BACKGROUND: Bacterial spore germination is a developmental process during which all required metabolic pathways are restored to transfer cells from their dormant state into vegetative growth. Streptomyces are soil dwelling filamentous bacteria with complex life cycle, studied mostly for they ability to synthesize secondary metabolites including antibiotics. RESULTS: Here, we present a systematic approach that analyzes gene expression data obtained from 13 time points taken over 5.5 h of Streptomyces germination. Genes whose expression was significantly enhanced/diminished during the time-course were identified, and classified to metabolic and regulatory pathways. The classification into metabolic pathways revealed timing of the activation of specific pathways during the course of germination. The analysis also identified remarkable changes in the expression of specific sigma factors over the course of germination. Based on our knowledge of the targets of these factors, we speculate on their possible roles during germination. Among the factors whose expression was enhanced during the initial part of germination, SigE is though to manage cell wall reconstruction, SigR controls protein re-aggregation, and others (SigH, SigB, SigI, SigJ) control osmotic and oxidative stress responses. CONCLUSIONS: From the results, we conclude that most of the metabolic pathway mRNAs required for the initial phases of germination were synthesized during the sporulation process and stably conserved in the spore. After rehydration in growth medium, the stored mRNAs are being degraded and resynthesized during first hour. From the analysis of sigma factors we conclude that conditions favoring germination evoke stress-like cell responses.

Institute of Microbiology Academy of Sciences of the Czech Republic Laboratory of Bioinformatics Vídeňská 1083 142 20 Prague 4 Czech Republic

Zobrazit více v PubMed

Hopwood DA. How do antibiotic-producing bacteria ensure their self-resistance before antibiotic biosynthesis incapacitates them? Mol Microbiol. 2007;63(4):937–940. doi: 10.1111/j.1365-2958.2006.05584.x. PubMed DOI

Kelemen GH, Buttner MJ. Initiation of aerial mycelium formation in Streptomyces. Curr Opin Microbiol. 1998;1(6):656–662. doi: 10.1016/S1369-5274(98)80111-2. PubMed DOI

Claessen D, de Jong W, Dijkhuizen L, Wosten HA. Regulation of Streptomyces development: reach for the sky! Trends Microbiol. 2006;14(7):313–319. doi: 10.1016/j.tim.2006.05.008. PubMed DOI

Yague P, Lopez-Garcia MT, Rioseras B, Sanchez J, Manteca A. Pre-sporulation stages of Streptomyces differentiation: state-of-the-art and future perspectives. FEMS Microbiol Lett. 2013;342(2):79–88. doi: 10.1111/1574-6968.12128. PubMed DOI PMC

Hodgson DA. Differentiation in actinomycetes. In: Mohan S, editor. Prokaryotic Structure and Function: A New Perspective. Cambridge: Cambridge University Press; 1992. pp. 407–440.

Stewart GS, Johnstone K, Hagelberg E, Ellar DJ. Commitment of bacterial spores to germinate. A measure of the trigger reaction. Biochem J. 1981;198(1):101–106. PubMed PMC

Miguelez EM, Martin C, Hardisson C, Manzanal MB. Synchronous germination of Streptomyces antibioticus spores: tool for the analysis of hyphal growth in liquid cultures. FEMS Microbiol Lett. 1993;109(2–3):123–129. doi: 10.1111/j.1574-6968.1993.tb06156.x. PubMed DOI

Mikulik K, Janda I, Maskova H, Stastna J, Jiranova A. Macromolecular synthesis accompanying the transition from spores to vegetative forms of Streptomyces granaticolor. Folia Microbiol (Praha) 1977;22(4):252–261. doi: 10.1007/BF02877654. PubMed DOI

Stastna J. A method of rapid wetting and synchronous germination of streptomycete spores. Folia Microbiol (Praha) 1977;22(2):137–138. doi: 10.1007/BF02881639. PubMed DOI

Haiser HJ, Yousef MR, Elliot MA. Cell wall hydrolases affect germination, vegetative growth, and sporulation in Streptomyces coelicolor. J Bacteriol. 2009;191(21):6501–6512. doi: 10.1128/JB.00767-09. PubMed DOI PMC

Mikulik K, Janda I, Weiser J, Stastna J, Jiranova A. RNA and ribosomal protein patterns during aerial spore germination in Streptomyces granaticolor. Eur J Biochem. 1984;145(2):381–388. doi: 10.1111/j.1432-1033.1984.tb08565.x. PubMed DOI

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

Hardisson C, Manzanal MB, Salas JA, Suarez JE. Fine structure, physiology and biochemistry of arthrospore germination in Streptomyces antibioticus. J Gen Microbiol. 1978;105(2):203–214. doi: 10.1099/00221287-105-2-203. PubMed DOI

Vohradsky J, Branny P, Thompson CJ. Comparative analysis of gene expression on mRNA and protein level during development of Streptomyces cultures by using singular value decomposition. Proteomics. 2007;7(21):3853–3866. doi: 10.1002/pmic.200700005. PubMed DOI

Vohradsky J, Li X, Dale G, Folcher M, Nguyen L, Viollier PH, Thompson CJ. Developmental control of stress stimulons in streptomyces coelicolor revealed by statistical analyses of global gene expression patterns. J Bacteriol. 2000;182(17):4979–4986. doi: 10.1128/JB.182.17.4979-4986.2000. PubMed DOI PMC

Laing E, Mersinias V, Smith CP, Hubbard SJ. Analysis of gene expression in operons of Streptomyces coelicolor. Genome Biol. 2006;7(6):R46. doi: 10.1186/gb-2006-7-6-r46. PubMed DOI PMC

Vohradsky J, Thompson C. Systems level analysis of protein synthesis patterns associated with bacterial growth and metabolic transitions. Proteomics. 2006;6(7):785–793. doi: 10.1002/pmic.200500206. PubMed DOI

Basler M, Linhartova I, Halada P, Novotna J, Bezouskova S, Osicka R, Weiser J, Vohradsky J, Sebo P. The iron-regulated transcriptome and proteome of Neisseria meningitidis serogroup C. Proteomics. 2006;6(23):6194–6206. doi: 10.1002/pmic.200600312. PubMed DOI

Jayapal KP, Philp RJ, Kok YJ, Yap MG, Sherman DH, Griffin TJ, Hu WS. Uncovering genes with divergent mRNA-protein dynamics in Streptomyces coelicolor. PLoS One. 2008;3(5):e2097. doi: 10.1371/journal.pone.0002097. PubMed DOI PMC

Strakova E, Bobek J, Zikova A, Vohradsky J. Global Features of Gene Expression on the Proteome and Transcriptome Levels in S-coelicolor during Germination. Plos One. 2013;8(9):e72842. doi: 10.1371/journal.pone.0072842. PubMed DOI PMC

Strakova E, Zikova A, Vohradsky J. Inference of sigma factor controlled networks by using numerical modeling applied to microarray time series data of the germinating prokaryote. Nucleic Acids Res. 2014;42(2):748–763. doi: 10.1093/nar/gkt917. PubMed DOI PMC

Kanehisa M, Goto S. KEGG: kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000;28(1):27–30. doi: 10.1093/nar/28.1.27. PubMed DOI PMC

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

Bobek J, Halada P, Angelis J, Vohradsky J, Mikulík K: Activation and expression of proteins during synchronous germination of aerial spores of Streptomyces granaticolor.Proteomics In press PubMed

Economou A. Bacterial preprotein translocase: mechanism and conformational dynamics of a processive enzyme. Mol Microbiol. 1998;27(3):511–518. doi: 10.1046/j.1365-2958.1998.00713.x. PubMed DOI

Herrmann KM, Weaver LM. The Shikimate Pathway. Annu Rev Plant Physiol Plant Mol Biol. 1999;50:473–503. doi: 10.1146/annurev.arplant.50.1.473. PubMed DOI

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

Takano H, Asker D, Beppu T, Ueda K. Genetic control for light-induced carotenoid production in non-phototrophic bacteria. J Ind Microbiol Biotechnol. 2006;33(2):88–93. doi: 10.1007/s10295-005-0005-z. PubMed DOI

Armstrong GA. Eubacteria show their true colors: genetics of carotenoid pigment biosynthesis from microbes to plants. J Bacteriol. 1994;176(16):4795–4802. PubMed PMC

Hong HJ, Paget MS, Buttner MJ. 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. 2002;44(5):1199–1211. doi: 10.1046/j.1365-2958.2002.02960.x. PubMed DOI

Paget MS, Chamberlin L, Atrih A, Foster SJ, Buttner MJ. Evidence that the extracytoplasmic function sigma factor sigmaE is required for normal cell wall structure in Streptomyces coelicolor A3(2) J Bacteriol. 1999;181(1):204–211. PubMed PMC

Paget MS, Leibovitz E, Buttner MJ. A putative two-component signal transduction system regulates sigmaE, a sigma factor required for normal cell wall integrity in Streptomyces coelicolor A3(2) Mol Microbiol. 1999;33(1):97–107. doi: 10.1046/j.1365-2958.1999.01452.x. PubMed DOI

Bobek J, Halada P, Angelis J, Vohradsky J, Mikulik K. Activation and expression of proteins during synchronous germination of aerial spores of Streptomyces granaticolor. Proteomics. 2004;4(12):3864–3880. doi: 10.1002/pmic.200400818. PubMed DOI

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

Zdanowski K, Doughty P, Jakimowicz P, O'Hara L, Buttner MJ, Paget MS, Kleanthous C. Assignment of the zinc ligands in RsrA, a redox-sensing ZAS protein from Streptomyces coelicolor. Biochemistry. 2006;45(27):8294–8300. doi: 10.1021/bi060711v. PubMed DOI

Shu D, Chen L, Wang W, Yu Z, Ren C, Zhang W, Yang S, Lu Y, Jiang W. 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. 2009;81(6):1149–1160. doi: 10.1007/s00253-008-1738-1. PubMed DOI

Kelemen GH, Viollier PH, Tenor J, Marri L, Buttner MJ, Thompson CJ. A connection between stress and development in the multicellular prokaryote Streptomyces coelicolor A3(2) Mol Microbiol. 2001;40(4):804–814. doi: 10.1046/j.1365-2958.2001.02417.x. PubMed DOI

Kormanec J, Sevcikova B, Halgasova N, Knirschova R, Rezuchova B. Identification and transcriptional characterization of the gene encoding the stress-response sigma factor sigma(H) in streptomyces coelicolor A3(2) FEMS Microbiol Lett. 2000;189(1):31–38. PubMed

Sevcikova B, Benada O, Kofronova O, Kormanec J. Stress-response sigma factor sigma(H) is essential for morphological differentiation of Streptomyces coelicolor A3(2) Arch Microbiol. 2001;177(1):98–106. doi: 10.1007/s00203-001-0367-1. PubMed DOI

Viollier PH, Weihofen A, Folcher M, Thompson CJ. 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. 2003;325(4):637–649. doi: 10.1016/S0022-2836(02)01280-9. PubMed DOI

Sevcikova B, Rezuchova B, Homerova D, Kormanec J. 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. 2010;192(21):5674–5681. doi: 10.1128/JB.00828-10. PubMed DOI PMC

Karoonuthaisiri N, Weaver D, Huang J, Cohen SN, Kao CM. Regional organization of gene expression in Streptomyces coelicolor. Gene. 2005;353(1):53–66. doi: 10.1016/j.gene.2005.03.042. PubMed DOI

Fernandez Martinez L, Bishop A, Parkes L, Del Sol R, Salerno P, Sevcikova B, Mazurakova V, Kormanec J, Dyson P. Osmoregulation in Streptomyces coelicolor: modulation of SigB activity by OsaC. Mol Microbiol. 2009;71(5):1250–1262. doi: 10.1111/j.1365-2958.2009.06599.x. PubMed DOI

Krasny L, Tiserova H, Jonak J, Rejman D, Sanderova H. The identity of the transcription +1 position is crucial for changes in gene expression in response to amino acid starvation in Bacillus subtilis. Mol Microbiol. 2008;69(1):42–54. doi: 10.1111/j.1365-2958.2008.06256.x. PubMed DOI

Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002;30(1):207–210. doi: 10.1093/nar/30.1.207. PubMed DOI PMC

Polyenic Antibiotics and Other Antifungal Compounds Produced by Hemolytic Streptomyces Species

6S-Like scr3559 RNA Affects Development and Antibiotic Production in Streptomyces coelicolor

DNA mapping and kinetic modeling of the HrdB regulon in Streptomyces coelicolor

Secondary Metabolites Produced during the Germination of Streptomyces coelicolor

A Waking Review: Old and Novel Insights into the Spore Germination in Streptomyces

RNase III-Binding-mRNAs Revealed Novel Complementary Transcripts in Streptomyces