---
_id: '11339'
abstract:
- lang: eng
  text: The interaction between a cell and its environment shapes fundamental intracellular
    processes such as cellular metabolism. In most cases growth rate is treated as
    a proximal metric for understanding the cellular metabolic status. However, changes
    in growth rate might not reflect metabolic variations in individuals responding
    to environmental fluctuations. Here we use single-cell microfluidics-microscopy
    combined with transcriptomics, proteomics and mathematical modelling to quantify
    the accumulation of glucose within Escherichia coli cells. In contrast to the
    current consensus, we reveal that environmental conditions which are comparatively
    unfavourable for growth, where both nutrients and salinity are depleted, increase
    glucose accumulation rates in individual bacteria and population subsets. We find
    that these changes in metabolic function are underpinned by variations at the
    translational and posttranslational level but not at the transcriptional level
    and are not dictated by changes in cell size. The metabolic response-characteristics
    identified greatly advance our fundamental understanding of the interactions between
    bacteria and their environment and have important ramifications when investigating
    cellular processes where salinity plays an important role.
acknowledgement: G.G. was supported by an EPSRC DTP PhD studentship (EP/M506527/1).
  M.V. and K.T.A. gratefully acknowledge financial support from the EPSRC (EP/N014391/1).
  U.L. was supported through a BBSRC grant (BB/V008021/1) and an MRC Proximity to
  Discovery EXCITEME2 grant (MCPC17189). This work was further supported by a Royal
  Society Research Grant (RG180007) awarded to S.P. and a QUEX Initiator grant awarded
  to S.P. and K.T.A.. D.S.M., T.A.R. and S.P.’s work in this area is also supported
  by a Marie Skłodowska-Curie project SINGEK (H2020-MSCA-ITN-2015-675752) and the
  Gordon and Betty Moore Foundation Marine Microbiology Initiative (GBMF5514). B.M.I.
  acknowledges support from a Wellcome Trust Institutional Strategic Support Award
  to the University of Exeter (204909/Z/16/Z). This project utilised equipment funded
  by the Wellcome Trust Institutional Strategic Support Fund (WT097835MF), Wellcome
  Trust Multi User Equipment Award (WT101650MA) and BBSRC LOLA award (BB/K003240/1).
article_number: '385'
article_processing_charge: No
article_type: original
author:
- first_name: Georgina
  full_name: Glover, Georgina
  last_name: Glover
- first_name: Margaritis
  full_name: Voliotis, Margaritis
  last_name: Voliotis
- first_name: Urszula
  full_name: Łapińska, Urszula
  last_name: Łapińska
- first_name: Brandon M.
  full_name: Invergo, Brandon M.
  last_name: Invergo
- first_name: Darren
  full_name: Soanes, Darren
  last_name: Soanes
- first_name: Paul
  full_name: O’Neill, Paul
  last_name: O’Neill
- first_name: Karen
  full_name: Moore, Karen
  last_name: Moore
- first_name: Nela
  full_name: Nikolic, Nela
  id: 42D9CABC-F248-11E8-B48F-1D18A9856A87
  last_name: Nikolic
  orcid: 0000-0001-9068-6090
- first_name: Peter
  full_name: Petrov, Peter
  last_name: Petrov
- first_name: David S.
  full_name: Milner, David S.
  last_name: Milner
- first_name: Sumita
  full_name: Roy, Sumita
  last_name: Roy
- first_name: Kate
  full_name: Heesom, Kate
  last_name: Heesom
- first_name: Thomas A.
  full_name: Richards, Thomas A.
  last_name: Richards
- first_name: Krasimira
  full_name: Tsaneva-Atanasova, Krasimira
  last_name: Tsaneva-Atanasova
- first_name: Stefano
  full_name: Pagliara, Stefano
  last_name: Pagliara
citation:
  ama: Glover G, Voliotis M, Łapińska U, et al. Nutrient and salt depletion synergistically
    boosts glucose metabolism in individual Escherichia coli cells. <i>Communications
    Biology</i>. 2022;5. doi:<a href="https://doi.org/10.1038/s42003-022-03336-6">10.1038/s42003-022-03336-6</a>
  apa: Glover, G., Voliotis, M., Łapińska, U., Invergo, B. M., Soanes, D., O’Neill,
    P., … Pagliara, S. (2022). Nutrient and salt depletion synergistically boosts
    glucose metabolism in individual Escherichia coli cells. <i>Communications Biology</i>.
    Springer Nature. <a href="https://doi.org/10.1038/s42003-022-03336-6">https://doi.org/10.1038/s42003-022-03336-6</a>
  chicago: Glover, Georgina, Margaritis Voliotis, Urszula Łapińska, Brandon M. Invergo,
    Darren Soanes, Paul O’Neill, Karen Moore, et al. “Nutrient and Salt Depletion
    Synergistically Boosts Glucose Metabolism in Individual Escherichia Coli Cells.”
    <i>Communications Biology</i>. Springer Nature, 2022. <a href="https://doi.org/10.1038/s42003-022-03336-6">https://doi.org/10.1038/s42003-022-03336-6</a>.
  ieee: G. Glover <i>et al.</i>, “Nutrient and salt depletion synergistically boosts
    glucose metabolism in individual Escherichia coli cells,” <i>Communications Biology</i>,
    vol. 5. Springer Nature, 2022.
  ista: Glover G, Voliotis M, Łapińska U, Invergo BM, Soanes D, O’Neill P, Moore K,
    Nikolic N, Petrov P, Milner DS, Roy S, Heesom K, Richards TA, Tsaneva-Atanasova
    K, Pagliara S. 2022. Nutrient and salt depletion synergistically boosts glucose
    metabolism in individual Escherichia coli cells. Communications Biology. 5, 385.
  mla: Glover, Georgina, et al. “Nutrient and Salt Depletion Synergistically Boosts
    Glucose Metabolism in Individual Escherichia Coli Cells.” <i>Communications Biology</i>,
    vol. 5, 385, Springer Nature, 2022, doi:<a href="https://doi.org/10.1038/s42003-022-03336-6">10.1038/s42003-022-03336-6</a>.
  short: G. Glover, M. Voliotis, U. Łapińska, B.M. Invergo, D. Soanes, P. O’Neill,
    K. Moore, N. Nikolic, P. Petrov, D.S. Milner, S. Roy, K. Heesom, T.A. Richards,
    K. Tsaneva-Atanasova, S. Pagliara, Communications Biology 5 (2022).
date_created: 2022-05-01T22:01:41Z
date_published: 2022-04-20T00:00:00Z
date_updated: 2023-08-03T06:45:26Z
day: '20'
ddc:
- '570'
department:
- _id: CaGu
doi: 10.1038/s42003-022-03336-6
external_id:
  isi:
  - '000784143400001'
  pmid:
  - '35444215'
file:
- access_level: open_access
  checksum: 7c6f76ab17393d650825cc240edc84b3
  content_type: application/pdf
  creator: dernst
  date_created: 2022-05-02T06:26:26Z
  date_updated: 2022-05-02T06:26:26Z
  file_id: '11342'
  file_name: 2022_CommBiology_Glover.pdf
  file_size: 2827723
  relation: main_file
  success: 1
file_date_updated: 2022-05-02T06:26:26Z
has_accepted_license: '1'
intvolume: '         5'
isi: 1
language:
- iso: eng
month: '04'
oa: 1
oa_version: Published Version
pmid: 1
publication: Communications Biology
publication_identifier:
  eissn:
  - 2399-3642
publication_status: published
publisher: Springer Nature
quality_controlled: '1'
scopus_import: '1'
status: public
title: Nutrient and salt depletion synergistically boosts glucose metabolism in individual
  Escherichia coli cells
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: 4359f0d1-fa6c-11eb-b949-802e58b17ae8
volume: 5
year: '2022'
...
---
_id: '11713'
abstract:
- lang: eng
  text: "Objective: MazF is a sequence-specific endoribonuclease-toxin of the MazEF
    toxin–antitoxin system. MazF cleaves single-stranded ribonucleic acid (RNA) regions
    at adenine–cytosine–adenine (ACA) sequences in the bacterium Escherichia coli.
    The MazEF system has been used in various biotechnology and synthetic biology
    applications. In this study, we infer how ectopic mazF overexpression affects
    production of heterologous proteins. To this end, we quantified the levels of
    fluorescent proteins expressed in E. coli from reporters translated from the ACA-containing
    or ACA-less messenger RNAs (mRNAs). Additionally, we addressed the impact of the
    5′-untranslated region of these reporter mRNAs under the same conditions by comparing
    expression from mRNAs that comprise (canonical mRNA) or lack this region (leaderless
    mRNA).\r\nResults: Flow cytometry analysis indicates that during mazF overexpression,
    fluorescent proteins are translated from the canonical as well as leaderless mRNAs.
    Our analysis further indicates that longer mazF overexpression generally increases
    the concentration of fluorescent proteins translated from ACA-less mRNAs, however
    it also substantially increases bacterial population heterogeneity. Finally, our
    results suggest that the strength and duration of mazF overexpression should be
    optimized for each experimental setup, to maximize the heterologous protein production
    and minimize the amount of phenotypic heterogeneity in bacterial populations,
    which is unfavorable in biotechnological processes."
acknowledgement: "We acknowledge the Max Perutz Labs FACS Facility together with Thomas
  Sauer. NN is grateful to Călin C. Guet for his support.\r\nThis work was funded
  by the Elise Richter grant V738 of the Austrian Science Fund (FWF), and the FWF
  Lise Meitner grant M1697, to NN; and by the FWF grant P22249, FWF Special Research
  Program RNA-REG F43 (subproject F4316), and FWF doctoral program RNA Biology (W1207),
  to IM. Open access funding provided by the Austrian Science Fund."
article_number: '173'
article_processing_charge: No
article_type: letter_note
author:
- first_name: Nela
  full_name: Nikolic, Nela
  id: 42D9CABC-F248-11E8-B48F-1D18A9856A87
  last_name: Nikolic
  orcid: 0000-0001-9068-6090
- first_name: Martina
  full_name: Sauert, Martina
  last_name: Sauert
- first_name: Tanino G.
  full_name: Albanese, Tanino G.
  last_name: Albanese
- first_name: Isabella
  full_name: Moll, Isabella
  last_name: Moll
citation:
  ama: Nikolic N, Sauert M, Albanese TG, Moll I. Quantifying heterologous gene expression
    during ectopic MazF production in Escherichia coli. <i>BMC Research Notes</i>.
    2022;15. doi:<a href="https://doi.org/10.1186/s13104-022-06061-9">10.1186/s13104-022-06061-9</a>
  apa: Nikolic, N., Sauert, M., Albanese, T. G., &#38; Moll, I. (2022). Quantifying
    heterologous gene expression during ectopic MazF production in Escherichia coli.
    <i>BMC Research Notes</i>. Springer Nature. <a href="https://doi.org/10.1186/s13104-022-06061-9">https://doi.org/10.1186/s13104-022-06061-9</a>
  chicago: Nikolic, Nela, Martina Sauert, Tanino G. Albanese, and Isabella Moll. “Quantifying
    Heterologous Gene Expression during Ectopic MazF Production in Escherichia Coli.”
    <i>BMC Research Notes</i>. Springer Nature, 2022. <a href="https://doi.org/10.1186/s13104-022-06061-9">https://doi.org/10.1186/s13104-022-06061-9</a>.
  ieee: N. Nikolic, M. Sauert, T. G. Albanese, and I. Moll, “Quantifying heterologous
    gene expression during ectopic MazF production in Escherichia coli,” <i>BMC Research
    Notes</i>, vol. 15. Springer Nature, 2022.
  ista: Nikolic N, Sauert M, Albanese TG, Moll I. 2022. Quantifying heterologous gene
    expression during ectopic MazF production in Escherichia coli. BMC Research Notes.
    15, 173.
  mla: Nikolic, Nela, et al. “Quantifying Heterologous Gene Expression during Ectopic
    MazF Production in Escherichia Coli.” <i>BMC Research Notes</i>, vol. 15, 173,
    Springer Nature, 2022, doi:<a href="https://doi.org/10.1186/s13104-022-06061-9">10.1186/s13104-022-06061-9</a>.
  short: N. Nikolic, M. Sauert, T.G. Albanese, I. Moll, BMC Research Notes 15 (2022).
date_created: 2022-08-01T09:04:27Z
date_published: 2022-05-13T00:00:00Z
date_updated: 2022-08-01T09:27:40Z
day: '13'
ddc:
- '570'
department:
- _id: CaGu
doi: 10.1186/s13104-022-06061-9
external_id:
  pmid:
  - '35562780'
file:
- access_level: open_access
  checksum: 008156e5340e9789f0f6d82bde4d347a
  content_type: application/pdf
  creator: dernst
  date_created: 2022-08-01T09:24:42Z
  date_updated: 2022-08-01T09:24:42Z
  file_id: '11714'
  file_name: 2022_BMCResearchNotes_Nikolic.pdf
  file_size: 1545310
  relation: main_file
  success: 1
file_date_updated: 2022-08-01T09:24:42Z
has_accepted_license: '1'
intvolume: '        15'
keyword:
- General Biochemistry
- Genetics and Molecular Biology
- General Medicine
language:
- iso: eng
month: '05'
oa: 1
oa_version: Published Version
pmid: 1
project:
- _id: 26956E74-B435-11E9-9278-68D0E5697425
  call_identifier: FWF
  grant_number: V00738
  name: Bacterial toxin-antitoxin systems as antiphage defense mechanisms
publication: BMC Research Notes
publication_identifier:
  issn:
  - 1756-0500
publication_status: published
publisher: Springer Nature
quality_controlled: '1'
related_material:
  link:
  - relation: erratum
    url: https://doi.org/10.1186/s13104-022-06152-7
scopus_import: '1'
status: public
title: Quantifying heterologous gene expression during ectopic MazF production in
  Escherichia coli
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 15
year: '2022'
...
---
_id: '138'
abstract:
- lang: eng
  text: Autoregulation is the direct modulation of gene expression by the product
    of the corresponding gene. Autoregulation of bacterial gene expression has been
    mostly studied at the transcriptional level, when a protein acts as the cognate
    transcriptional repressor. A recent study investigating dynamics of the bacterial
    toxin–antitoxin MazEF system has shown how autoregulation at both the transcriptional
    and post-transcriptional levels affects the heterogeneity of Escherichia coli
    populations. Toxin–antitoxin systems hold a crucial but still elusive part in
    bacterial response to stress. This perspective highlights how these modules can
    also serve as a great model system for investigating basic concepts in gene regulation.
    However, as the genomic background and environmental conditions substantially
    influence toxin activation, it is important to study (auto)regulation of toxin–antitoxin
    systems in well-defined setups as well as in conditions that resemble the environmental
    niche.
article_processing_charge: Yes (via OA deal)
author:
- first_name: Nela
  full_name: Nikolic, Nela
  id: 42D9CABC-F248-11E8-B48F-1D18A9856A87
  last_name: Nikolic
  orcid: 0000-0001-9068-6090
citation:
  ama: 'Nikolic N. Autoregulation of bacterial gene expression: lessons from the MazEF
    toxin–antitoxin system. <i>Current Genetics</i>. 2019;65(1):133-138. doi:<a href="https://doi.org/10.1007/s00294-018-0879-8">10.1007/s00294-018-0879-8</a>'
  apa: 'Nikolic, N. (2019). Autoregulation of bacterial gene expression: lessons from
    the MazEF toxin–antitoxin system. <i>Current Genetics</i>. Springer. <a href="https://doi.org/10.1007/s00294-018-0879-8">https://doi.org/10.1007/s00294-018-0879-8</a>'
  chicago: 'Nikolic, Nela. “Autoregulation of Bacterial Gene Expression: Lessons from
    the MazEF Toxin–Antitoxin System.” <i>Current Genetics</i>. Springer, 2019. <a
    href="https://doi.org/10.1007/s00294-018-0879-8">https://doi.org/10.1007/s00294-018-0879-8</a>.'
  ieee: 'N. Nikolic, “Autoregulation of bacterial gene expression: lessons from the
    MazEF toxin–antitoxin system,” <i>Current Genetics</i>, vol. 65, no. 1. Springer,
    pp. 133–138, 2019.'
  ista: 'Nikolic N. 2019. Autoregulation of bacterial gene expression: lessons from
    the MazEF toxin–antitoxin system. Current Genetics. 65(1), 133–138.'
  mla: 'Nikolic, Nela. “Autoregulation of Bacterial Gene Expression: Lessons from
    the MazEF Toxin–Antitoxin System.” <i>Current Genetics</i>, vol. 65, no. 1, Springer,
    2019, pp. 133–38, doi:<a href="https://doi.org/10.1007/s00294-018-0879-8">10.1007/s00294-018-0879-8</a>.'
  short: N. Nikolic, Current Genetics 65 (2019) 133–138.
date_created: 2018-12-11T11:44:50Z
date_published: 2019-02-01T00:00:00Z
date_updated: 2023-09-08T13:23:42Z
day: '01'
ddc:
- '570'
department:
- _id: CaGu
doi: 10.1007/s00294-018-0879-8
ec_funded: 1
external_id:
  isi:
  - '000456958800017'
file:
- access_level: open_access
  checksum: 6779708b0b632a1a6ed28c56f5161142
  content_type: application/pdf
  creator: dernst
  date_created: 2019-02-06T07:50:58Z
  date_updated: 2020-07-14T12:44:47Z
  file_id: '5930'
  file_name: 2019_CurrentGenetics_Nikolic.pdf
  file_size: 776399
  relation: main_file
file_date_updated: 2020-07-14T12:44:47Z
has_accepted_license: '1'
intvolume: '        65'
isi: 1
issue: '1'
language:
- iso: eng
month: '02'
oa: 1
oa_version: Published Version
page: 133-138
project:
- _id: 25681D80-B435-11E9-9278-68D0E5697425
  call_identifier: FP7
  grant_number: '291734'
  name: International IST Postdoc Fellowship Programme
publication: Current Genetics
publication_status: published
publisher: Springer
publist_id: '7785'
quality_controlled: '1'
scopus_import: '1'
status: public
title: 'Autoregulation of bacterial gene expression: lessons from the MazEF toxin–antitoxin
  system'
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: c635000d-4b10-11ee-a964-aac5a93f6ac1
volume: 65
year: '2019'
...
---
_id: '5569'
abstract:
- lang: eng
  text: "Nela Nikolic, Tobias Bergmiller, Alexandra Vandervelde, Tanino G. Albanese,
    Lendert Gelens, and Isabella Moll (2018)\r\n“Autoregulation of mazEF expression
    underlies growth heterogeneity in bacterial populations” Nucleic Acids Research,
    doi: 10.15479/AT:ISTA:74;\r\nmicroscopy experiments by Tobias Bergmiller; image
    and data analysis by Nela Nikolic."
article_processing_charge: No
author:
- first_name: Tobias
  full_name: Bergmiller, Tobias
  id: 2C471CFA-F248-11E8-B48F-1D18A9856A87
  last_name: Bergmiller
  orcid: 0000-0001-5396-4346
- first_name: Nela
  full_name: Nikolic, Nela
  id: 42D9CABC-F248-11E8-B48F-1D18A9856A87
  last_name: Nikolic
  orcid: 0000-0001-9068-6090
citation:
  ama: Bergmiller T, Nikolic N. Time-lapse microscopy data. 2018. doi:<a href="https://doi.org/10.15479/AT:ISTA:74">10.15479/AT:ISTA:74</a>
  apa: Bergmiller, T., &#38; Nikolic, N. (2018). Time-lapse microscopy data. Institute
    of Science and Technology Austria. <a href="https://doi.org/10.15479/AT:ISTA:74">https://doi.org/10.15479/AT:ISTA:74</a>
  chicago: Bergmiller, Tobias, and Nela Nikolic. “Time-Lapse Microscopy Data.” Institute
    of Science and Technology Austria, 2018. <a href="https://doi.org/10.15479/AT:ISTA:74">https://doi.org/10.15479/AT:ISTA:74</a>.
  ieee: T. Bergmiller and N. Nikolic, “Time-lapse microscopy data.” Institute of Science
    and Technology Austria, 2018.
  ista: Bergmiller T, Nikolic N. 2018. Time-lapse microscopy data, Institute of Science
    and Technology Austria, <a href="https://doi.org/10.15479/AT:ISTA:74">10.15479/AT:ISTA:74</a>.
  mla: Bergmiller, Tobias, and Nela Nikolic. <i>Time-Lapse Microscopy Data</i>. Institute
    of Science and Technology Austria, 2018, doi:<a href="https://doi.org/10.15479/AT:ISTA:74">10.15479/AT:ISTA:74</a>.
  short: T. Bergmiller, N. Nikolic, (2018).
datarep_id: '74'
date_created: 2018-12-12T12:31:35Z
date_published: 2018-02-07T00:00:00Z
date_updated: 2024-02-21T13:44:45Z
day: '07'
ddc:
- '579'
department:
- _id: CaGu
doi: 10.15479/AT:ISTA:74
file:
- access_level: open_access
  checksum: 61ebb92213cfffeba3ddbaff984b81af
  content_type: application/zip
  creator: system
  date_created: 2018-12-12T13:04:39Z
  date_updated: 2020-07-14T12:47:04Z
  file_id: '5637'
  file_name: IST-2018-74-v1+2_15-11-05.zip
  file_size: 3558703796
  relation: main_file
- access_level: open_access
  checksum: bf26649af310ef6892d68576515cde6d
  content_type: application/zip
  creator: system
  date_created: 2018-12-12T13:04:55Z
  date_updated: 2020-07-14T12:47:04Z
  file_id: '5638'
  file_name: IST-2018-74-v1+3_15-07-31.zip
  file_size: 1830422606
  relation: main_file
- access_level: open_access
  checksum: 8e46eedce06f22acb2be1a9b9d3f56bd
  content_type: application/zip
  creator: system
  date_created: 2018-12-12T13:05:11Z
  date_updated: 2020-07-14T12:47:04Z
  file_id: '5639'
  file_name: IST-2018-74-v1+4_Images_for_analysis.zip
  file_size: 2140849248
  relation: main_file
file_date_updated: 2020-07-14T12:47:04Z
has_accepted_license: '1'
keyword:
- microscopy
- microfluidics
license: https://creativecommons.org/publicdomain/zero/1.0/
month: '02'
oa: 1
oa_version: Published Version
publisher: Institute of Science and Technology Austria
publist_id: '7385'
related_material:
  record:
  - id: '438'
    relation: research_paper
    status: public
status: public
title: Time-lapse microscopy data
tmp:
  image: /images/cc_0.png
  legal_code_url: https://creativecommons.org/publicdomain/zero/1.0/legalcode
  name: Creative Commons Public Domain Dedication (CC0 1.0)
  short: CC0 (1.0)
type: research_data
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
year: '2018'
...
---
_id: '438'
abstract:
- lang: eng
  text: The MazF toxin sequence-specifically cleaves single-stranded RNA upon various
    stressful conditions, and it is activated as a part of the mazEF toxin–antitoxin
    module in Escherichia coli. Although autoregulation of mazEF expression through
    the MazE antitoxin-dependent transcriptional repression has been biochemically
    characterized, less is known about post-transcriptional autoregulation, as well
    as how both of these autoregulatory features affect growth of single cells during
    conditions that promote MazF production. Here, we demonstrate post-transcriptional
    autoregulation of mazF expression dynamics by MazF cleaving its own transcript.
    Single-cell analyses of bacterial populations during ectopic MazF production indicated
    that two-level autoregulation of mazEF expression influences cell-to-cell growth
    rate heterogeneity. The increase in growth rate heterogeneity is governed by the
    MazE antitoxin, and tuned by the MazF-dependent mazF mRNA cleavage. Also, both
    autoregulatory features grant rapid exit from the stress caused by mazF overexpression.
    Time-lapse microscopy revealed that MazF-mediated cleavage of mazF mRNA leads
    to increased temporal variability in length of individual cells during ectopic
    mazF overexpression, as explained by a stochastic model indicating that mazEF
    mRNA cleavage underlies temporal fluctuations in MazF levels during stress.
article_processing_charge: Yes (in subscription journal)
author:
- first_name: Nela
  full_name: Nikolic, Nela
  id: 42D9CABC-F248-11E8-B48F-1D18A9856A87
  last_name: Nikolic
  orcid: 0000-0001-9068-6090
- first_name: Tobias
  full_name: Bergmiller, Tobias
  id: 2C471CFA-F248-11E8-B48F-1D18A9856A87
  last_name: Bergmiller
  orcid: 0000-0001-5396-4346
- first_name: Alexandra
  full_name: Vandervelde, Alexandra
  last_name: Vandervelde
- first_name: Tanino
  full_name: Albanese, Tanino
  last_name: Albanese
- first_name: Lendert
  full_name: Gelens, Lendert
  last_name: Gelens
- first_name: Isabella
  full_name: Moll, Isabella
  last_name: Moll
citation:
  ama: Nikolic N, Bergmiller T, Vandervelde A, Albanese T, Gelens L, Moll I. Autoregulation
    of mazEF expression underlies growth heterogeneity in bacterial populations. <i>Nucleic
    Acids Research</i>. 2018;46(6):2918-2931. doi:<a href="https://doi.org/10.1093/nar/gky079">10.1093/nar/gky079</a>
  apa: Nikolic, N., Bergmiller, T., Vandervelde, A., Albanese, T., Gelens, L., &#38;
    Moll, I. (2018). Autoregulation of mazEF expression underlies growth heterogeneity
    in bacterial populations. <i>Nucleic Acids Research</i>. Oxford University Press.
    <a href="https://doi.org/10.1093/nar/gky079">https://doi.org/10.1093/nar/gky079</a>
  chicago: Nikolic, Nela, Tobias Bergmiller, Alexandra Vandervelde, Tanino Albanese,
    Lendert Gelens, and Isabella Moll. “Autoregulation of MazEF Expression Underlies
    Growth Heterogeneity in Bacterial Populations.” <i>Nucleic Acids Research</i>.
    Oxford University Press, 2018. <a href="https://doi.org/10.1093/nar/gky079">https://doi.org/10.1093/nar/gky079</a>.
  ieee: N. Nikolic, T. Bergmiller, A. Vandervelde, T. Albanese, L. Gelens, and I.
    Moll, “Autoregulation of mazEF expression underlies growth heterogeneity in bacterial
    populations,” <i>Nucleic Acids Research</i>, vol. 46, no. 6. Oxford University
    Press, pp. 2918–2931, 2018.
  ista: Nikolic N, Bergmiller T, Vandervelde A, Albanese T, Gelens L, Moll I. 2018.
    Autoregulation of mazEF expression underlies growth heterogeneity in bacterial
    populations. Nucleic Acids Research. 46(6), 2918–2931.
  mla: Nikolic, Nela, et al. “Autoregulation of MazEF Expression Underlies Growth
    Heterogeneity in Bacterial Populations.” <i>Nucleic Acids Research</i>, vol. 46,
    no. 6, Oxford University Press, 2018, pp. 2918–31, doi:<a href="https://doi.org/10.1093/nar/gky079">10.1093/nar/gky079</a>.
  short: N. Nikolic, T. Bergmiller, A. Vandervelde, T. Albanese, L. Gelens, I. Moll,
    Nucleic Acids Research 46 (2018) 2918–2931.
date_created: 2018-12-11T11:46:29Z
date_published: 2018-04-06T00:00:00Z
date_updated: 2024-02-21T13:44:45Z
day: '06'
ddc:
- '576'
department:
- _id: CaGu
doi: 10.1093/nar/gky079
external_id:
  isi:
  - '000429009500021'
file:
- access_level: open_access
  checksum: 3ff4f545c27e11a4cd20ccb30778793e
  content_type: application/pdf
  creator: system
  date_created: 2018-12-12T10:15:30Z
  date_updated: 2020-07-14T12:46:27Z
  file_id: '5151'
  file_name: IST-2018-971-v1+1_2018_Nikoloc_Autoregulation_of.pdf
  file_size: 5027978
  relation: main_file
file_date_updated: 2020-07-14T12:46:27Z
has_accepted_license: '1'
intvolume: '        46'
isi: 1
issue: '6'
language:
- iso: eng
month: '04'
oa: 1
oa_version: Published Version
page: 2918-2931
project:
- _id: 3AC91DDA-15DF-11EA-824D-93A3E7B544D1
  call_identifier: FWF
  name: FWF Open Access Fund
publication: Nucleic Acids Research
publication_status: published
publisher: Oxford University Press
pubrep_id: '971'
quality_controlled: '1'
related_material:
  record:
  - id: '5569'
    relation: popular_science
    status: public
scopus_import: '1'
status: public
title: Autoregulation of mazEF expression underlies growth heterogeneity in bacterial
  populations
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: c635000d-4b10-11ee-a964-aac5a93f6ac1
volume: 46
year: '2018'
...
---
_id: '541'
abstract:
- lang: eng
  text: 'While we have good understanding of bacterial metabolism at the population
    level, we know little about the metabolic behavior of individual cells: do single
    cells in clonal populations sometimes specialize on different metabolic pathways?
    Such metabolic specialization could be driven by stochastic gene expression and
    could provide individual cells with growth benefits of specialization. We measured
    the degree of phenotypic specialization in two parallel metabolic pathways, the
    assimilation of glucose and arabinose. We grew Escherichia coli in chemostats,
    and used isotope-labeled sugars in combination with nanometer-scale secondary
    ion mass spectrometry and mathematical modeling to quantify sugar assimilation
    at the single-cell level. We found large variation in metabolic activities between
    single cells, both in absolute assimilation and in the degree to which individual
    cells specialize in the assimilation of different sugars. Analysis of transcriptional
    reporters indicated that this variation was at least partially based on cell-to-cell
    variation in gene expression. Metabolic differences between cells in clonal populations
    could potentially reduce metabolic incompatibilities between different pathways,
    and increase the rate at which parallel reactions can be performed.'
article_number: e1007122
author:
- first_name: Nela
  full_name: Nikolic, Nela
  id: 42D9CABC-F248-11E8-B48F-1D18A9856A87
  last_name: Nikolic
  orcid: 0000-0001-9068-6090
- first_name: Frank
  full_name: Schreiber, Frank
  last_name: Schreiber
- first_name: Alma
  full_name: Dal Co, Alma
  last_name: Dal Co
- first_name: Daniel
  full_name: Kiviet, Daniel
  last_name: Kiviet
- first_name: Tobias
  full_name: Bergmiller, Tobias
  id: 2C471CFA-F248-11E8-B48F-1D18A9856A87
  last_name: Bergmiller
  orcid: 0000-0001-5396-4346
- first_name: Sten
  full_name: Littmann, Sten
  last_name: Littmann
- first_name: Marcel
  full_name: Kuypers, Marcel
  last_name: Kuypers
- first_name: Martin
  full_name: Ackermann, Martin
  last_name: Ackermann
citation:
  ama: Nikolic N, Schreiber F, Dal Co A, et al. Cell-to-cell variation and specialization
    in sugar metabolism in clonal bacterial populations. <i>PLoS Genetics</i>. 2017;13(12).
    doi:<a href="https://doi.org/10.1371/journal.pgen.1007122">10.1371/journal.pgen.1007122</a>
  apa: Nikolic, N., Schreiber, F., Dal Co, A., Kiviet, D., Bergmiller, T., Littmann,
    S., … Ackermann, M. (2017). Cell-to-cell variation and specialization in sugar
    metabolism in clonal bacterial populations. <i>PLoS Genetics</i>. Public Library
    of Science. <a href="https://doi.org/10.1371/journal.pgen.1007122">https://doi.org/10.1371/journal.pgen.1007122</a>
  chicago: Nikolic, Nela, Frank Schreiber, Alma Dal Co, Daniel Kiviet, Tobias Bergmiller,
    Sten Littmann, Marcel Kuypers, and Martin Ackermann. “Cell-to-Cell Variation and
    Specialization in Sugar Metabolism in Clonal Bacterial Populations.” <i>PLoS Genetics</i>.
    Public Library of Science, 2017. <a href="https://doi.org/10.1371/journal.pgen.1007122">https://doi.org/10.1371/journal.pgen.1007122</a>.
  ieee: N. Nikolic <i>et al.</i>, “Cell-to-cell variation and specialization in sugar
    metabolism in clonal bacterial populations,” <i>PLoS Genetics</i>, vol. 13, no.
    12. Public Library of Science, 2017.
  ista: Nikolic N, Schreiber F, Dal Co A, Kiviet D, Bergmiller T, Littmann S, Kuypers
    M, Ackermann M. 2017. Cell-to-cell variation and specialization in sugar metabolism
    in clonal bacterial populations. PLoS Genetics. 13(12), e1007122.
  mla: Nikolic, Nela, et al. “Cell-to-Cell Variation and Specialization in Sugar Metabolism
    in Clonal Bacterial Populations.” <i>PLoS Genetics</i>, vol. 13, no. 12, e1007122,
    Public Library of Science, 2017, doi:<a href="https://doi.org/10.1371/journal.pgen.1007122">10.1371/journal.pgen.1007122</a>.
  short: N. Nikolic, F. Schreiber, A. Dal Co, D. Kiviet, T. Bergmiller, S. Littmann,
    M. Kuypers, M. Ackermann, PLoS Genetics 13 (2017).
date_created: 2018-12-11T11:47:04Z
date_published: 2017-12-18T00:00:00Z
date_updated: 2023-02-23T14:10:34Z
day: '18'
ddc:
- '576'
- '579'
department:
- _id: CaGu
doi: 10.1371/journal.pgen.1007122
ec_funded: 1
file:
- access_level: open_access
  checksum: 22426d9382f21554bad5fa5967afcfd0
  content_type: application/pdf
  creator: system
  date_created: 2018-12-12T10:14:35Z
  date_updated: 2020-07-14T12:46:46Z
  file_id: '5088'
  file_name: IST-2018-959-v1+1_2017_Nikolic_Cell-to-cell.pdf
  file_size: 1308475
  relation: main_file
file_date_updated: 2020-07-14T12:46:46Z
has_accepted_license: '1'
intvolume: '        13'
issue: '12'
language:
- iso: eng
month: '12'
oa: 1
oa_version: Published Version
project:
- _id: 25681D80-B435-11E9-9278-68D0E5697425
  call_identifier: FP7
  grant_number: '291734'
  name: International IST Postdoc Fellowship Programme
publication: PLoS Genetics
publication_identifier:
  issn:
  - '15537390'
publication_status: published
publisher: Public Library of Science
publist_id: '7275'
pubrep_id: '959'
quality_controlled: '1'
related_material:
  record:
  - id: '9844'
    relation: research_data
    status: public
  - id: '9845'
    relation: research_data
    status: public
  - id: '9846'
    relation: research_data
    status: public
scopus_import: 1
status: public
title: Cell-to-cell variation and specialization in sugar metabolism in clonal bacterial
  populations
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 13
year: '2017'
...
---
_id: '624'
abstract:
- lang: eng
  text: Bacteria adapt to adverse environmental conditions by altering gene expression
    patterns. Recently, a novel stress adaptation mechanism has been described that
    allows Escherichia coli to alter gene expression at the post-transcriptional level.
    The key player in this regulatory pathway is the endoribonuclease MazF, the toxin
    component of the toxin-antitoxin module mazEF that is triggered by various stressful
    conditions. In general, MazF degrades the majority of transcripts by cleaving
    at ACA sites, which results in the retardation of bacterial growth. Furthermore,
    MazF can process a small subset of mRNAs and render them leaderless by removing
    their ribosome binding site. MazF concomitantly modifies ribosomes, making them
    selective for the translation of leaderless mRNAs. In this study, we employed
    fluorescent reporter-systems to investigate mazEF expression during stressful
    conditions, and to infer consequences of the mRNA processing mediated by MazF
    on gene expression at the single-cell level. Our results suggest that mazEF transcription
    is maintained at low levels in single cells encountering adverse conditions, such
    as antibiotic stress or amino acid starvation. Moreover, using the grcA mRNA as
    a model for MazF-mediated mRNA processing, we found that MazF activation promotes
    heterogeneity in the grcA reporter expression, resulting in a subpopulation of
    cells with increased levels of GrcA reporter protein.
acknowledgement: 'Austrian Science Fund (FWF): M1697, P22249; Swiss National Science
  Foundation (SNF): 145706; European Commission;FWF Special Research Program: RNA-REG
  F43'
article_number: '3830'
author:
- first_name: Nela
  full_name: Nikolic, Nela
  id: 42D9CABC-F248-11E8-B48F-1D18A9856A87
  last_name: Nikolic
  orcid: 0000-0001-9068-6090
- first_name: Zrinka
  full_name: Didara, Zrinka
  last_name: Didara
- first_name: Isabella
  full_name: Moll, Isabella
  last_name: Moll
citation:
  ama: Nikolic N, Didara Z, Moll I. MazF activation promotes translational heterogeneity
    of the grcA mRNA in Escherichia coli populations. <i>PeerJ</i>. 2017;2017(9).
    doi:<a href="https://doi.org/10.7717/peerj.3830">10.7717/peerj.3830</a>
  apa: Nikolic, N., Didara, Z., &#38; Moll, I. (2017). MazF activation promotes translational
    heterogeneity of the grcA mRNA in Escherichia coli populations. <i>PeerJ</i>.
    PeerJ. <a href="https://doi.org/10.7717/peerj.3830">https://doi.org/10.7717/peerj.3830</a>
  chicago: Nikolic, Nela, Zrinka Didara, and Isabella Moll. “MazF Activation Promotes
    Translational Heterogeneity of the GrcA MRNA in Escherichia Coli Populations.”
    <i>PeerJ</i>. PeerJ, 2017. <a href="https://doi.org/10.7717/peerj.3830">https://doi.org/10.7717/peerj.3830</a>.
  ieee: N. Nikolic, Z. Didara, and I. Moll, “MazF activation promotes translational
    heterogeneity of the grcA mRNA in Escherichia coli populations,” <i>PeerJ</i>,
    vol. 2017, no. 9. PeerJ, 2017.
  ista: Nikolic N, Didara Z, Moll I. 2017. MazF activation promotes translational
    heterogeneity of the grcA mRNA in Escherichia coli populations. PeerJ. 2017(9),
    3830.
  mla: Nikolic, Nela, et al. “MazF Activation Promotes Translational Heterogeneity
    of the GrcA MRNA in Escherichia Coli Populations.” <i>PeerJ</i>, vol. 2017, no.
    9, 3830, PeerJ, 2017, doi:<a href="https://doi.org/10.7717/peerj.3830">10.7717/peerj.3830</a>.
  short: N. Nikolic, Z. Didara, I. Moll, PeerJ 2017 (2017).
date_created: 2018-12-11T11:47:33Z
date_published: 2017-09-21T00:00:00Z
date_updated: 2021-01-12T08:06:48Z
day: '21'
ddc:
- '579'
department:
- _id: CaGu
doi: 10.7717/peerj.3830
file:
- access_level: open_access
  checksum: 3d79ae6b6eabc90b0eaaed82ff3493b0
  content_type: application/pdf
  creator: system
  date_created: 2018-12-12T10:11:51Z
  date_updated: 2020-07-14T12:47:24Z
  file_id: '4908'
  file_name: IST-2017-909-v1+1_peerj-3830.pdf
  file_size: 682064
  relation: main_file
file_date_updated: 2020-07-14T12:47:24Z
has_accepted_license: '1'
intvolume: '      2017'
issue: '9'
language:
- iso: eng
month: '09'
oa: 1
oa_version: Published Version
publication: PeerJ
publication_identifier:
  issn:
  - '21678359'
publication_status: published
publisher: PeerJ
publist_id: '7172'
pubrep_id: '909'
quality_controlled: '1'
scopus_import: 1
status: public
title: MazF activation promotes translational heterogeneity of the grcA mRNA in Escherichia
  coli populations
tmp:
  image: /images/cc_by.png
  legal_code_url: https://creativecommons.org/licenses/by/4.0/legalcode
  name: Creative Commons Attribution 4.0 International Public License (CC-BY 4.0)
  short: CC BY (4.0)
type: journal_article
user_id: 2DF688A6-F248-11E8-B48F-1D18A9856A87
volume: 2017
year: '2017'
...
---
_id: '9844'
article_processing_charge: No
author:
- first_name: Nela
  full_name: Nikolic, Nela
  id: 42D9CABC-F248-11E8-B48F-1D18A9856A87
  last_name: Nikolic
  orcid: 0000-0001-9068-6090
- first_name: Frank
  full_name: Schreiber, Frank
  last_name: Schreiber
- first_name: Alma
  full_name: Dal Co, Alma
  last_name: Dal Co
- first_name: Daniel
  full_name: Kiviet, Daniel
  last_name: Kiviet
- first_name: Tobias
  full_name: Bergmiller, Tobias
  id: 2C471CFA-F248-11E8-B48F-1D18A9856A87
  last_name: Bergmiller
  orcid: 0000-0001-5396-4346
- first_name: Sten
  full_name: Littmann, Sten
  last_name: Littmann
- first_name: Marcel
  full_name: Kuypers, Marcel
  last_name: Kuypers
- first_name: Martin
  full_name: Ackermann, Martin
  last_name: Ackermann
citation:
  ama: Nikolic N, Schreiber F, Dal Co A, et al. Source data for figures and tables.
    2017. doi:<a href="https://doi.org/10.1371/journal.pgen.1007122.s018">10.1371/journal.pgen.1007122.s018</a>
  apa: Nikolic, N., Schreiber, F., Dal Co, A., Kiviet, D., Bergmiller, T., Littmann,
    S., … Ackermann, M. (2017). Source data for figures and tables. Public Library
    of Science. <a href="https://doi.org/10.1371/journal.pgen.1007122.s018">https://doi.org/10.1371/journal.pgen.1007122.s018</a>
  chicago: Nikolic, Nela, Frank Schreiber, Alma Dal Co, Daniel Kiviet, Tobias Bergmiller,
    Sten Littmann, Marcel Kuypers, and Martin Ackermann. “Source Data for Figures
    and Tables.” Public Library of Science, 2017. <a href="https://doi.org/10.1371/journal.pgen.1007122.s018">https://doi.org/10.1371/journal.pgen.1007122.s018</a>.
  ieee: N. Nikolic <i>et al.</i>, “Source data for figures and tables.” Public Library
    of Science, 2017.
  ista: Nikolic N, Schreiber F, Dal Co A, Kiviet D, Bergmiller T, Littmann S, Kuypers
    M, Ackermann M. 2017. Source data for figures and tables, Public Library of Science,
    <a href="https://doi.org/10.1371/journal.pgen.1007122.s018">10.1371/journal.pgen.1007122.s018</a>.
  mla: Nikolic, Nela, et al. <i>Source Data for Figures and Tables</i>. Public Library
    of Science, 2017, doi:<a href="https://doi.org/10.1371/journal.pgen.1007122.s018">10.1371/journal.pgen.1007122.s018</a>.
  short: N. Nikolic, F. Schreiber, A. Dal Co, D. Kiviet, T. Bergmiller, S. Littmann,
    M. Kuypers, M. Ackermann, (2017).
date_created: 2021-08-09T13:27:16Z
date_published: 2017-12-18T00:00:00Z
date_updated: 2023-02-23T12:25:04Z
day: '18'
department:
- _id: CaGu
doi: 10.1371/journal.pgen.1007122.s018
month: '12'
oa_version: Published Version
publisher: Public Library of Science
related_material:
  record:
  - id: '541'
    relation: used_in_publication
    status: public
status: public
title: Source data for figures and tables
type: research_data_reference
user_id: 6785fbc1-c503-11eb-8a32-93094b40e1cf
year: '2017'
...
---
_id: '9845'
abstract:
- lang: eng
  text: "Estimates of 13 C-arabinose and 2 H-glucose uptake from the fractions of
    heavy isotopes measured\tin single cells"
article_processing_charge: No
author:
- first_name: Nela
  full_name: Nikolic, Nela
  id: 42D9CABC-F248-11E8-B48F-1D18A9856A87
  last_name: Nikolic
  orcid: 0000-0001-9068-6090
- first_name: Frank
  full_name: Schreiber, Frank
  last_name: Schreiber
- first_name: Alma
  full_name: Dal Co, Alma
  last_name: Dal Co
- first_name: Daniel
  full_name: Kiviet, Daniel
  last_name: Kiviet
- first_name: Tobias
  full_name: Bergmiller, Tobias
  id: 2C471CFA-F248-11E8-B48F-1D18A9856A87
  last_name: Bergmiller
  orcid: 0000-0001-5396-4346
- first_name: Sten
  full_name: Littmann, Sten
  last_name: Littmann
- first_name: Marcel
  full_name: Kuypers, Marcel
  last_name: Kuypers
- first_name: Martin
  full_name: Ackermann, Martin
  last_name: Ackermann
citation:
  ama: Nikolic N, Schreiber F, Dal Co A, et al. Mathematical model. 2017. doi:<a href="https://doi.org/10.1371/journal.pgen.1007122.s017">10.1371/journal.pgen.1007122.s017</a>
  apa: Nikolic, N., Schreiber, F., Dal Co, A., Kiviet, D., Bergmiller, T., Littmann,
    S., … Ackermann, M. (2017). Mathematical model. Public Library of Science. <a
    href="https://doi.org/10.1371/journal.pgen.1007122.s017">https://doi.org/10.1371/journal.pgen.1007122.s017</a>
  chicago: Nikolic, Nela, Frank Schreiber, Alma Dal Co, Daniel Kiviet, Tobias Bergmiller,
    Sten Littmann, Marcel Kuypers, and Martin Ackermann. “Mathematical Model.” Public
    Library of Science, 2017. <a href="https://doi.org/10.1371/journal.pgen.1007122.s017">https://doi.org/10.1371/journal.pgen.1007122.s017</a>.
  ieee: N. Nikolic <i>et al.</i>, “Mathematical model.” Public Library of Science,
    2017.
  ista: Nikolic N, Schreiber F, Dal Co A, Kiviet D, Bergmiller T, Littmann S, Kuypers
    M, Ackermann M. 2017. Mathematical model, Public Library of Science, <a href="https://doi.org/10.1371/journal.pgen.1007122.s017">10.1371/journal.pgen.1007122.s017</a>.
  mla: Nikolic, Nela, et al. <i>Mathematical Model</i>. Public Library of Science,
    2017, doi:<a href="https://doi.org/10.1371/journal.pgen.1007122.s017">10.1371/journal.pgen.1007122.s017</a>.
  short: N. Nikolic, F. Schreiber, A. Dal Co, D. Kiviet, T. Bergmiller, S. Littmann,
    M. Kuypers, M. Ackermann, (2017).
date_created: 2021-08-09T13:31:51Z
date_published: 2017-12-18T00:00:00Z
date_updated: 2023-02-23T12:25:04Z
day: '18'
department:
- _id: CaGu
doi: 10.1371/journal.pgen.1007122.s017
month: '12'
oa_version: None
publisher: Public Library of Science
related_material:
  record:
  - id: '541'
    relation: used_in_publication
    status: public
status: public
title: Mathematical model
type: research_data_reference
user_id: 6785fbc1-c503-11eb-8a32-93094b40e1cf
year: '2017'
...
---
_id: '9846'
article_processing_charge: No
author:
- first_name: Nela
  full_name: Nikolic, Nela
  id: 42D9CABC-F248-11E8-B48F-1D18A9856A87
  last_name: Nikolic
  orcid: 0000-0001-9068-6090
- first_name: Frank
  full_name: Schreiber, Frank
  last_name: Schreiber
- first_name: Alma
  full_name: Dal Co, Alma
  last_name: Dal Co
- first_name: Daniel
  full_name: Kiviet, Daniel
  last_name: Kiviet
- first_name: Tobias
  full_name: Bergmiller, Tobias
  id: 2C471CFA-F248-11E8-B48F-1D18A9856A87
  last_name: Bergmiller
  orcid: 0000-0001-5396-4346
- first_name: Sten
  full_name: Littmann, Sten
  last_name: Littmann
- first_name: Marcel
  full_name: Kuypers, Marcel
  last_name: Kuypers
- first_name: Martin
  full_name: Ackermann, Martin
  last_name: Ackermann
citation:
  ama: Nikolic N, Schreiber F, Dal Co A, et al. Supplementary methods. 2017. doi:<a
    href="https://doi.org/10.1371/journal.pgen.1007122.s016">10.1371/journal.pgen.1007122.s016</a>
  apa: Nikolic, N., Schreiber, F., Dal Co, A., Kiviet, D., Bergmiller, T., Littmann,
    S., … Ackermann, M. (2017). Supplementary methods. Public Library of Science.
    <a href="https://doi.org/10.1371/journal.pgen.1007122.s016">https://doi.org/10.1371/journal.pgen.1007122.s016</a>
  chicago: Nikolic, Nela, Frank Schreiber, Alma Dal Co, Daniel Kiviet, Tobias Bergmiller,
    Sten Littmann, Marcel Kuypers, and Martin Ackermann. “Supplementary Methods.”
    Public Library of Science, 2017. <a href="https://doi.org/10.1371/journal.pgen.1007122.s016">https://doi.org/10.1371/journal.pgen.1007122.s016</a>.
  ieee: N. Nikolic <i>et al.</i>, “Supplementary methods.” Public Library of Science,
    2017.
  ista: Nikolic N, Schreiber F, Dal Co A, Kiviet D, Bergmiller T, Littmann S, Kuypers
    M, Ackermann M. 2017. Supplementary methods, Public Library of Science, <a href="https://doi.org/10.1371/journal.pgen.1007122.s016">10.1371/journal.pgen.1007122.s016</a>.
  mla: Nikolic, Nela, et al. <i>Supplementary Methods</i>. Public Library of Science,
    2017, doi:<a href="https://doi.org/10.1371/journal.pgen.1007122.s016">10.1371/journal.pgen.1007122.s016</a>.
  short: N. Nikolic, F. Schreiber, A. Dal Co, D. Kiviet, T. Bergmiller, S. Littmann,
    M. Kuypers, M. Ackermann, (2017).
date_created: 2021-08-09T13:35:17Z
date_published: 2017-12-18T00:00:00Z
date_updated: 2023-02-23T12:25:04Z
day: '18'
department:
- _id: CaGu
doi: 10.1371/journal.pgen.1007122.s016
month: '12'
oa_version: Published Version
publisher: Public Library of Science
related_material:
  record:
  - id: '541'
    relation: used_in_publication
    status: public
status: public
title: Supplementary methods
type: research_data_reference
user_id: 6785fbc1-c503-11eb-8a32-93094b40e1cf
year: '2017'
...
