Germination and Growth Analysis of Streptomyces lividans at the Single-Cell Level Under Varying Medium Compositions

Koepff J, Sachs CC, Wiechert W, Kohlheyer D, Noeh K, Oldiges M, Grünberger A (2018)
FRONTIERS IN MICROBIOLOGY 9: 2680.

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Quantitative single-cell cultivation has provided fundamental contributions to our understanding of heterogeneity among industrially used microorganisms. Filamentous growing Streptomyces species are emerging platform organisms for industrial production processes, but their exploitation is still limited due to often reported high batch-to-batch variations and unexpected growth and production differences. Population heterogeneity is suspected to be one responsible factor, which is so far not systematically investigated at the single-cell level. Novel microfluidic single-cell cultivation devices offer promising solutions to investigate these phenomena. In this study, we investigated the germination and growth behavior of Streptomyces lividans TK24 under varying medium compositions on different complexity levels (i.e., mycelial growth, hyphal growth and tip elongation) on single-cell level. Our analysis reveals a remarkable stability within growth and germination of spores and early mycelium development when exposed to constant and defined environments. We show that spores undergo long metabolic adaptation processes of up to > 30 h to adjust to new medium conditions, rather than using a "persister" strategy as a possibility to cope with rapidly changing environments. Due to this uniform behavior, we conclude that S. lividans can be cultivated quite robustly under constant environmental conditions as provided by microfluidic cultivation approaches. Failure and non-reproducible cultivations are thus most likely to be found in less controllable larger-scale cultivation workflows and as a result of environmental gradients within large-scale cultivations.
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FRONTIERS IN MICROBIOLOGY
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9
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2680
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Article Processing Charge funded by the Deutsche Forschungsgemeinschaft and the Open Access Publication Fund of Bielefeld University.
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Koepff J, Sachs CC, Wiechert W, et al. Germination and Growth Analysis of Streptomyces lividans at the Single-Cell Level Under Varying Medium Compositions. FRONTIERS IN MICROBIOLOGY. 2018;9: 2680.
Koepff, J., Sachs, C. C., Wiechert, W., Kohlheyer, D., Noeh, K., Oldiges, M., & Grünberger, A. (2018). Germination and Growth Analysis of Streptomyces lividans at the Single-Cell Level Under Varying Medium Compositions. FRONTIERS IN MICROBIOLOGY, 9, 2680. doi:10.3389/fmicb.2018.02680
Koepff, J., Sachs, C. C., Wiechert, W., Kohlheyer, D., Noeh, K., Oldiges, M., and Grünberger, A. (2018). Germination and Growth Analysis of Streptomyces lividans at the Single-Cell Level Under Varying Medium Compositions. FRONTIERS IN MICROBIOLOGY 9:2680.
Koepff, J., et al., 2018. Germination and Growth Analysis of Streptomyces lividans at the Single-Cell Level Under Varying Medium Compositions. FRONTIERS IN MICROBIOLOGY, 9: 2680.
J. Koepff, et al., “Germination and Growth Analysis of Streptomyces lividans at the Single-Cell Level Under Varying Medium Compositions”, FRONTIERS IN MICROBIOLOGY, vol. 9, 2018, : 2680.
Koepff, J., Sachs, C.C., Wiechert, W., Kohlheyer, D., Noeh, K., Oldiges, M., Grünberger, A.: Germination and Growth Analysis of Streptomyces lividans at the Single-Cell Level Under Varying Medium Compositions. FRONTIERS IN MICROBIOLOGY. 9, : 2680 (2018).
Koepff, Joachim, Sachs, Christian Carsten, Wiechert, Wolfgang, Kohlheyer, Dietrich, Noeh, Katharina, Oldiges, Marco, and Grünberger, Alexander. “Germination and Growth Analysis of Streptomyces lividans at the Single-Cell Level Under Varying Medium Compositions”. FRONTIERS IN MICROBIOLOGY 9 (2018): 2680.
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Characterization of Sigma Factor Genes in Streptomyces lividans TK24 Using a Genomic Library-Based Approach for Multiple Gene Deletions.
Rebets Y, Tsolis KC, Guðmundsdóttir EE, Koepff J, Wawiernia B, Busche T, Bleidt A, Horbal L, Myronovskyi M, Ahmed Y, Wiechert W, Rückert C, Hamed MB, Bilyk B, Anné J, Friðjónsson Ó, Kalinowski J, Oldiges M, Economou A, Luzhetskyy A., Front Microbiol 9(), 2018
PMID: 30619125

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PMID: 25680930
The Taming of the Shrew--Controlling the Morphology of Filamentous Eukaryotic and Prokaryotic Microorganisms.
Walisko R, Moench-Tegeder J, Blotenberg J, Wucherpfennig T, Krull R., Adv. Biochem. Eng. Biotechnol. 149(), 2015
PMID: 25796624
Development of a minimal defined medium for recombinant human interleukin-3 production by Streptomyces lividans 66.
Nowruzi K, Elkamel A, Scharer JM, Cossar D, Moo-Young M., Biotechnol. Bioeng. 99(1), 2008
PMID: 17615562
Fast and reliable strain characterization of Streptomyces lividans through micro-scale cultivation.
Koepff J, Keller M, Tsolis KC, Busche T, Ruckert C, Hamed MB, Anne J, Kalinowski J, Wiechert W, Economou A, Oldiges M., Biotechnol. Bioeng. 114(9), 2017
PMID: 28436005
Unlocking Streptomyces spp. for use as sustainable industrial production platforms by morphological engineering.
van Wezel GP, Krabben P, Traag BA, Keijser BJ, Kerste R, Vijgenboom E, Heijnen JJ, Kraal B., Appl. Environ. Microbiol. 72(8), 2006
PMID: 16885277
Beyond growth rate 0.6: What drives Corynebacterium glutamicum to higher growth rates in defined medium.
Unthan S, Grunberger A, van Ooyen J, Gatgens J, Heinrich J, Paczia N, Wiechert W, Kohlheyer D, Noack S., Biotechnol. Bioeng. 111(2), 2013
PMID: 23996851
Spatiotemporal microbial single-cell analysis using a high-throughput microfluidics cultivation platform.
Grunberger A, Probst C, Helfrich S, Nanda A, Stute B, Wiechert W, von Lieres E, Noh K, Frunzke J, Kohlheyer D., Cytometry A 87(12), 2015
PMID: 26348020
Bioactive microbial metabolites.
Berdy J., J. Antibiot. 58(1), 2005
PMID: 15813176
Fungal mycelia show lag time before re-growth on endogenous carbon.
Pollack JK, Li ZJ, Marten MR., Biotechnol. Bioeng. 100(3), 2008
PMID: 18183629
Dynamic localization of Tat protein transport machinery components in Streptomyces coelicolor.
Willemse J, Ruban-Osmialowska B, Widdick D, Celler K, Hutchings MI, van Wezel GP, Palmer T., J. Bacteriol. 194(22), 2012
PMID: 23002216
Mathematical model for apical growth, septation, and branching of mycelial microorganisms.
Yang H, King R, Reichl U, Gilles ED., Biotechnol. Bioeng. 39(1), 1992
PMID: 18600886
Protein Secretion in Gram-Positive Bacteria: From Multiple Pathways to Biotechnology.
Anne J, Economou A, Bernaerts K., Curr. Top. Microbiol. Immunol. 404(), 2017
PMID: 27885530
Morphogenesis of Streptomyces in submerged cultures.
van Dissel D, Claessen D, van Wezel GP., Adv. Appl. Microbiol. 89(), 2014
PMID: 25131399
Microfluidic picoliter bioreactor for microbial single-cell analysis: fabrication, system setup, and operation.
Gruenberger A, Probst C, Heyer A, Wiechert W, Frunzke J, Kohlheyer D., J Vis Exp (82), 2013
PMID: 24336165
Bet-hedging during bacterial diauxic shift.
Solopova A, van Gestel J, Weissing FJ, Bachmann H, Teusink B, Kok J, Kuipers OP., Proc. Natl. Acad. Sci. U.S.A. 111(20), 2014
PMID: 24799698
Miniaturized and automated adaptive laboratory evolution: Evolving Corynebacterium glutamicum towards an improved d-xylose utilization.
Radek A, Tenhaef N, Muller MF, Brusseler C, Wiechert W, Marienhagen J, Polen T, Noack S., Bioresour. Technol. 245(Pt B), 2017
PMID: 28552568
Recent advances in understanding Streptomyces.
Chater KF., F1000Res 5(), 2016
PMID: 27990276
A novel locus for mycelial aggregation forms a gateway to improved Streptomyces cell factories.
van Dissel D, Claessen D, Roth M, van Wezel GP., Microb. Cell Fact. 14(), 2015
PMID: 25889360
Amino acid uptake profiling of wild type and recombinant Streptomyces lividans TK24 batch fermentations.
D'Huys PJ, Lule I, Van Hove S, Vercammen D, Wouters C, Bernaerts K, Anne J, Van Impe JF., J. Biotechnol. 152(4), 2010
PMID: 20797416
On-line study of fungal morphology during submerged growth in a small flow-through cell.
Spohr A, Dam-Mikkelsen C, Carlsen M, Nielsen J, Villadsen J., Biotechnol. Bioeng. 58(5), 1998
PMID: 10099291
Antitumor compounds from marine actinomycetes.
Olano C, Mendez C, Salas JA., Mar Drugs 7(2), 2009
PMID: 19597582
Formation, properties, and germination of actinomycete spores.
Ensign JC., Annu. Rev. Microbiol. 32(), 1978
PMID: 360964
Forty years of genetics with Streptomyces: from in vivo through in vitro to in silico.
Hopwood DA., Microbiology (Reading, Engl.) 145 ( Pt 9)(), 1999
PMID: 10517572
Bacterial solutions to multicellularity: a tale of biofilms, filaments and fruiting bodies.
Claessen D, Rozen DE, Kuipers OP, Sogaard-Andersen L, van Wezel GP., Nat. Rev. Microbiol. 12(2), 2014
PMID: 24384602
Living with heterogeneities in bioreactors: understanding the effects of environmental gradients on cells.
Lara AR, Galindo E, Ramirez OT, Palomares LA., Mol. Biotechnol. 34(3), 2006
PMID: 17284782
Engineering E. coli for large-scale production - Strategies considering ATP expenses and transcriptional responses.
Loffler M, Simen JD, Jager G, Schaferhoff K, Freund A, Takors R., Metab. Eng. 38(), 2016
PMID: 27378496
Aggregation of germlings is a major contributing factor towards mycelial heterogeneity of Streptomyces.
Zacchetti B, Willemse J, Recter B, van Dissel D, van Wezel GP, Wosten HA, Claessen D., Sci Rep 6(), 2016
PMID: 27244565
Homogenizing bacterial cell factories: Analysis and engineering of phenotypic heterogeneity.
Binder D, Drepper T, Jaeger KE, Delvigne F, Wiechert W, Kohlheyer D, Grunberger A., Metab. Eng. 42(), 2017
PMID: 28645641
New approaches to achieve high level enzyme production in Streptomyces lividans.
Sevillano L, Vijgenboom E, van Wezel GP, Diaz M, Santamaria RI., Microb. Cell Fact. 15(), 2016
PMID: 26846788
The genome sequence of Streptomyces lividans 66 reveals a novel tRNA-dependent peptide biosynthetic system within a metal-related genomic island.
Cruz-Morales P, Vijgenboom E, Iruegas-Bocardo F, Girard G, Yanez-Guerra LA, Ramos-Aboites HE, Pernodet JL, Anne J, van Wezel GP, Barona-Gomez F., Genome Biol Evol 5(6), 2013
PMID: 23709624
Metabolic profile of 1,5-diaminopentane producing Corynebacterium glutamicum under scale-down conditions: Blueprint for robustness to bioreactor inhomogeneities.
Limberg MH, Schulte J, Aryani T, Mahr R, Baumgart M, Bott M, Wiechert W, Oldiges M., Biotechnol. Bioeng. 114(3), 2016
PMID: 27641904
Phenotypic bistability in Escherichia coli's central carbon metabolism.
Kotte O, Volkmer B, Radzikowski JL, Heinemann M., Mol. Syst. Biol. 10(), 2014
PMID: 24987115
Time-lapse microscopy of Streptomyces coelicolor growth and sporulation.
Jyothikumar V, Tilley EJ, Wali R, Herron PR., Appl. Environ. Microbiol. 74(21), 2008
PMID: 18791015
Complete genome sequence of Streptomyces lividans TK24.
Ruckert C, Albersmeier A, Busche T, Jaenicke S, Winkler A, Friðjonsson OH, Hreggviðsson GO, Lambert C, Badcock D, Bernaerts K, Anne J, Economou A, Kalinowski J., J. Biotechnol. 199(), 2015
PMID: 25680930
The Taming of the Shrew--Controlling the Morphology of Filamentous Eukaryotic and Prokaryotic Microorganisms.
Walisko R, Moench-Tegeder J, Blotenberg J, Wucherpfennig T, Krull R., Adv. Biochem. Eng. Biotechnol. 149(), 2015
PMID: 25796624
Development of a minimal defined medium for recombinant human interleukin-3 production by Streptomyces lividans 66.
Nowruzi K, Elkamel A, Scharer JM, Cossar D, Moo-Young M., Biotechnol. Bioeng. 99(1), 2008
PMID: 17615562
Fast and reliable strain characterization of Streptomyces lividans through micro-scale cultivation.
Koepff J, Keller M, Tsolis KC, Busche T, Ruckert C, Hamed MB, Anne J, Kalinowski J, Wiechert W, Economou A, Oldiges M., Biotechnol. Bioeng. 114(9), 2017
PMID: 28436005
Unlocking Streptomyces spp. for use as sustainable industrial production platforms by morphological engineering.
van Wezel GP, Krabben P, Traag BA, Keijser BJ, Kerste R, Vijgenboom E, Heijnen JJ, Kraal B., Appl. Environ. Microbiol. 72(8), 2006
PMID: 16885277

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