A minimum information standard for reproducing bench-scale bacterial cell growth and productivity

Salit, Marc; Hecht, Ariel; Munro, Sarah A.; Filliben, James

doi:10.1038/s42003-018-0220-6

Title: A minimum information standard for reproducing bench-scale bacterial cell growth and productivity

Abstract

Reproducing, exchanging, comparing, and building on each other’s work is foundational to technology advances. Advancing biotechnology calls for reliable reuse of engineered organisms. Reliable reuse of engineered organisms requires reproducible growth and productivity. Here, we identify the experimental factors that have the greatest effect on the growth and productivity of our engineered organisms in order to demonstrate reproducibility for biotechnology. Here, we present a draft of a Minimum Information Standard for Engineered Organism Experiments based on this method. We evaluate the effect of 22 factors on Escherichia coli engineered to produce the small molecule lycopene, and 18 factors on E. coli engineered to produce red fluorescent protein. Container geometry and shaking have the greatest effect on product titer and yield. We reproduce our results under two different conditions of reproducibility: conditions of use (different fractional factorial experiments), and time (48 biological replicates performed on 12 different days over four months).

Authors:

Salit, Marc ^[1]; Hecht, Ariel ^[2]; Munro, Sarah A. ^[3]; Filliben, James ^[4]

Joint Initiative for Metrology in Biology, Stanford, CA (United States); National Inst. of Standards and Technology, Stanford, CA (United States); Stanford Univ., Stanford, CA (United States); SLAC National Accelerator Lab., Menlo Park, CA (United States)
Joint Initiative for Metrology in Biology, Stanford, CA (United States); National Inst. of Standards and Technology, Stanford, CA (United States); Stanford Univ., Stanford, CA (United States)
Joint Initiative for Metrology in Biology, Stanford, CA (United States); National Inst. of Standards and Technology, Stanford, CA (United States); Stanford Univ., Stanford, CA (United States); Univ. of Minnesota, Minneapolis, MN (United States)
National Inst. of Standards and Technology (NIST), Gaithersburg, MD (United States)

Publication Date:: Sat Dec 01 00:00:00 EST 2018

Research Org.:: SLAC National Accelerator Laboratory (SLAC), Menlo Park, CA (United States)

Sponsoring Org.:: USDOE

OSTI Identifier:: 1480469

Grant/Contract Number:: AC02-76SF00515

Resource Type:: Accepted Manuscript

Journal Name:: Communications Biology

Additional Journal Information:: Journal Volume: 1; Journal Issue: 1; Journal ID: ISSN 2399-3642

Publisher:: Springer Nature

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Salit, Marc, Hecht, Ariel, Munro, Sarah A., and Filliben, James. A minimum information standard for reproducing bench-scale bacterial cell growth and productivity.  United States: N. p., 2018. 
Web.  doi:10.1038/s42003-018-0220-6.

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                    Salit, Marc, Hecht, Ariel, Munro, Sarah A., & Filliben, James. A minimum information standard for reproducing bench-scale bacterial cell growth and productivity.  United States.  https://doi.org/10.1038/s42003-018-0220-6

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                    Salit, Marc, Hecht, Ariel, Munro, Sarah A., and Filliben, James. Sat .  
"A minimum information standard for reproducing bench-scale bacterial cell growth and productivity".  United States.  https://doi.org/10.1038/s42003-018-0220-6.  https://www.osti.gov/servlets/purl/1480469.

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@article{osti_1480469,

  title        = {A minimum information standard for reproducing bench-scale bacterial cell growth and productivity},

  author       = {Salit, Marc and Hecht, Ariel and Munro, Sarah A. and Filliben, James},

  abstractNote = {Reproducing, exchanging, comparing, and building on each other’s work is foundational to technology advances. Advancing biotechnology calls for reliable reuse of engineered organisms. Reliable reuse of engineered organisms requires reproducible growth and productivity. Here, we identify the experimental factors that have the greatest effect on the growth and productivity of our engineered organisms in order to demonstrate reproducibility for biotechnology. Here, we present a draft of a Minimum Information Standard for Engineered Organism Experiments based on this method. We evaluate the effect of 22 factors on Escherichia coli engineered to produce the small molecule lycopene, and 18 factors on E. coli engineered to produce red fluorescent protein. Container geometry and shaking have the greatest effect on product titer and yield. We reproduce our results under two different conditions of reproducibility: conditions of use (different fractional factorial experiments), and time (48 biological replicates performed on 12 different days over four months).},

  doi          = {10.1038/s42003-018-0220-6},

  journal      = {Communications Biology},

  number       = 1,

  volume       = 1,

  place        = {United States},

  year         = {Sat Dec 01 00:00:00 EST 2018},

  month        = {Sat Dec 01 00:00:00 EST 2018}

}

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Cited by: 15 works

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Figures / Tables:

Table 1: 32 experimental factors that have been documented to affect cell growth and productivity

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Figshare
DOI: 10.6084/m9.figshare.6848957.v1

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margin-top: 0.5em; padding-left: 0; line-height:1.8em;"> <li> <span style="color:#5C7B2D;"> Singh, Vineeta; Haque, Shafiul; Niwas, Ram</span> </li> <li> Frontiers in Microbiology, Vol. 7</li> <li> <span class="text-muted related-url">DOI: <a href="https://doi.org/10.3389/fmicb.2016.02087" class="text-muted" target="_blank" rel="noopener noreferrer">10.3389/fmicb.2016.02087<span class="fa fa-external-link" aria-hidden="true"></span></a></span> </li> </ul> <hr/> </div> </div> <div class="pagination-container small"> <a class="pure-button prev page" href="#" rel="prev"><span class="sr-only">Previous Page</span><span class="fa fa-angle-left"></span></a> <ul class="pagination d-inline-block" style="padding-left:.2em;"></ul> <a class="pure-button next page" href="#" rel="next"><span class="sr-only">Next Page</span><span class="fa fa-angle-right"></span></a> </div> </div> </div> <div class="col-sm-3 order-sm-3"> <ul class="nav nav-stacked"> <li class="active"><a href="" class="reference-type-filter tab-nav" data-tab="biblio-references" data-filter="type" data-pattern=""><span class="fa fa-angle-right"></span> All References</a></li> <li class="small" style="margin-left:.75em; 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margin-top:0px;">Similar Records in DOE PAGES and OSTI.GOV collections:</p> <aside> <ul class="item-list" itemscope itemtype="http://schema.org/ItemList" style="padding-left:0; list-style-type: none;"> <li> <div class="article item document" itemprop="itemListElement" itemscope itemtype="http://schema.org/WebPage"><meta itemprop="position" content="0" /><div class="item-info"> <h2 class="title" itemprop="name headline"><a href="/pages/biblio/1807728-promoter-architecture-differences-among-alphaproteobacteria-other-bacterial-taxa" itemprop="url">Promoter Architecture Differences among <i>Alphaproteobacteria</i> and Other Bacterial Taxa</a></h2> <div class="metadata"> <small class="text-muted" style="text-transform:uppercase;display:block;line-height:2.5em;">Journal Article</small><span class="authors"> <span class="author">Myers, Kevin S.</span> ; <span class="author">Noguera, Daniel R.</span> ; <span class="author">Donohue, Timothy J.</span> ; <span class="author">...</span> <span class="text-muted pubdata"> - mSystems</span> </span> </div> <div class="abstract">Much of our knowledge of bacterial transcription initiation has been derived from studying the promoters of Escherichia coli and Bacillus subtilis. Given the expansive diversity across the bacterial phylogeny, it is unclear how much of this knowledge can be applied to other organisms. Here, we report on bioinformatic analyses of promoter sequences of the primary σ factor (σ<sup>70</sup>) by leveraging publicly available transcription start site (TSS) sequencing data sets for nine bacterial species spanning five phyla. This analysis identifies previously unreported differences in the –35 and –10 elements of σ<sup>70</sup>-dependent promoters in several groups of bacteria. We found that <em>Actinobacteria</em><a href='#' onclick='$(this).hide().next().show().next().show();return false;' style='margin-left:10px;'>more »</a><span style='display:none;'> and <em>Betaproteobacteria</em> σ<sup>70</sup>-dependent promoters lack the TTG triad in their –35 element, which is predicted to be conserved across the bacterial phyla. In addition, the majority of the <em>Alphaproteobacteria</em> σ<sup>70</sup>-dependent promoters analyzed lacked the thymine at position –7 that is highly conserved in other phyla. Bioinformatic examination of the <em>Alphaproteobacteria</em> σ<sup>70</sup>-dependent promoters identifies a significant overrepresentation of essential genes and ones encoding proteins with common cellular functions downstream of promoters containing an A, C, or G at position –7. We propose that transcription of many σ<sup>70</sup>-dependent promoters in <em>Alphaproteobacteria</em> depends on the transcription factor CarD, which is an essential protein in several members of this phylum. Our analysis expands the knowledge of promoter architecture across the bacterial phylogeny and provides new information that can be used to engineer bacteria for use in medical, environmental, agricultural, and biotechnological processes.</span><a href='#' onclick='$(this).hide().prev().hide().prev().show();return false;' style='margin-left:10px;display:none;'>« less</a></div><div class="metadata-links small clearfix text-muted" style="margin-top:15px;"> <div class="pure-menu pure-menu-horizontal pull-right" style="width:unset;"> <ul class="pure-menu-list"> <li class="pure-menu-item"><span class="item-info-ftlink"><a class="misc doi-link " href="https://doi.org/10.1128/mSystems.00526-21" target="_blank" rel="noopener" title="Link to document DOI" data-ostiid="1807728" data-product-type="Journal Article" data-product-subtype="PA" >https://doi.org/10.1128/mSystems.00526-21</a></span></li> </ul> </div> </div> </div> <div class="clearfix"></div> </div> </li> <li> <div class="article item document" itemprop="itemListElement" itemscope itemtype="http://schema.org/WebPage"><meta itemprop="position" content="2" /><div class="item-info"> <h2 class="title" itemprop="name headline"><a href="/pages/biblio/1432073-improving-methyl-ketone-production-escherichia-coli-heterologous-expression-nadhdependent-fabg" itemprop="url">Improving methyl ketone production in <i>Escherichia coli</i> by heterologous expression of NADH‐dependent FabG</a></h2> <div class="metadata"> <small class="text-muted" style="text-transform:uppercase;display:block;line-height:2.5em;">Journal Article</small><span class="authors"> <span class="author">Goh, Ee‐Been</span> ; <span class="author">Chen, Yan</span> ; <span class="author">Petzold, Christopher J.</span> ; <span class="author">...</span> <span class="text-muted pubdata"> - Biotechnology and Bioengineering</span> </span> </div> <div class="abstract">Abstract We previously engineered Escherichia coli to overproduce medium‐ to long‐chain saturated and monounsaturated methyl ketones, which could potentially be applied as diesel fuel blending agents or in the flavor and fragrance industry. Recent efforts at strain optimization have focused on cofactor balance, as fatty acid‐derived pathways face the systematic metabolic challenge of net NADPH consumption (in large part, resulting from the key fatty acid biosynthetic enzyme FabG [β‐ketoacyl‐ACP reductase]) and net NADH production. In this study, we attempted to mitigate cofactor imbalance by heterologously expressing NADH‐dependent, rather than NADPH‐dependent, versions of FabG identified in previous studies. Of the four<a href='#' onclick='$(this).hide().next().show().next().show();return false;' style='margin-left:10px;'>more »</a><span style='display:none;'> NADH‐dependent versions of FabG tested in our previously best‐reported methyl ketone‐producing strain (EGS1895), the version from Acholeplasma laidlawii (Al_FabG) showed the greatest increase in methyl ketone yield in shake flasks (35–75% higher than for an RFP negative‐control strain, depending on sugar loading). An improved strain (EGS2920) attained methyl ketone titers during fed‐batch fermentation of 5.4 ± 0.5 g/L, which were, on average, ca. 40% greater than those for the base strain (EGS1895) under fermentation conditions optimized in this study. Shotgun proteomic data for strains EGS2920 and EGS1895 during fed‐batch fermentation were consistent with the goal of alleviating NADPH limitation through expression of Al_FabG. For example, relative to strain EGS1895, strain EGS2920 significantly upregulated glucose‐6‐phosphate isomerase (directing flux into glycolysis rather than the NADPH‐producing pentose phosphate pathway) and downregulated MaeB (a NADP <sup>+</sup> ‐dependent malate dehydrogenase). Overall, the results suggest that heterologous expression of NADH‐dependent FabG in E. coli may improve sustained production of fatty acid‐derived renewable fuels and chemicals.</span><a href='#' onclick='$(this).hide().prev().hide().prev().show();return false;' style='margin-left:10px;display:none;'>« less</a></div><div class="metadata-links small clearfix text-muted" style="margin-top:15px;"> <span class="fa fa-book text-muted" aria-hidden="true"></span> Cited by 12<div class="pure-menu pure-menu-horizontal pull-right" style="width:unset;"> <ul class="pure-menu-list"> <li class="pure-menu-item"><span class="item-info-ftlink"><a class="misc doi-link " href="https://doi.org/10.1002/bit.26558" target="_blank" rel="noopener" title="Link to document DOI" data-ostiid="1432073" data-product-type="Journal Article" data-product-subtype="PM" >https://doi.org/10.1002/bit.26558</a></span></li> </ul> </div> </div> </div> <div class="clearfix"></div> </div> </li> <li> <div class="article item document" itemprop="itemListElement" itemscope itemtype="http://schema.org/WebPage"><meta itemprop="position" content="4" /><div class="item-info"> <h2 class="title" itemprop="name headline"><a href="/pages/biblio/1631188-enhancing-photosynthetic-production-glycogen-rich-biomass-use-fermentation-feedstock" itemprop="url">Enhancing Photosynthetic Production of Glycogen-Rich Biomass for Use as a Fermentation Feedstock</a></h2> <div class="metadata"> <small class="text-muted" style="text-transform:uppercase;display:block;line-height:2.5em;">Journal Article</small><span class="authors"> <span class="author">Comer, Austin D.</span> ; <span class="author">Abraham, Joshua P.</span> ; <span class="author">Steiner, Alexander J.</span> ; <span class="author">...</span> <span class="text-muted pubdata"> - Frontiers in Energy Research</span> </span> </div> <div class="abstract">Current sources of fermentation feedstocks, i.e., corn, sugar cane, or plant biomass, fall short of demand for liquid transportation fuels and commodity chemicals in the United States. Aquatic phototrophs including cyanobacteria have the potential to supplement the supply of current fermentable feedstocks. In our strategy, cells are engineered to accumulate storage molecules including glycogen, cellulose, and/or lipid oils that can be extracted from harvested biomass and fed to heterotrophic organisms engineered to produce desired chemical products. Here in this manuscript, we examine the production of glycogen in the model cyanobacteria, Synechococcus sp. strain PCC 7002, and subsequent conversion of cyanobacterial<a href='#' onclick='$(this).hide().next().show().next().show();return false;' style='margin-left:10px;'>more »</a><span style='display:none;'> biomass by an engineered Escherichia coli to octanoic acid as a model product. In effort to maximize glycogen production, we explored the deletion of catabolic enzymes and overexpression of GlgC, an enzyme that catalyzes the first committed step toward glycogen synthesis. We found that deletion of glgP increased final glycogen titers when cells were grown in diurnal light. Overexpression of GlgC led to a temporal increase in glycogen content but not in an overall increase in final titer or content. The best strains were grown, harvested, and used to formulate media for growth of E. coli. The cyanobacterial media was able to support the growth of an engineered E. coli and produce octanoic acid at the same titer as common laboratory media.</span><a href='#' onclick='$(this).hide().prev().hide().prev().show();return false;' style='margin-left:10px;display:none;'>« less</a></div><div class="metadata-links small clearfix text-muted" style="margin-top:15px;"> <span class="fa fa-book text-muted" aria-hidden="true"></span> Cited by 8<div class="pure-menu pure-menu-horizontal pull-right" style="width:unset;"> <ul class="pure-menu-list"> <li class="pure-menu-item"><span class="item-info-ftlink"><a class="misc doi-link " href="https://doi.org/10.3389/fenrg.2020.00093" target="_blank" rel="noopener" title="Link to document DOI" data-ostiid="1631188" data-product-type="Journal Article" data-product-subtype="PA" >https://doi.org/10.3389/fenrg.2020.00093</a></span></li> </ul> </div> </div> </div> <div class="clearfix"></div> </div> </li> <li> <div class="article item document" itemprop="itemListElement" itemscope itemtype="http://schema.org/WebPage"><meta itemprop="position" content="5" /><div class="item-info"> <h2 class="title" itemprop="name headline"><a href="/pages/biblio/1213053-improving-microbial-biogasoline-production-escherichia-coli-using-tolerance-engineering" itemprop="url">Improving microbial biogasoline production in <i>Escherichia coli</i> using tolerance engineering</a></h2> <div class="metadata"> <small class="text-muted" style="text-transform:uppercase;display:block;line-height:2.5em;">Journal Article</small><span class="authors"> <span class="author">Foo, Jee Loon</span> ; <span class="author">Jensen, Heather M.</span> ; <span class="author">Dahl, Robert H.</span> ; <span class="author">...</span> <span class="text-muted pubdata"> - mBio (Online)</span> </span> </div> <div class="abstract">Engineering microbial hosts for the production of fungible fuels requires mitigation of limitations posed on the production capacity. One such limitation arises from the inherent toxicity of solvent-like biofuel compounds to production strains, such as <i>Escherichia coli</i>. Here we show the importance of host engineering for the production of short-chain alcohols by studying the overexpression of genes upregulated in response to exogenous isopentenol. Using systems biology data, we selected 40 genes that were upregulated following isopentenol exposure and subsequently overexpressed them in <i>E. coli</i>. Overexpression of several of these candidates improved tolerance to exogenously added isopentenol. Genes conferring isopentenol tolerance<a href='#' onclick='$(this).hide().next().show().next().show();return false;' style='margin-left:10px;'>more »</a><span style='display:none;'> phenotypes belonged to diverse functional groups, such as oxidative stress response (<i>soxS</i>, <i>fpr</i>, and <i>nrdH</i>), general stress response (<i>metR</i>, <i>yqhD</i>, and <i>gidB</i>), heat shock-related response (<i>ibpA</i>), and transport (<i>mdlB</i>). To determine if these genes could also improve isopentenol production, we coexpressed the tolerance-enhancing genes individually with an isopentenol production pathway. Our data show that expression of 6 of the 8 candidates improved the production of isopentenol in <i>E. coli</i>, with the methionine biosynthesis regulator MetR improving the titer for isopentenol production by 55%. Additionally, expression of MdlB, an ABC transporter, facilitated a 12% improvement in isopentenol production. To our knowledge, MdlB is the first example of a transporter that can be used to improve production of a short-chain alcohol and provides a valuable new avenue for host engineering in biogasoline production.The use of microbial host platforms for the production of bulk commodities, such as chemicals and fuels, is now a focus of many biotechnology efforts. Many of these compounds are inherently toxic to the host microbe, which in turn places a limit on production despite efforts to optimize the bioconversion pathways. In order to achieve economically viable production levels, it is also necessary to engineer production strains with improved tolerance to these compounds. We demonstrate that microbial tolerance engineering using transcriptomics data can also identify targets that improve production. Our results include an exporter and a methionine biosynthesis regulator that improve isopentenol production, providing a starting point to further engineer the host for biogasoline production.</span><a href='#' onclick='$(this).hide().prev().hide().prev().show();return false;' style='margin-left:10px;display:none;'>« less</a></div><div class="metadata-links small clearfix text-muted" style="margin-top:15px;"> <span class="fa fa-book text-muted" aria-hidden="true"></span> Cited by 88<div class="pure-menu pure-menu-horizontal pull-right" style="width:unset;"> <ul class="pure-menu-list"> <li class="pure-menu-item"><span class="item-info-ftlink"><a class="misc doi-link " href="https://doi.org/10.1128/mBio.01932-14" target="_blank" rel="noopener" title="Link to document DOI" data-ostiid="1213053" data-product-type="Journal Article" data-product-subtype="AM" >https://doi.org/10.1128/mBio.01932-14</a></span></li> <li class="pure-menu-item"><span class="item-info-ftlink"><a class="misc fulltext-link " href="/pages/servlets/purl/1213053" title="Link to document media" target="_blank" rel="noopener" data-ostiid="1213053" data-product-type="Journal Article" data-product-subtype="AM" >Full Text Available</a></span></li> </ul> </div> </div> </div> <div class="clearfix"></div> </div> </li> <li> <div class="article item document" itemprop="itemListElement" itemscope itemtype="http://schema.org/WebPage"><meta itemprop="position" content="8" /><div class="item-info"> <h2 class="title" itemprop="name headline"><a href="/pages/biblio/1604827-vivo-thermodynamic-analysis-glycolysis-clostridium-thermocellum-thermoanaerobacterium-saccharolyticum-using-tracers" itemprop="url"><em>In Vivo</em> Thermodynamic Analysis of Glycolysis in <em>Clostridium thermocellum</em> and <em>Thermoanaerobacterium saccharolyticum</em> Using <sup>13</sup> C and <sup>2</sup> H Tracers</a></h2> <div class="metadata"> <small class="text-muted" style="text-transform:uppercase;display:block;line-height:2.5em;">Journal Article</small><span class="authors"> <span class="author">Jacobson, Tyler B.</span> ; <span class="author">Korosh, Travis K.</span> ; <span class="author">Stevenson, David M.</span> ; <span class="author">...</span> <span class="text-muted pubdata"> - mSystems</span> </span> </div> <div class="abstract">Clostridium thermocellumandThermoanaerobacterium saccharolyticumare thermophilic anaerobic bacteria with complementary metabolic capabilities that utilize distinct glycolytic pathways for the conversion of cellulosic sugars to biofuels. We integrated quantitative metabolomics with <sup>2</sup>H and<sup>13</sup>C metabolic flux analysis to investigate the in vivo reversibility and thermodynamics of the central metabolic networks of these two microbes. We found that the glycolytic pathway in C. thermocellum operates remarkably close to thermodynamic equilibrium, with an overall drop in Gibbs free energy 5-fold lower than that of T. saccharolyticum or anaerobically grownEscherichia coli. The limited thermodynamic driving force of glycolysis in C. thermocellum could be attributed in large part<a href='#' onclick='$(this).hide().next().show().next().show();return false;' style='margin-left:10px;'>more »</a><span style='display:none;'> to the small free energy of the phosphofructokinase reaction producing fructose bisphosphate. The ethanol fermentation pathway was also substantially more reversible in C. thermocellummthan in T. saccharolyticum. These observations help explain the comparatively low ethanol titers of C. thermocellum and suggest engineering interventions that can be used to increase its ethanol productivity and glycolytic rate. In addition to thermodynamic analysis, we used our isotope tracer data to reconstruct the T. saccharolyticum central metabolic network, revealing exclusive use of the Embden-Meyerhof-Parnas (EMP) pathway for glycolysis, a bifurcated tricarboxylic acid (TCA) cycle, and a sedoheptulose bisphosphate bypass active within the pentose phosphate pathway. Thermodynamics constitutes a key determinant of flux and enzyme efficiency in metabolic networks. Here, we provide new insights into the divergent thermodynamics of the glycolytic pathways of C. thermocellum and T. saccharolyticum, two industrially relevant thermophilic bacteria whose metabolism still is not well understood. We report that while the glycolytic pathway in T. saccharolyticum is as thermodynamically favorable as that found in model organisms, such asE. coliorSaccharomyces cerevisiae, the glycolytic pathway of C. thermocellum operates near equilibrium. The use of a near-equilibrium glycolytic pathway, with potentially increased ATP yield, by this cellulolytic microbe may represent an evolutionary adaptation to growth on cellulose, but it has the drawback of being highly susceptible to product feedback inhibition. The results of this study will facilitate future engineering of high-performance strains capable of transforming cellulosic biomass to biofuels at high yields and titers.</span><a href='#' onclick='$(this).hide().prev().hide().prev().show();return false;' style='margin-left:10px;display:none;'>« less</a></div><div class="metadata-links small clearfix text-muted" style="margin-top:15px;"> <span class="fa fa-book text-muted" aria-hidden="true"></span> Cited by 26<div class="pure-menu pure-menu-horizontal pull-right" style="width:unset;"> <ul class="pure-menu-list"> <li class="pure-menu-item"><span class="item-info-ftlink"><a class="misc doi-link " href="https://doi.org/10.1128/mSystems.00736-19" target="_blank" rel="noopener" title="Link to document DOI" data-ostiid="1604827" data-product-type="Journal Article" data-product-subtype="PA" >https://doi.org/10.1128/mSystems.00736-19</a></span></li> </ul> </div> </div> </div> <div class="clearfix"></div> </div> </li> </ul> </aside> </div> </section> </div> <div class="col-sm-3 order-sm-3"> <ul class="nav nav-stacked"> <li class="active"><a class="tab-nav disabled" data-tab="related" style="color: #636c72 !important; opacity: 1;"><span class="fa fa-angle-right"></span> Similar Records</a></li> </ul> </div> </div> </section> </div></div> </div> </div> </section> <footer class="" style="background-color:#f9f9f9;"> <div class="footer-minor"> <div class="container"> <hr class="footer-separator"/> <br/> <div class="col text-center mt-3"> <div class="pure-menu pure-menu-horizontal"> <ul class="pure-menu-list" id="footer-org-menu"> <li class="pure-menu-item"> <a href="https://energy.gov" target="_blank" rel="noopener noreferrer"> <img src="data:image/gif;base64,R0lGODlhAQABAIAAAP///wAAACH5BAEAAAAALAAAAAABAAEAAAICRAEAOw==" class="sprite sprite-footer-us-doe-min" alt="U.S. Department of Energy" /> </a> </li> <li class="pure-menu-item"> <a href="https://www.energy.gov/science/office-science" target="_blank" rel="noopener noreferrer"> <img src="data:image/gif;base64,R0lGODlhAQABAIAAAP///wAAACH5BAEAAAAALAAAAAABAAEAAAICRAEAOw==" class="sprite sprite-footer-office-of-science-min" alt="Office of Science" /> </a> </li> <li class="pure-menu-item"> <a href="https://www.osti.gov" target="_blank" rel="noopener noreferrer"> <img src="data:image/gif;base64,R0lGODlhAQABAIAAAP///wAAACH5BAEAAAAALAAAAAABAAEAAAICRAEAOw==" class="sprite sprite-footer-osti-min" alt="Office of Scientific and Technical Information" /> </a> </li> </ul> </div> </div> <div class="col text-center small" style="margin-top: 0.5em;margin-bottom:2.0rem;"> <div class="row justify-content-center" style="color:white"> <div class="pure-menu pure-menu-horizontal" style='white-space:normal'> <ul class="pure-menu-list"> <li class="pure-menu-item"><a href="https://www.osti.gov/disclaim" class="pure-menu-link" target="_blank" ref="noopener noreferrer"><span class="fa fa-institution"></span> Website Policies <span class="d-none d-sm-inline d-print-none" style="color:#737373;">/ Important Links</span></a></li> <li class="pure-menu-item" style='float:none;'><a href="/pages/contact" class="pure-menu-link"><span class="fa fa-comments-o"></span>Contact Us</a></li> <li class="d-block d-md-none mb-1"></li> <li class="pure-menu-item" style='float:none;'><a target="_blank" title="Vulnerability Disclosure Program" class="pure-menu-link" href="https://doe.responsibledisclosure.com/hc/en-us" rel="noopener noreferrer">Vulnerability Disclosure Program</a></li> <li class="d-block d-lg-none mb-1"></li> <li class="pure-menu-item" style="float:none;"><a href="https://www.facebook.com/ostigov" target="_blank" class="pure-menu-link social ext fa fa-facebook" rel="noopener noreferrer"><span class="sr-only" style="background-color: #fff; color: #333;">Facebook</span></a></li> <li class="pure-menu-item" style="float:none;"><a href="https://twitter.com/OSTIgov" target="_blank" class="pure-menu-link social ext fa fa-twitter" rel="noopener noreferrer"><span class="sr-only" style="background-color: #fff; color: #333;">Twitter</span></a></li> <li class="pure-menu-item" style="float:none;"><a href="https://www.youtube.com/user/ostigov" target="_blank" class="pure-menu-link social ext fa fa-youtube-play" rel="noopener noreferrer"><span class="sr-only" style="background-color: #fff; color: #333;">Youtube</span></a></li> </ul> </div> </div> </div> </div> </div> </footer> <link href="/pages/css/pages.fonts.240327.0205.css" rel="stylesheet"> <script src="/pages/js/pages.240327.0205.js"></script><noscript></noscript> <script defer src="/pages/js/pages.biblio.240327.0205.js"></script><noscript></noscript> <script defer src="/pages/js/lity.js"></script><noscript></noscript> <script async type="text/javascript" src="/pages/js/Universal-Federated-Analytics-Min.js?agency=DOE" id="_fed_an_ua_tag"></script><noscript></noscript> </body>  </html>

Title: A minimum information standard for reproducing bench-scale bacterial cell growth and productivity

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Figures / Tables:

Response of Escherichia coli growth rate to osmotic shock journal, May 2014

High-Level Production of the Industrial Product Lycopene by the Photosynthetic Bacterium Rhodospirillum rubrum journal, August 2012

Correlation for the maximum oxygen transfer capacity in shake flasks for a wide range of operating conditions and for different culture media journal, May 2016

Growth of E. coli BL21 in minimal media with different gluconeogenic carbon sources and salt contents journal, August 2006

Bacteriocin production by Bacillus licheniformis strain P40 in cheese whey using response surface methodology journal, September 2004

Standards for systems biology journal, August 2006

Rapid Evaluation of Oxygen and Water Permeation through Microplate Sealing Tapes journal, June 2003

R Package FrF2 for Creating and Analyzing Fractional Factorial 2-Level Designs journal, January 2014

Testing plasmid stability of Escherichia coli using the Continuously Operated Shaken BIOreactor System journal, September 2016

1,500 scientists lift the lid on reproducibility journal, May 2016

Minimum information about a microarray experiment (MIAME)—toward standards for microarray data journal, December 2001

Methods for Intense Aeration, Growth, Storage, and Replication of Bacterial Strains in Microtiter Plates journal, June 2000

An approach to integrated data assessment in a proficiency test on the enumeration of Escherichia coli: Assessment of PT data for E. coli enumeration journal, November 2010

Oxygen supply in disposable shake-flasks: prediction of oxygen transfer rate, oxygen saturation and maximum cell concentration during aerobic growth journal, April 2013

Foundations for engineering biology journal, November 2005

Characterisation of operation conditions and online monitoring of physiological culture parameters in shaken 24-well microtiter plates journal, October 2005

The MIQE Guidelines: Minimum Information for Publication of Quantitative Real-Time PCR Experiments journal, February 2009

Guidelines for evaluating and expressing the uncertainty of NIST measurement results report, January 1994

Measuring the activity of BioBrick promoters using an in vivo reference standard journal, January 2009

Characterization of oxygen transfer conditions and their effects on Phaffia rhodozyma growth and carotenoid production in shake-flask cultures journal, January 2006

Wet Lab Accelerator: A Web-Based Application Democratizing Laboratory Automation for Synthetic Biology journal, September 2016

The Synthetic Biology Open Language (SBOL) provides a community standard for communicating designs in synthetic biology journal, June 2014

A Strategy Capitalizing on Synergies: The Reporting Structure for Biological Investigation (RSBI) Working Group journal, June 2006

Metabolic Burden: Cornerstones in Synthetic Biology and Metabolic Engineering Applications journal, August 2016

Medium-dependent control of the bacterial growth rate journal, April 2013

Reproducibility of Fluorescent Expression from Engineered Biological Constructs in E. coli journal, March 2016

Reproducibility of High-Throughput Plate-Reader Experiments in Synthetic Biology journal, November 2016

Lessons from the organization of a proficiency testing program in food microbiology by interlaboratory comparison: Analytical methods in use, impact of methods on bacterial counts and measurement uncertainty of bacterial counts journal, February 2006

Molecular structure and enzymatic function of lycopene cyclase from the cyanobacterium Synechococcus sp strain PCC7942. journal, August 1994

Oxygen transfer rates in shaken culture vessels from Fernbach flasks to microtiter plates: Oxygen Transfer Rates in Shaken Culture Vessels journal, February 2016

Assessment of measurement uncertainty for quantitative methods of analysis: Comparative assessment of the precision (uncertainty) of bacterial colony counts journal, May 2007

The baffled microtiter plate: Increased oxygen transfer and improved online monitoring in small scale fermentations journal, August 2009

Precise and reliable gene expression via standard transcription and translation initiation elements journal, March 2013

Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli journal, June 2009

Liquid films on shake flask walls explain increasing maximum oxygen transfer capacities with elevating viscosity: Liquid Films on Shake Flask Walls journal, August 2013

A fast, robust and tunable synthetic gene oscillator journal, October 2008

Characterization of gas-liquid mass transfer phenomena in microtiter plates: Gas-Liquid Mass Transfer in Microtiter Plates journal, November 2002

Oxygen transfer by orbital shaking of square vessels and deepwell microtiter plates of various dimensions journal, March 2004

Effects of Freezing, Freeze-Drying, and Storage in the Freeze-Dried and Frozen State on Viability of Escherichia coli Cells journal, February 1961

Framework for the Rapid Optimization of Soluble Protein Expression in Escherichia coli Combining Microscale Experiments and Statistical Experimental Design journal, August 2007

Disposable bioreactors: the current state-of-the-art and recommended applications in biotechnology journal, January 2010

Operating Conditions That Affect the Resistance of Lactic Acid Bacteria to Freezing and Frozen Storage journal, November 2001

pH Regulates Genes for Flagellar Motility, Catabolism, and Oxidative Stress in Escherichia coli K-12 journal, December 2004

Protein production by auto-induction in high-density shaking cultures journal, May 2005

Synthetic biology: new engineering rules for an emerging discipline journal, January 2006

Optimization of recombinant aminolevulinate synthase production in Escherichia coli using factorial design journal, December 2003

Top-down standards will not serve systems biology journal, March 2006

Suitability of the shaking flask for oxygen supply to microbiological cultures journal, November 1991

Recombinant bromelain production in Escherichia coli: process optimization in shake flask culture by response surface methodology journal, January 2012

Oxygen transfer phenomena in 48-well microtiter plates: Determination by optical monitoring of sulfite oxidation and verification by real-time measurement during microbial growth: Oxygen Transfer Phenomena in 48-Well MTP journal, February 2005

The minimum information about a genome sequence (MIGS) specification journal, May 2008

Correlation between mass transfer coefficient kLa and relevant operating parameters in cylindrical disposable shaken bioreactors on a bench-to-pilot scale journal, January 2013

A minimum information standard for reproducing bench-scale cell growth and productivity dataset, January 2018

Response of Escherichia coli growth rate to osmotic shock
journal, May 2014

High-Level Production of the Industrial Product Lycopene by the Photosynthetic Bacterium Rhodospirillum rubrum
journal, August 2012

Correlation for the maximum oxygen transfer capacity in shake flasks for a wide range of operating conditions and for different culture media
journal, May 2016

Growth of E. coli BL21 in minimal media with different gluconeogenic carbon sources and salt contents
journal, August 2006

Bacteriocin production by Bacillus licheniformis strain P40 in cheese whey using response surface methodology
journal, September 2004

Standards for systems biology
journal, August 2006

Rapid Evaluation of Oxygen and Water Permeation through Microplate Sealing Tapes
journal, June 2003

R Package FrF2 for Creating and Analyzing Fractional Factorial 2-Level Designs
journal, January 2014

Testing plasmid stability of Escherichia coli using the Continuously Operated Shaken BIOreactor System
journal, September 2016

1,500 scientists lift the lid on reproducibility
journal, May 2016

Minimum information about a microarray experiment (MIAME)—toward standards for microarray data
journal, December 2001

Methods for Intense Aeration, Growth, Storage, and Replication of Bacterial Strains in Microtiter Plates
journal, June 2000

An approach to integrated data assessment in a proficiency test on the enumeration of Escherichia coli: Assessment of PT data for E. coli enumeration
journal, November 2010

Oxygen supply in disposable shake-flasks: prediction of oxygen transfer rate, oxygen saturation and maximum cell concentration during aerobic growth
journal, April 2013

Foundations for engineering biology
journal, November 2005

Characterisation of operation conditions and online monitoring of physiological culture parameters in shaken 24-well microtiter plates
journal, October 2005

The MIQE Guidelines: Minimum Information for Publication of Quantitative Real-Time PCR Experiments
journal, February 2009

Guidelines for evaluating and expressing the uncertainty of NIST measurement results
report, January 1994

Measuring the activity of BioBrick promoters using an in vivo reference standard
journal, January 2009

Characterization of oxygen transfer conditions and their effects on Phaffia rhodozyma growth and carotenoid production in shake-flask cultures
journal, January 2006

Wet Lab Accelerator: A Web-Based Application Democratizing Laboratory Automation for Synthetic Biology
journal, September 2016

The Synthetic Biology Open Language (SBOL) provides a community standard for communicating designs in synthetic biology
journal, June 2014

A Strategy Capitalizing on Synergies: The Reporting Structure for Biological Investigation (RSBI) Working Group
journal, June 2006

Metabolic Burden: Cornerstones in Synthetic Biology and Metabolic Engineering Applications
journal, August 2016

Medium-dependent control of the bacterial growth rate
journal, April 2013

Reproducibility of Fluorescent Expression from Engineered Biological Constructs in E. coli
journal, March 2016

Reproducibility of High-Throughput Plate-Reader Experiments in Synthetic Biology
journal, November 2016

Lessons from the organization of a proficiency testing program in food microbiology by interlaboratory comparison: Analytical methods in use, impact of methods on bacterial counts and measurement uncertainty of bacterial counts
journal, February 2006

Molecular structure and enzymatic function of lycopene cyclase from the cyanobacterium Synechococcus sp strain PCC7942.
journal, August 1994

Oxygen transfer rates in shaken culture vessels from Fernbach flasks to microtiter plates: Oxygen Transfer Rates in Shaken Culture Vessels
journal, February 2016

Assessment of measurement uncertainty for quantitative methods of analysis: Comparative assessment of the precision (uncertainty) of bacterial colony counts
journal, May 2007

The baffled microtiter plate: Increased oxygen transfer and improved online monitoring in small scale fermentations
journal, August 2009

Precise and reliable gene expression via standard transcription and translation initiation elements
journal, March 2013

Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli
journal, June 2009

Liquid films on shake flask walls explain increasing maximum oxygen transfer capacities with elevating viscosity: Liquid Films on Shake Flask Walls
journal, August 2013

A fast, robust and tunable synthetic gene oscillator
journal, October 2008

Characterization of gas-liquid mass transfer phenomena in microtiter plates: Gas-Liquid Mass Transfer in Microtiter Plates
journal, November 2002

Oxygen transfer by orbital shaking of square vessels and deepwell microtiter plates of various dimensions
journal, March 2004

Effects of Freezing, Freeze-Drying, and Storage in the Freeze-Dried and Frozen State on Viability of Escherichia coli Cells
journal, February 1961

Framework for the Rapid Optimization of Soluble Protein Expression in Escherichia coli Combining Microscale Experiments and Statistical Experimental Design
journal, August 2007

Disposable bioreactors: the current state-of-the-art and recommended applications in biotechnology
journal, January 2010

Operating Conditions That Affect the Resistance of Lactic Acid Bacteria to Freezing and Frozen Storage
journal, November 2001

pH Regulates Genes for Flagellar Motility, Catabolism, and Oxidative Stress in Escherichia coli K-12
journal, December 2004

Protein production by auto-induction in high-density shaking cultures
journal, May 2005

Synthetic biology: new engineering rules for an emerging discipline
journal, January 2006

Optimization of recombinant aminolevulinate synthase production in Escherichia coli using factorial design
journal, December 2003

Top-down standards will not serve systems biology
journal, March 2006

Suitability of the shaking flask for oxygen supply to microbiological cultures
journal, November 1991

Recombinant bromelain production in Escherichia coli: process optimization in shake flask culture by response surface methodology
journal, January 2012

Oxygen transfer phenomena in 48-well microtiter plates: Determination by optical monitoring of sulfite oxidation and verification by real-time measurement during microbial growth: Oxygen Transfer Phenomena in 48-Well MTP
journal, February 2005

The minimum information about a genome sequence (MIGS) specification
journal, May 2008

Correlation between mass transfer coefficient kLa and relevant operating parameters in cylindrical disposable shaken bioreactors on a bench-to-pilot scale
journal, January 2013

A minimum information standard for reproducing bench-scale cell growth and productivity
dataset, January 2018