Mismatch-CRISPRi Reveals the Co-varying Expression-Fitness Relationships of Essential Genes in Escherichia coli and Bacillus subtilis

Alkan, 2018, CRISPR-Cas9 off-targeting assessment with nucleic acid duplex energy parameters, Genome Biol, 19, 177, 10.1186/s13059-018-1534-x Baba, 2006, Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection, Molecular Systems Biology, 10.1038/msb4100050 Barreteau, 2008, Cytoplasmic steps of peptidoglycan biosynthesis, FEMS Microbiol. Rev., 32, 168, 10.1111/j.1574-6976.2008.00104.x Bauer, 2015, Essential gene disruptions reveal complex relationships between phenotypic robustness, pleiotropy, and fitness, Mol. Syst. Biol., 11, 773, 10.15252/msb.20145264 Bhattacharyya, 2016, Transient protein-protein interactions perturb E. coli metabolome and cause gene dosage toxicity, eLife, 5, 10.7554/eLife.20309 Bobrovskyy, 2016, Diverse mechanisms of post-transcriptional repression by the small RNA regulator of glucose-phosphate stress, Mol. Microbiol., 99, 254, 10.1111/mmi.13230 Borkowski, 2016, Translation elicits a growth rate-dependent, genome-wide, differential protein production in Bacillus subtilis, Mol. Syst. Biol., 12, 870, 10.15252/msb.20156608 Boy, 1972, Multivalent repression of aspartic semialdehyde dehydrogenase in Escherichia coli K-12, J. Bacteriol., 112, 84, 10.1128/jb.112.1.84-92.1972 Boyle, 2017, High-throughput biochemical profiling reveals sequence determinants of dCas9 off-target binding and unbinding, Proc. Natl. Acad. Sci. USA, 114, 5461, 10.1073/pnas.1700557114 Bustin, 2009, The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments, Clin. Chem., 55, 611, 10.1373/clinchem.2008.112797 Calvo-Villamañán, 2020, On-target activity predictions enable improved CRISPR-dCas9 screens in bacteria, Nucleic Acids Res, 48, e64, 10.1093/nar/gkaa294 Christodoulou, 2018, Reserve flux capacity in the pentose phosphate pathway enables Escherichia coli’s rapid response to oxidative stress, Cell Syst, 6, 569, 10.1016/j.cels.2018.04.009 Cui, 2018, A CRISPRi screen in E. coli reveals sequence-specific toxicity of dCas9, Nat. Commun., 9, 1912, 10.1038/s41467-018-04209-5 Dai, 2016, Reduction of translating ribosomes enables Escherichia coli to maintain elongation rates during slow growth, Nat. Microbiol., 2, 16231, 10.1038/nmicrobiol.2016.231 Datsenko, 2000, One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products, Proc. Natl. Acad. Sci. USA, 97, 6640, 10.1073/pnas.120163297 Dekel, 2005, Optimality and evolutionary tuning of the expression level of a protein, Nature, 436, 588, 10.1038/nature03842 Eames, 2012, Cost-benefit tradeoffs in engineered lac operons, Science, 336, 911, 10.1126/science.1219083 Fransen, 2017, Pharmacodynamics of fosfomycin against ESBL- and/or carbapenemase-producing Enterobacteriaceae, J. Antimicrob. Chemother., 72, 3374, 10.1093/jac/dkx328 Gilbert, 2014, Genome-scale CRISPR-mediated control of gene repression and activation, Cell, 159, 647, 10.1016/j.cell.2014.09.029 Gilbert, 2013, CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes, Cell, 154, 442, 10.1016/j.cell.2013.06.044 Gong, 2018, DNA unwinding is the primary determinant of CRISPR-Cas9 activity, Cell Rep., 22, 359, 10.1016/j.celrep.2017.12.041 Harris, 2016, Relative rates of surface and volume synthesis set bacterial cell size, Cell, 165, 1479, 10.1016/j.cell.2016.05.045 Hellemans, 2007, qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data, Genome Biol., 8, R19, 10.1186/gb-2007-8-2-r19 Johnson, 2019, Large-scale chemical-genetics yields new M. tuberculosis inhibitor classes, Nature, 571, 72, 10.1038/s41586-019-1315-z Johnson, 2013, Bacterial cell-wall recycling, Ann. N. Y. Acad. Sci., 1277, 54, 10.1111/j.1749-6632.2012.06813.x Jost, 2020, Titrating gene expression using libraries of systematically attenuated CRISPR guide RNAs, Nat. Biotechnol., 38, 355, 10.1038/s41587-019-0387-5 Kahan, 1974, The mechanism of action of fosfomycin (phosphonomycin), Ann. N. Y. Acad. Sci., 235, 364, 10.1111/j.1749-6632.1974.tb43277.x Kampmann, 2013, Integrated platform for genome-wide screening and construction of high-density genetic interaction maps in mammalian cells, Proc. Natl. Acad. Sci. USA, 110, E2317, 10.1073/pnas.1307002110 Keren, 2016, Massively parallel interrogation of the effects of gene expression levels on fitness, Cell, 166, 1282, 10.1016/j.cell.2016.07.024 Kim, 2013, A novel balanced-lethal host-vector system based on glmS, PLoS One, 8 Koo, 2017, Construction and analysis of two genome-scale deletion libraries for Bacillus subtilis, Cell Syst, 4, 291, 10.1016/j.cels.2016.12.013 Lalanne, 2018, Evolutionary convergence of pathway-specific enzyme expression stoichiometry, Cell, 173, 749, 10.1016/j.cell.2018.03.007 Langmead, 2012, Fast gapped-read alignment with Bowtie 2, Nature Methods, 9, 357, 10.1038/nmeth.1923 Langmead, 2009, Ultrafast and memory-efficient alignment of short DNA sequences to the human genome, Genome Biol, 10, R25, 10.1186/gb-2009-10-3-r25 Liu, 2017, High-throughput CRISPRi phenotyping identifies new essential genes in Streptococcus pneumoniae, Mol. Syst. Biol., 13, 931, 10.15252/msb.20167449 Lutz, 1997, Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements, Nucleic Acids Res, 25, 1203, 10.1093/nar/25.6.1203 McLennan, 1998, GroE is vital for cell-wall synthesis, Nature, 392, 139, 10.1038/32317 Mengin-Lecreulx, 1991, The murG gene of Escherichia coli codes for the UDP-N-acetylglucosamine: N-acetylmuramyl-(pentapeptide) pyrophosphoryl-undecaprenol N-acetylglucosamine transferase involved in the membrane steps of peptidoglycan synthesis, J. Bacteriol., 173, 4625, 10.1128/jb.173.15.4625-4636.1991 Mengin-Lecreulx, 1985, Effect of growth conditions on peptidoglycan content and cytoplasmic steps of its biosynthesis in Escherichia coli, J. Bacteriol., 163, 208, 10.1128/jb.163.1.208-212.1985 Nichols, 2011, Phenotypic landscape of a bacterial cell, Cell, 144, 143, 10.1016/j.cell.2010.11.052 Nomura, 1980, Feedback regulation of ribosomal protein gene expression in Escherichia coli: structural homology of ribosomal RNA and ribosomal protein MRNA, Proc. Natl. Acad. Sci. USA, 77, 7084, 10.1073/pnas.77.12.7084 Ogura, 1999, Balanced biosynthesis of major membrane components through regulated degradation of the committed enzyme of lipid A biosynthesis by the AAA protease FtsH (HflB) in Escherichia coli, Mol. Microbiol., 31, 833, 10.1046/j.1365-2958.1999.01221.x Peters, 2016, A comprehensive, CRISPR-based functional analysis of essential genes in bacteria, Cell, 165, 1493, 10.1016/j.cell.2016.05.003 Peters, 2019, Enabling genetic analysis of diverse bacteria with Mobile-CRISPRi, Nat. Microbiol., 4, 244, 10.1038/s41564-018-0327-z Qi, 2013, Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression, Cell, 152, 1173, 10.1016/j.cell.2013.02.022 Radeck, 2013, The Bacillus BioBrick Box: generation and evaluation of essential genetic building blocks for standardized work with Bacillus subtilis, Journal of Biological Engineering, 7, 10.1186/1754-1611-7-29 Rancati, 2018, Emerging and evolving concepts in gene essentiality, Nat. Rev. Genet., 19, 34, 10.1038/nrg.2017.74 Rauch, 2017, Inhibition of CRISPR-Cas9 with bacteriophage proteins, Cell, 168, 150, 10.1016/j.cell.2016.12.009 Reis, 2019, Simultaneous repression of multiple bacterial genes using nonrepetitive extra-long sgRNA arrays, Nat. Biotechnol., 37, 1294, 10.1038/s41587-019-0286-9 Rest, 2013, Nonlinear fitness consequences of variation in expression level of a eukaryotic gene, Mol. Biol. Evol., 30, 448, 10.1093/molbev/mss248 Reverend, 1982, Improvement of Escherichia coli strains overproducing lysine using recombinant DNA techniques, European J. Appl. Microbiol. Biotechnol., 15, 227, 10.1007/BF00499961 Rock, 2017, Programmable transcriptional repression in mycobacteria using an orthogonal CRISPR interference platform, Nat. Microbiol., 2, 16274, 10.1038/nmicrobiol.2016.274 Rodionov, 2003, Regulation of lysine biosynthesis and transport genes in bacteria: yet another RNA riboswitch?, Nucleic Acids Res, 31, 6748, 10.1093/nar/gkg900 Rousset, 2018, Genome-wide CRISPR-dCas9 screens in E. coli identify essential genes and phage host factors, PLoS Genet, 14, 10.1371/journal.pgen.1007749 Schaechter, 1958, Dependency on medium and temperature of cell size and chemical composition during balanced grown of Salmonella typhimurium, J. Gen. Microbiol., 19, 592, 10.1099/00221287-19-3-592 Scott, 2010, Interdependence of cell growth and gene expression: origins and consequences, Science, 330, 1099, 10.1126/science.1192588 Scott, 2014, Emergence of robust growth laws from optimal regulation of ribosome synthesis, Mol. Syst. Biol., 10, 747, 10.15252/msb.20145379 Thomason, 2007, E. coli genome manipulation by P1 transduction, Curr. Protoc. Mol. Biol., 79, 10.1002/0471142727.mb0117s79 Thomason, 2014, Recombineering: genetic engineering in bacteria using homologous recombination, Curr. Protoc. Mol. Biol., 106, 10.1002/0471142727.mb0116s106 Urban, 2008, Two seemingly homologous noncoding RNAs act hierarchically to activate glmS mRNA translation, PLoS Biol, 6, e64, 10.1371/journal.pbio.0060064 Vigouroux, 2018, Tuning dCas9’s ability to block transcription enables robust, noiseless knockdown of bacterial genes, Mol. Syst. Biol., 14, e7899, 10.15252/msb.20177899 Wang, 2018, Pooled CRISPR interference screening enables genome-scale functional genomics study in bacteria with superior performance, Nat. Commun., 9, 2475, 10.1038/s41467-018-04899-x Zheng, 2008, Genetic analysis of MraY inhibition by the phiX174 protein, E. Genetics, 180, 1459