Technical bias of microcultivation environments on single cell physiology

Dusny C, Grünberger A, Probst C, Wiechert W, Kohlheyer D, Schmid A (2015)
Lab on a chip 15(8): 1822-1834.

Download
Es wurde kein Volltext hochgeladen. Nur Publikationsnachweis!
Zeitschriftenaufsatz | Veröffentlicht | Englisch
Autor
; ; ; ; ;
Abstract / Bemerkung
Microscale cultivation systems are important tools to elucidate cellular dynamics beyond the population average and understand the functional architecture of single cells. However, there is scant knowledge about the bias of different microcultivation technologies on cellular functions. We therefore performed a systematic cross-platform comparison of three different microscale cultivation systems commonly harnessed in single-cell analysis: microfluidic non-contact cell traps driven by negative dielectrophoresis, microfluidic monolayer growth chambers, and semi-solid agarose pads. We assessed the specific single-cell growth rates, division rates and morphological characteristics of single Corynebacterium glutamicum cells and microcolonies as a bacterial model organism with medical and biotechnological relevance under standardized growth conditions. Strikingly, the specific single-cell and microcolony growth rates, μmax, were robust and conserved for several cell generations with all three microcultivation technologies, whereas the division rates of cells grown on agarose pads deviated by up to 50% from those of cells cultivated in negative dielectrophoresis traps and monolayer growth chambers. Furthermore, morphological characteristics like cell lengths and division symmetries of individual cells were affected when the cells were grown on agarose pads. This indicated a significant impact of solid cultivation supports on cellular traits. The results demonstrate the impact of microcultivation technology on microbial physiology for the first time and show the need for a careful selection and design of the microcultivation technology in order to allow unbiased analysis of cellular behavior.
Erscheinungsjahr
Zeitschriftentitel
Lab on a chip
Band
15
Ausgabe
8
Seite(n)
1822-1834
eISSN
PUB-ID

Zitieren

Dusny C, Grünberger A, Probst C, Wiechert W, Kohlheyer D, Schmid A. Technical bias of microcultivation environments on single cell physiology. Lab on a chip. 2015;15(8):1822-1834.
Dusny, C., Grünberger, A., Probst, C., Wiechert, W., Kohlheyer, D., & Schmid, A. (2015). Technical bias of microcultivation environments on single cell physiology. Lab on a chip, 15(8), 1822-1834. doi:10.1039/C4LC01270D
Dusny, C., Grünberger, A., Probst, C., Wiechert, W., Kohlheyer, D., and Schmid, A. (2015). Technical bias of microcultivation environments on single cell physiology. Lab on a chip 15, 1822-1834.
Dusny, C., et al., 2015. Technical bias of microcultivation environments on single cell physiology. Lab on a chip, 15(8), p 1822-1834.
C. Dusny, et al., “Technical bias of microcultivation environments on single cell physiology”, Lab on a chip, vol. 15, 2015, pp. 1822-1834.
Dusny, C., Grünberger, A., Probst, C., Wiechert, W., Kohlheyer, D., Schmid, A.: Technical bias of microcultivation environments on single cell physiology. Lab on a chip. 15, 1822-1834 (2015).
Dusny, Christian, Grünberger, Alexander, Probst, Christopher, Wiechert, Wolfgang, Kohlheyer, Dietrich, and Schmid, Andreas. “Technical bias of microcultivation environments on single cell physiology”. Lab on a chip 15.8 (2015): 1822-1834.

13 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Single-cell Microfluidic Analysis of Bacillus subtilis.
Cabeen MT, Losick R., J Vis Exp (131), 2018
PMID: 29443042
Simple and Precise Counting of Viable Bacteria by Resazurin-Amplified Picoarray Detection.
Hsieh K, Zec HC, Chen L, Kaushik AM, Mach KE, Liao JC, Wang TH., Anal Chem 90(15), 2018
PMID: 29969556
Recent Advances in the Analysis of Single Cells.
Armbrecht L, Dittrich PS., Anal Chem 89(1), 2017
PMID: 28105840
Coarse-graining bacteria colonies for modelling critical solute distributions in picolitre bioreactors for bacterial studies on single-cell level.
Westerwalbesloh C, Grünberger A, Wiechert W, Kohlheyer D, von Lieres E., Microb Biotechnol 10(4), 2017
PMID: 28371389
Homogenizing bacterial cell factories: Analysis and engineering of phenotypic heterogeneity.
Binder D, Drepper T, Jaeger KE, Delvigne F, Wiechert W, Kohlheyer D, Grünberger A., Metab Eng 42(), 2017
PMID: 28645641
Beyond the bulk: disclosing the life of single microbial cells.
Rosenthal K, Oehling V, Dusny C, Schmid A., FEMS Microbiol Rev 41(6), 2017
PMID: 29029257
Comparative Single-Cell Analysis of Different E. coli Expression Systems during Microfluidic Cultivation.
Binder D, Probst C, Grünberger A, Hilgers F, Loeschcke A, Jaeger KE, Kohlheyer D, Drepper T., PLoS One 11(8), 2016
PMID: 27525986
Modeling and CFD simulation of nutrient distribution in picoliter bioreactors for bacterial growth studies on single-cell level.
Westerwalbesloh C, Grünberger A, Stute B, Weber S, Wiechert W, Kohlheyer D, von Lieres E., Lab Chip 15(21), 2015
PMID: 26345659
Spatiotemporal microbial single-cell analysis using a high-throughput microfluidics cultivation platform.
Grünberger A, Probst C, Helfrich S, Nanda A, Stute B, Wiechert W, von Lieres E, Nöh K, Frunzke J, Kohlheyer D., Cytometry A 87(12), 2015
PMID: 26348020

60 References

Daten bereitgestellt von Europe PubMed Central.

Stochastic pulse regulation in bacterial stress response.
Locke JC, Young JW, Fontes M, Hernandez Jimenez MJ, Elowitz MB., Science 334(6054), 2011
PMID: 21979936
Rate of environmental change determines stress response specificity.
Young JW, Locke JC, Elowitz MB., Proc. Natl. Acad. Sci. U.S.A. 110(10), 2013
PMID: 23407164
Bacterial persistence as a phenotypic switch.
Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S., Science 305(5690), 2004
PMID: 15308767
Microbial phenotypic heterogeneity and antibiotic tolerance.
Dhar N, McKinney JD., Curr. Opin. Microbiol. 10(1), 2007
PMID: 17215163
Persister cells, dormancy and infectious disease.
Lewis K., Nat. Rev. Microbiol. 5(1), 2006
PMID: 17143318
Bacterial persister cell formation and dormancy.
Wood TK, Knabel SJ, Kwan BW., Appl. Environ. Microbiol. 79(23), 2013
PMID: 24038684
Robust growth of Escherichia coli.
Wang P, Robert L, Pelletier J, Dang WL, Taddei F, Wright A, Jun S., Curr. Biol. 20(12), 2010
PMID: 20537537
The role of physiological heterogeneity in microbial population behavior.
Lidstrom ME, Konopka MC., Nat. Chem. Biol. 6(10), 2010
PMID: 20852608
Single-cell analysis in biotechnology, systems biology, and biocatalysis.
Fritzsch FS, Dusny C, Frick O, Schmid A., Annu Rev Chem Biomol Eng 3(), 2012
PMID: 22468600
Chemical and biological single cell analysis.
Schmid A, Kortmann H, Dittrich PS, Blank LM., Curr. Opin. Biotechnol. 21(1), 2010
PMID: 20167469
Single-cell microfluidics: opportunity for bioprocess development.
Grunberger A, Wiechert W, Kohlheyer D., Curr. Opin. Biotechnol. 29(), 2014
PMID: 24642389

Love, AIChE J. 56(), 2010
Microfluidic single cell analysis: from promise to practice.
Lecault V, White AK, Singhal A, Hansen CL., Curr Opin Chem Biol 16(3-4), 2012
PMID: 22525493
Fluidic and microfluidic tools for quantitative systems biology.
Okumus B, Yildiz S, Toprak E., Curr. Opin. Biotechnol. 25(), 2013
PMID: 24484878
Picoliter nDEP traps enable time-resolved contactless single bacterial cell analysis in controlled microenvironments.
Fritzsch FS, Rosenthal K, Kampert A, Howitz S, Dusny C, Blank LM, Schmid A., Lab Chip 13(3), 2013
PMID: 23223864
The Envirostat - a new bioreactor concept.
Kortmann H, Chasanis P, Blank LM, Franzke J, Kenig EY, Schmid A., Lab Chip 9(4), 2008
PMID: 19190793
Measuring single-cell gene expression dynamics in bacteria using fluorescence time-lapse microscopy.
Young JW, Locke JC, Altinok A, Rosenfeld N, Bacarian T, Swain PS, Mjolsness E, Elowitz MB., Nat Protoc 7(1), 2011
PMID: 22179594
A disposable picolitre bioreactor for cultivation and investigation of industrially relevant bacteria on the single cell level.
Grunberger A, Paczia N, Probst C, Schendzielorz G, Eggeling L, Noack S, Wiechert W, Kohlheyer D., Lab Chip 12(11), 2012
PMID: 22511122
Three-dimensional electric field traps for manipulation of cells--calculation and experimental verification.
Schnelle T, Hagedorn R, Fuhr G, Fiedler S, Muller T., Biochim. Biophys. Acta 1157(2), 1993
PMID: 8507649
Beyond growth rate 0.6: Corynebacterium glutamicum cultivated in highly diluted environments.
Grunberger A, van Ooyen J, Paczia N, Rohe P, Schiendzielorz G, Eggeling L, Wiechert W, Kohlheyer D, Noack S., Biotechnol. Bioeng. 110(1), 2012
PMID: 22890752
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
Studies on the amino acid fermentation. Part 1. Production of L-glutamic acid by various microorganisms.
Kinoshita S, Udaka S, Shimono M., J. Gen. Appl. Microbiol. 50(6), 2004
PMID: 15965888
Growth, cell and nuclear divisions in some bacteria.
SCHAECHTER M, WILLIAMSON JP, HOOD JR Jr, KOCH AL., J. Gen. Microbiol. 29(), 1962
PMID: 13976593
Charting microbial phenotypes in multiplex nanoliter batch bioreactors.
Dai J, Yoon SH, Sim HY, Yang YS, Oh TK, Kim JF, Hong JW., Anal. Chem. 85(12), 2013
PMID: 23581968
Single-cell dynamics reveals sustained growth during diauxic shifts.
Boulineau S, Tostevin F, Kiviet DJ, ten Wolde PR, Nghe P, Tans SJ., PLoS ONE 8(4), 2013
PMID: 23637881
Isolated microbial single cells and resulting micropopulations grow faster in controlled environments.
Dusny C, Fritzsch FS, Frick O, Schmid A., Appl. Environ. Microbiol. 78(19), 2012
PMID: 22820335
Light-responsive control of bacterial gene expression: precise triggering of the lac promoter activity using photocaged IPTG.
Binder D, Grunberger A, Loeschcke A, Probst C, Bier C, Pietruszka J, Wiechert W, Kohlheyer D, Jaeger KE, Drepper T., Integr Biol (Camb) 6(8), 2014
PMID: 24894989
Towards real time analysis of protein secretion from single cells.
Kortmann H, Kurth F, Blank LM, Dittrich PS, Schmid A., Lab Chip 9(21), 2009
PMID: 19823717

Probst, Anal. Methods 7(), 2015
Streaming instability in growing cell populations.
Mather W, Mondragon-Palomino O, Danino T, Hasty J, Tsimring LS., Phys. Rev. Lett. 104(20), 2010
PMID: 20867071
The development and application of a single-cell biosensor for the detection of l-methionine and branched-chain amino acids.
Mustafi N, Grunberger A, Kohlheyer D, Bott M, Frunzke J., Metab. Eng. 14(4), 2012
PMID: 22583745
Microfluidic growth chambers with optical tweezers for full spatial single-cell control and analysis of evolving microbes.
Probst C, Grunberger A, Wiechert W, Kohlheyer D., J. Microbiol. Methods 95(3), 2013
PMID: 24041615
High-throughput gene expression analysis at the level of single proteins using a microfluidic turbidostat and automated cell tracking.
Ullman G, Wallden M, Marklund EG, Mahmutovic A, Razinkov I, Elf J., Philos. Trans. R. Soc. Lond., B, Biol. Sci. 368(1611), 2012
PMID: 23267179
Whole lifespan microscopic observation of budding yeast aging through a microfluidic dissection platform.
Lee SS, Avalos Vizcarra I, Huberts DH, Lee LP, Heinemann M., Proc. Natl. Acad. Sci. U.S.A. 109(13), 2012
PMID: 22421136
Mixed messages: how bacteria resolve conflicting signals.
Young JW, Elowitz MB., Mol. Cell 42(4), 2011
PMID: 21596304

Gruenberger, J. Visualized Exp. 82(), 2013
Cell growth and cell division in the rod-shaped actinomycete Corynebacterium glutamicum.
Letek M, Fiuza M, Ordonez E, Villadangos AF, Ramos A, Mateos LM, Gil JA., Antonie Van Leeuwenhoek 94(1), 2008
PMID: 18283557
Single cell growth rate and morphological dynamics revealing an "opportunistic" persistence.
Li B, Qiu Y, Glidle A, Cooper J, Shi H, Yin H., Analyst 139(13), 2014
PMID: 24733150
Single-cell model of prokaryotic cell cycle.
Abner K, Aaviksaar T, Adamberg K, Vilu R., J. Theor. Biol. 341(), 2013
PMID: 24099718
Metabolic viability of Escherichia coli trapped by dielectrophoresis in microfluidics.
Donato SS, Chu V, Prazeres DM, Conde JP., Electrophoresis 34(4), 2013
PMID: 23175163
Induction of a global stress response during the first step of Escherichia coli plate growth.
Cuny C, Lesbats M, Dukan S., Appl. Environ. Microbiol. 73(3), 2006
PMID: 17142356
New technologies for measuring single cell mass.
Popescu G, Park K, Mir M, Bashir R., Lab Chip 14(4), 2014
PMID: 24322181
Cell division site placement and asymmetric growth in mycobacteria.
Joyce G, Williams KJ, Robb M, Noens E, Tizzano B, Shahrezaei V, Robertson BD., PLoS ONE 7(9), 2012
PMID: 22970255
Morphological plasticity as a bacterial survival strategy.
Justice SS, Hunstad DA, Cegelski L, Hultgren SJ., Nat. Rev. Microbiol. 6(2), 2008
PMID: 18157153
Analysis of SOS-induced spontaneous prophage induction in Corynebacterium glutamicum at the single-cell level.
Nanda AM, Heyer A, Kramer C, Grunberger A, Kohlheyer D, Frunzke J., J. Bacteriol. 196(1), 2013
PMID: 24163339
Screening of antibiotic susceptibility to β-lactam-induced elongation of Gram-negative bacteria based on dielectrophoresis.
Chung CC, Cheng IF, Chen HM, Kan HC, Yang WH, Chang HC., Anal. Chem. 84(7), 2012
PMID: 22404714
The lipid II flippase RodA determines morphology and growth in Corynebacterium glutamicum.
Sieger B, Schubert K, Donovan C, Bramkamp M., Mol. Microbiol. 90(5), 2013
PMID: 24118443
Emergence of antibiotic resistance from multinucleated bacterial filaments.
Bos J, Zhang Q, Vyawahare S, Rogers E, Rosenberg SM, Austin RH., Proc. Natl. Acad. Sci. U.S.A. 112(1), 2014
PMID: 25492931
Robustness and accuracy of cell division in Escherichia coli in diverse cell shapes.
Mannik J, Wu F, Hol FJ, Bisicchia P, Sherratt DJ, Keymer JE, Dekker C., Proc. Natl. Acad. Sci. U.S.A. 109(18), 2012
PMID: 22509007
Bacterial growth and motility in sub-micron constrictions.
Mannik J, Driessen R, Galajda P, Keymer JE, Dekker C., Proc. Natl. Acad. Sci. U.S.A. 106(35), 2009
PMID: 19706420
Monitoring of population dynamics of Corynebacterium glutamicum by multiparameter flow cytometry.
Neumeyer A, Hubschmann T, Muller S, Frunzke J., Microb Biotechnol 6(2), 2012
PMID: 23279937

Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®

Quellen

PMID: 25710324
PubMed | Europe PMC

Suchen in

Google Scholar