biosynthesis and morphological development in Streptomyces coelicolor. Mol. Microbiol. 30 33–46. 10.1046/j.1365-2958.1998.01033.x PubMed DOI

Telkov M. V., Demina G. R., Voloshin S. A., Salina E. G., Dudik T. V., Stekhanova T. N., et al. (2006). Proteins of the Rpf (resuscitation promoting factor) family are peptidoglycan hydrolases. Biochemistry 71 414–422. 10.1134/S0006297906040092 PubMed DOI

Thevelein J. M. (1984). Regulation of trehalose mobilization in fungi. Microbiol. Rev. 48 42–59. PubMed PMC

Thomas K. J., III, Rice C. V. (2014). Revised model of calcium and magnesium binding to the bacterial cell wall. Biometals 27 1361–1370. 10.1007/s10534-014-9797-5 PubMed DOI PMC

Traag B. A., van Wezel G. P. (2008). The SsgA-like proteins in actinomycetes: small proteins up to a big task. Antonie Van Leeuwenhoek 94 85–97. 10.1007/s10482-008-9225-3 PubMed DOI PMC

Traxler M. F., Watrous J. D., Alexandrov T., Dorrestein P. C., Kolter R. (2013). Interspecies interactions stimulate diversification of the Streptomyces coelicolor secreted metabolome. mBio 4:e00459-13. 10.1128/mBio.00459-13 PubMed DOI PMC

Trevelyan W. E., Harrison J. S. (1956). Studies on yeast metabolism. 5. The trehalose content of baker’s yeast during anaerobic fermentation. Biochem. J. 62 177–183. 10.1042/bj0620177b PubMed DOI PMC

Tschowri N., Schumacher M. A., Schlimpert S., Chinnam N. B., Findlay K. C., Brennan R. G., et al. (2014). Tetrameric c-di-GMP mediates effective transcription factor dimerization to control Streptomyces development. Cell 158 1136–1147. 10.1016/j.cell.2014.07.022 PubMed DOI PMC

van Vliet S. (2015). Bacterial dormancy: how to decide when to wake up. Curr. Biol. 25 R753–R755. 10.1016/j.cub.2015.07.039 PubMed DOI

van Wezel G. P., van der Meulen J., Kawamoto S., Luiten R. G., Koerten H. K., Kraal B. (2000). ssgA is essential for sporulation of Streptomyces coelicolor A3(2) and affects hyphal development by stimulating septum formation. J. Bacteriol. 182 5653–5662. 10.1128/JB.182.20.5653-5662.2000 PubMed DOI PMC

Viollier P. H., Weihofen A., Folcher M., Thompson C. J. (2003). Post-transcriptional regulation of the Streptomyces coelicolor stress responsive sigma factor, SigH, involves translational control, proteolytic processing, and an anti-sigma factor homolog. J. Mol. Biol. 325 637–649. 10.1016/S0022-2836(02)01280-9 PubMed DOI

Wang L., Yu Y., He X., Zhou X., Deng Z., Chater K. F., et al. (2007). Role of an FtsK-like protein in genetic stability in Streptomyces coelicolor A3(2). J. Bacteriol. 189 2310–2318. 10.1128/JB.01660-06 PubMed DOI PMC

Wang S. L., Fan K. Q., Yang X., Lin Z. X., Xu X. P., Yang K. Q. (2008). CabC, an EF-hand calcium-binding protein, is involved in Ca2+-mediated regulation of spore germination and aerial hypha formation in Streptomyces coelicolor. J. Bacteriol. 190 4061–4068. 10.1128/JB.01954-07 PubMed DOI PMC

Wiemken A. (1990). Trehalose in yeast, stress protectant rather than reserve carbohydrate. Antonie Van Leeuwenhoek 58 209–217. 10.1007/BF00548935 PubMed DOI

Wildermuth H., Wehrli E., Horne R. W. (1971). The surface structure of spores and aerial mycelium in Streptomyces coelicolor. J. Ultrastruct. Res. 35 168–180. 10.1016/S0022-5320(71)80149-1 PubMed DOI

Willemse J., Borst J. W., de Waal E., Bisseling T., van Wezel G. P. (2011). Positive control of cell division: FtsZ is recruited by SsgB during sporulation of Streptomyces. Genes Dev. 25 89–99. 10.1101/gad.600211 PubMed DOI PMC

Wolanski M., Wali R., Tilley E., Jakimowicz D., Zakrzewska-Czerwinska J., Herron P. (2011). Replisome trafficking in growing vegetative hyphae of Streptomyces coelicolor A3(2). J. Bacteriol. 193 1273–1275. 10.1128/JB.01326-10 PubMed DOI PMC

Wyatt T. T., Wosten H. A., Dijksterhuis J. (2013). Fungal spores for dispersion in space and time. Adv. Appl. Microbiol. 85 43–91. 10.1016/B978-0-12-407672-3.00002-2 PubMed DOI

Xu Y., Vetsigian K. (2017). Phenotypic variability and community interactions of germinating Streptomyces spores. Sci. Rep. 7 699. 10.1038/s41598-017-00792-7 PubMed DOI PMC

Yoshinaga K., Yoshioka H., Kurosaki H., Hirasawa M., Uritani M., Hasegawa K. (1997). Protection by trehalose of DNA from radiation damage. Biosci. Biotechnol. Biochem. 61 160–161. 10.1271/bbb.61.160 PubMed DOI

Zdanowski K., Doughty P., Jakimowicz P., O’Hara L., Buttner M. J., Paget M. S., et al. (2006). Assignment of the zinc ligands in RsrA, a redox-sensing ZAS protein from Streptomyces coelicolor. Biochemistry 45 8294–8300. 10.1021/bi060711v PubMed DOI

Zhao B., Guengerich F. P., Bellamine A., Lamb D. C., Izumikawa M., Lei L., et al. (2005). Binding of two flaviolin substrate molecules, oxidative coupling, and crystal structure of Streptomyces coelicolor A3(2) cytochrome P450 158A2. J. Biol. Chem. 280 11599–11607. 10.1074/jbc.M410933200 PubMed DOI

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Secondary Metabolites Produced during the Germination of Streptomyces coelicolor