1932

Abstract

The ability to detect disease early and deliver precision therapy would be transformative for the treatment of human illnesses. To achieve these goals, biosensors that can pinpoint when and where diseases emerge are needed. Rapid advances in synthetic biology are enabling us to exploit the information-processing abilities of living cells to diagnose disease and then treat it in a controlled fashion. For example, living sensors could be designed to precisely sense disease biomarkers, such as by-products of inflammation, and to respond by delivering targeted therapeutics in situ. Here, we provide an overview of ongoing efforts in microbial biosensor design, highlight translational opportunities, and discuss challenges for enabling sense-and-respond precision medicines.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-micro-022620-081059
2020-09-08
2024-10-12
Loading full text...

Full text loading...

/deliver/fulltext/micro/74/1/annurev-micro-022620-081059.html?itemId=/content/journals/10.1146/annurev-micro-022620-081059&mimeType=html&fmt=ahah

Literature Cited

  1. 1. 
    Abbas M, Matta J, Le T, Bensmail H, Obafemi-Ajayi T et al. 2019. Biomarker discovery in inflammatory bowel diseases using network-based feature selection. PLOS ONE 14:11e0225382
    [Google Scholar]
  2. 2. 
    Abil Z, Ellefson JW, Gollihar JD, Watkins E, Ellington AD 2017. Compartmentalized partnered replication for the directed evolution of genetic parts and circuits. Nat. Protoc. 12:2493–512
    [Google Scholar]
  3. 3. 
    Adames NR, Wilson ML, Fang G, Lux MW, Glick BS, Peccoud J 2015. GenoLIB: a database of biological parts derived from a library of common plasmid features. Nucleic Acids Res 43:104823–32
    [Google Scholar]
  4. 4. 
    Adeniran A, Stainbrook S, Bostick JW, Tyo KEJ 2018. Detection of a peptide biomarker by engineered yeast receptors. ACS Synth. Biol. 7:2696–705
    [Google Scholar]
  5. 5. 
    Appleton E. 2016. A design-build-test-learn tool for synthetic biology PhD Diss., Boston Univ Boston:
    [Google Scholar]
  6. 6. 
    Archer EJ, Robinson AB, Süel GM 2012. Engineered E. coli that detect and respond to gut inflammation through nitric oxide sensing. ACS Synth. Biol. 1:10451–57
    [Google Scholar]
  7. 7. 
    Aslan S, Noor E, Benito Vaquerizo S, Lindner SN, Bar-Even A 2020. Design and engineering of E. coli metabolic sensor strains with a wide sensitivity range for glycerate. Metab. Eng. 57:96–109
    [Google Scholar]
  8. 8. 
    Ausländer S, Ausländer D, Fussenegger M 2017. Synthetic biology—the synthesis of biology. Angew. Chem. Int. Ed. 56:236396–419
    [Google Scholar]
  9. 9. 
    Barger N, Litovco P, Li X, Habib M, Daniel R 2019. Synthetic metabolic computation in a bioluminescence-sensing system. Nucleic Acids Res 47:1910464–74
    [Google Scholar]
  10. 10. 
    Basu S, Mehreja R, Thiberge S, Chen M, Weiss R 2004. Spatiotemporal control of gene expression with pulse-generating networks. PNAS 101:176355–60
    [Google Scholar]
  11. 11. 
    Bereza-Malcolm LT, Mann G, Franks AE 2015. Environmental sensing of heavy metals through whole cell microbial biosensors: a synthetic biology approach. ACS Synth. Biol. 4:5535–46
    [Google Scholar]
  12. 12. 
    Bourdeau RW, Lee-Gosselin A, Lakshmanan A, Farhadi A, Kumar SR et al. 2018. Acoustic reporter genes for noninvasive imaging of microorganisms in mammalian hosts. Nature 553:768686–90
    [Google Scholar]
  13. 13. 
    Boyapati RK, Kalla R, Satsangi J, Ho GT 2016. Biomarkers in search of precision medicine in IBD. Am. J. Gastroenterol. 111:121682–90
    [Google Scholar]
  14. 14. 
    Ceroni F, Algar R, Stan G-B, Ellis T 2015. Quantifying cellular capacity identifies gene expression designs with reduced burden. Nat. Methods 12:5415–18
    [Google Scholar]
  15. 15. 
    Chang H, Mayonove P, Zavala A, De Visch A, Minard P et al. 2018. A modular receptor platform to expand the sensing repertoire of bacteria. ACS Synth. Biol. 7:1166–75
    [Google Scholar]
  16. 16. 
    Cleynen I, Boucher G, Jostins L, Schumm LP, Zeissig S et al. 2016. Inherited determinants of Crohn's disease and ulcerative colitis phenotypes: a genetic association study. Lancet 387:10014156–67
    [Google Scholar]
  17. 17. 
    Courbet A, Endy D, Renard E, Molina F, Bonnet J 2015. Detection of pathological biomarkers in human clinical samples via amplifying genetic switches and logic gates. Sci. Transl. Med. 7:289289ra83
    [Google Scholar]
  18. 18. 
    Crook N, Ferreiro A, Gasparrini AJ, Pesesky MW, Gibson MK et al. 2019. Adaptive strategies of the candidate probiotic E. coli Nissle in the mammalian gut. Cell Host Microbe 25:4499–512.e8
    [Google Scholar]
  19. 19. 
    Daeffler KN, Galley JD, Sheth RU, Ortiz‐Velez LC, Bibb CO et al. 2017. Engineering bacterial thiosulfate and tetrathionate sensors for detecting gut inflammation. Mol. Syst. Biol. 13:4923
    [Google Scholar]
  20. 20. 
    Daniel R, Rubens JR, Sarpeshkar R, Lu TK 2013. Synthetic analog computation in living cells. Nature 497:7451619–23
    [Google Scholar]
  21. 21. 
    Danino T, Kwong GA, Skalak M, Allen K, Bhatia SN et al. 2015. Programmable probiotics for detection of cancer in urine. Sci. Transl. Med. 7:289289ra84
    [Google Scholar]
  22. 22. 
    de Marco A, Vigh L, Diamant S, Goloubinoff P 2005. Native folding of aggregation-prone recombinant proteins in Escherichia coli by osmolytes, plasmid- or benzyl alcohol-overexpressed molecular chaperones. Cell Stress Chaperones 10:4329–39
    [Google Scholar]
  23. 23. 
    Donaldson GP, Lee SM, Mazmanian SK 2016. Gut biogeography of the bacterial microbiota. Nat. Rev. Microbiol. 14:120–32
    [Google Scholar]
  24. 24. 
    Fajardo-Cavazos P, Waters SM, Schuerger AC, George S, Marois JJ, Nicholson WL 2012. Evolution of Bacillussubtilis to enhanced growth at low pressure: up-regulated transcription of des-desKR, encoding the fatty acid desaturase system. Astrobiology 12:3258–70
    [Google Scholar]
  25. 25. 
    Farzadfard AF, Gharaei N, Higashikuni Y, Jung G 2018. Single-nucleotide-resolution computing and memory in living cells. Mol. Cell 75:4769–80.e4
    [Google Scholar]
  26. 26. 
    Farzadfard F, Lu TK. 2014. Genomically encoded analog memory with precise in vivo DNA writing in living cell populations. Science 346:62111256272
    [Google Scholar]
  27. 27. 
    Farzadfard F, Lu TK. 2018. Emerging applications for DNA writers and molecular recorders. Science 361:6405870–75
    [Google Scholar]
  28. 28. 
    Fernandez-Rodriguez J, Moser F, Song M, Voigt CA 2017. Engineering RGB color vision into Escherichia coli. Nat. Chem. Biol 13:7706–8
    [Google Scholar]
  29. 29. 
    Friedland AE, Lu TK, Wang X, Shi D, Church G, Collins JJ 2009. Synthetic gene networks that count. Science 324:59311199–202
    [Google Scholar]
  30. 30. 
    Gaudelli NM, Komor AC, Rees HA, Packer MS, Badran AH et al. 2017. Programmable base editing of A·T to G·C in genomic DNA without DNA cleavage. Nature 551:7681464–71
    [Google Scholar]
  31. 31. 
    Gilbert C, Tang TC, Ott W, Dorr BA, Shaw WM et al. 2019. Living materials with programmable functionalities grown from engineered microbial co-cultures. bioRxiv 2019.12.20.882472. https://doi.org/10.1101/2019.12.20.882472
    [Crossref]
  32. 32. 
    Gorochowski TE, van den Berg E, Kerkman R, Roubos JA, Bovenberg RAL 2014. Using synthetic biological parts and microbioreactors to explore the protein expression characteristics of Escherichia coli. ACS Synth. Biol 3:3129–39
    [Google Scholar]
  33. 33. 
    Groner B. 2016. “Signal Transduction: Principles, Pathways, and Processes. ,” edited by Lewis C. Cantley, Tony Hunter, Richard Sever, and Jeremy Thorner Q. Rev. Biol 91193–94
    [Google Scholar]
  34. 34. 
    Han L, Cui W, Suo F, Miao S, Hao W et al. 2019. Development of a novel strategy for robust synthetic bacterial promoters based on a stepwise evolution targeting the spacer region of the core promoter in Bacillus subtilis. Microb. Cell Fact. 18:196
    [Google Scholar]
  35. 35. 
    Heeney DD, Gareau MG, Marco ML 2018. Intestinal Lactobacillus in health and disease, a driver or just along for the ride. Curr. Opin. Biotechnol. 49:140–47
    [Google Scholar]
  36. 36. 
    Hensel M, Hinsley AP, Nikolaus T, Sawers G, Berks BC 1999. The genetic basis of tetrathionate respiration in Salmonellatyphimurium. Mol. Microbiol 32:275–87
    [Google Scholar]
  37. 37. 
    Hillson NJ, Rosengarten RD, Keasling JD 2012. j5 DNA assembly design automation software. ACS Synth. Biol. 1:114–21
    [Google Scholar]
  38. 37a. 
    Inda ME, Almada JC, Vazquez DB, Bortolotti A, Fernández Aet al. 2019. Driving the catalytic activity of a transmembrane thermosensor kinase. Cell. Mol. Life Sci2019 https://doi.org/10.1007/s00018-019-03400-1
    [Crossref] [Google Scholar]
  39. 38. 
    Inda ME, Mimee M, Lu T 2019. Cell-based biosensors for immunology, inflammation, and allergy. J. Allergy Clin. Immunol. 144:3645–47
    [Google Scholar]
  40. 38a. 
    Inda ME, Vazquez DB, Fernández A, Cybulski LE 2019. Reverse engineering of a thermosensing regulator switch. J. Mol. Biol 431:51016–24 https://doi.org/10.1016/j.jmb.2019.01.025
    [Crossref] [Google Scholar]
  41. 39. 
    Isabella VM, Ha BN, Castillo MJ, Lubkowicz DJ, Rowe SE et al. 2018. Development of a synthetic live bacterial therapeutic for the human metabolic disease phenylketonuria. Nat. Biotechnol. 36:857–64
    [Google Scholar]
  42. 40. 
    Jimenez M, Langer R, Traverso G 2019. Microbial therapeutics: new opportunities for drug delivery. J. Exp. Med. 216:51005–9
    [Google Scholar]
  43. 41. 
    Joe MH, Lee KH, Lim SY, Im SH, Song HP et al. 2012. Pigment-based whole-cell biosensor system for cadmium detection using genetically engineered Deinococcusradiodurans. BioprocessBiosyst. . Eng 35:265–72
    [Google Scholar]
  44. 42. 
    Junjua M, Galia W, Gaci N, Uriot O, Genay M et al. 2014. Development of the recombinase-based in vivo expression technology in Streptococcusthermophilus and validation using the lactose operon promoter. J. Appl. Microbiol. 116:3620–31
    [Google Scholar]
  45. 43. 
    Kaplan S, Bren A, Dekel E, Alon U 2008. The incoherent feed-forward loop can generate non-monotonic input functions for genes. Mol. Syst. Biol. 4:1203
    [Google Scholar]
  46. 44. 
    Kashyap DR, Rompca A, Gaballa A, Helmann JD, Chan J et al. 2014. Peptidoglycan recognition proteins kill bacteria by inducing oxidative, thiol, and metal stress. PLOS Pathog 10:7e1004280
    [Google Scholar]
  47. 45. 
    Kearney SM, Gibbons SM, Erdman SE, Alm EJ 2018. Orthogonal dietary niche enables reversible engraftment of a gut bacterial commensal. Cell Rep 24:71842–51
    [Google Scholar]
  48. 46. 
    Kitada T, DiAndreth B, Teague B, Weiss R 2018. Programming gene and engineered-cell therapies with synthetic biology. Science 359:6376eaad1067
    [Google Scholar]
  49. 47. 
    Komor AC, Kim YB, Packer MS, Zuris JA, Liu DR 2016. Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature 533:7603420–24
    [Google Scholar]
  50. 48. 
    Konig H, Frank D, Heil R, Coenen C 2013. Synthetic genomics and synthetic biology applications between hopes and concerns. Curr. Genom. 14:111–24
    [Google Scholar]
  51. 49. 
    Kotula JW, Kerns SJ, Shaket LA, Siraj L, Collins JJ et al. 2014. Programmable bacteria detect and record an environmental signal in the mammalian gut. PNAS 111:134838–43
    [Google Scholar]
  52. 50. 
    Kurtz CB, Millet YA, Puurunen MK, Perreault M, Charbonneau MR et al. 2019. An engineered E. coli Nissle improves hyperammonemia and survival in mice and shows dose-dependent exposure in healthy humans. Sci. Transl. Med. 11:475eaau7975
    [Google Scholar]
  53. 51. 
    Lakshmanan A, Farhadi A, Nety SP, Lee-Gosselin A, Bourdeau RW et al. 2016. Molecular engineering of acoustic protein nanostructures. ACS Nano 10:87314–22
    [Google Scholar]
  54. 52. 
    Landry BP, Tabor JJ. 2017. Engineering diagnostic and therapeutic gut bacteria. Microbiol. Spectr. 5:5BAD–0020-2017
    [Google Scholar]
  55. 53. 
    Leventhal DS, Sokolovska A, Li N, Plescia C, Kolodziej SA et al. 2020. Immunotherapy with engineered bacteria by targeting the STING pathway for anti-tumor immunity. Nat. Commun. 11:2739
    [Google Scholar]
  56. 54. 
    Levskaya A, Chevalier AA, Tabor JJ, Simpson ZB, Lavery LA et al. 2005. Engineering Escherichia coli to see light. Nature 438:7067441–42
    [Google Scholar]
  57. 55. 
    Li S, Si T, Wang M, Zhao H 2015. Development of a synthetic malonyl-CoA sensor in Saccharomycescerevisiae for intracellular metabolite monitoring and genetic screening. ACS Synth. Biol. 4:121308–15
    [Google Scholar]
  58. 56. 
    Liu X, Tang T-C, Tham E, Yuk H, Lin S et al. 2017. Stretchable living materials and devices with hydrogel-elastomer hybrids hosting programmed cells. PNAS 114:92200–5
    [Google Scholar]
  59. 57. 
    Lubkowicz D, Ho CL, Hwang IY, Yew WS, Lee YS, Chang MW 2018. Reprogramming probiotic Lactobacillusreuteri as a biosensor for Staphylococcusaureus derived AIP-I detection. ACS Synth. Biol. 7:51229–37
    [Google Scholar]
  60. 58. 
    Mangan S, Itzkovitz S, Zaslaver A, Alon U 2006. The incoherent feed-forward loop accelerates the response-time of the gal system of Escherichia coli. J. Mol. . Biol 356:51073–81
    [Google Scholar]
  61. 59. 
    Mao N, Cubillos-Ruiz A, Cameron DE, Collins JJ 2018. Probiotic strains detect and suppress cholera in mice. Sci. Transl. Med. 10:445eaao2586
    [Google Scholar]
  62. 60. 
    Meyer AJ, Segall-Shapiro TH, Glassey E, Zhang J, Voigt CA 2019. Escherichia coli “Marionette” strains with 12 highly optimized small-molecule sensors. Nat. Chem. Biol. 15:2196–204
    [Google Scholar]
  63. 61. 
    Mimee M, Citorik RJ, Lu TK 2016. Microbiome therapeutics—advances and challenges. Adv. Drug Deliv. Rev. 105:44–54
    [Google Scholar]
  64. 62. 
    Mimee M, Nadeau P, Hayward A, Carim S, Flanagan S et al. 2018. An ingestible bacterial-electronic system to monitor gastrointestinal health. Science 360:6391915–18
    [Google Scholar]
  65. 63. 
    Mimee M, Tucker AC, Voigt CA, Lu TK 2015. Programming a human commensal bacterium, Bacteroidesthetaiotaomicron, to sense and respond to stimuli in the murine gut microbiota. Cell Syst 1:162–71
    [Google Scholar]
  66. 64. 
    Moser F, Broers NJ, Hartmans S, Tamsir A, Kerkman R et al. 2012. Genetic circuit performance under conditions relevant for industrial bioreactors. ACS Synth. Biol. 1:11555–64
    [Google Scholar]
  67. 65. 
    Müller IE, Rubens JR, Jun T, Graham D, Xavier R, Lu TK 2019. Gene networks that compensate for crosstalk with crosstalk. Nat. Commun. 10:14028
    [Google Scholar]
  68. 66. 
    Naydich AD, Nangle SN, Bues JJ, Trivedi D, Nissar N et al. 2019. Synthetic gene circuits enable systems-level biosensor discovery at the host-microbe interface. mSystems 4:4e00125–19
    [Google Scholar]
  69. 67. 
    Nejman D, Livyatan I, Fuks G, Gavert N, Zwang Y et al. 2020. The human tumor microbiome is composed of tumor type–specific intracellular bacteria. Science 368:6494973–80
    [Google Scholar]
  70. 68. 
    Nielsen AAK, Der BS, Shin J, Vaidyanathan P, Paralanov V et al. 2016. Genetic circuit design automation. Science 352:6281aac7341
    [Google Scholar]
  71. 69. 
    Ostrov N, Jimenez M, Billerbeck S, Brisbois J, Matragrano J et al. 2017. A modular yeast biosensor for low-cost point-of-care pathogen detection. Sci. Adv. 3:6e1603221
    [Google Scholar]
  72. 70. 
    Packer MS, Liu DR. 2015. Methods for the directed evolution of proteins. Nat. Rev. Genet. 16:7379–94
    [Google Scholar]
  73. 71. 
    Persson BA, Lund M, Forsman J, Chatterton DEW, Åkesson T 2010. Molecular evidence of stereo-specific lactoferrin dimers in solution. Biophys. Chem. 151:3187–89
    [Google Scholar]
  74. 72. 
    Piraner DI, Abedi MH, Moser BA, Lee-Gosselin A, Shapiro MG 2017. Tunable thermal bioswitches for in vivo control of microbial therapeutics. Nat. Chem. Biol. 13:75–80
    [Google Scholar]
  75. 73. 
    Price-Carter M, Tingey J, Bobik TA, Roth JR 2001. The alternative electron acceptor tetrathionate supports B12-dependent anaerobic growth of Salmonellaenterica serovar Typhimurium on ethanolamine or 1,2-propanediol. J. Bacteriol. 183:2463–75
    [Google Scholar]
  76. 74. 
    Ravikumar S, Ganesh I, Yoo I, Hong SH 2012. Construction of a bacterial biosensor for zinc and copper and its application to the development of multifunctional heavy metal adsorption bacteria. Process Biochem 47:5758–65
    [Google Scholar]
  77. 75. 
    Richard HT, Foster JW. 2003. Acid resistance in Escherichia coli. Adv. Appl. Microbiol 52:167–86
    [Google Scholar]
  78. 76. 
    Riglar DT, Giessen TW, Baym M, Kerns SJ, Niederhuber MJ et al. 2017. Engineered bacteria can function in the mammalian gut long-term as live diagnostics of inflammation. Nat. Biotechnol. 35:7653–58
    [Google Scholar]
  79. 77. 
    Riglar DT, Silver PA. 2018. Engineering bacteria for diagnostic and therapeutic applications. Nat. Rev. Microbiol. 16:4214–25
    [Google Scholar]
  80. 78. 
    Roquet N, Soleimany AP, Ferris AC, Aaronson S, Lu TK 2016. Synthetic recombinase-based state machines in living cells. Science 353:6297aad8559
    [Google Scholar]
  81. 79. 
    Rosenfeld N, Elowitz MB, Alon U 2002. Negative autoregulation speeds the response times of transcription networks. J. Mol. Biol. 323:5785–93
    [Google Scholar]
  82. 80. 
    Rubens JR, Selvaggio G, Lu TK 2016. Synthetic mixed-signal computation in living cells. Nat. Commun. 7:11658
    [Google Scholar]
  83. 81. 
    Saltzman DA, Heise CP, Hasz DE, Zebede M, Kelly SM 1996. Attenuated Salmonellatyphimurium containing interleukin-2 decreases MC-38 hepatic metastases: a novel anti-tumor agent. Cancer Biother. Radiopharm. 11:2145–53
    [Google Scholar]
  84. 82. 
    Sands BE. 2015. Biomarkers of inflammation in inflammatory bowel disease. Gastroenterology 149:51275–85.e2
    [Google Scholar]
  85. 83. 
    Schmidl SR, Ekness F, Sofjan K, Daeffler KN-M, Brink KR et al. 2019. Rewiring bacterial two-component systems by modular DNA-binding domain swapping. Nat. Chem. Biol. 15:7690–98
    [Google Scholar]
  86. 84. 
    Schultz M, Watzl S, Oelschlaeger TA, Rath HC, Göttl C et al. 2005. Green fluorescent protein for detection of the probiotic microorganism Escherichia coli strain Nissle 1917 (EcN) in vivo. J. Microbiol. Methods 61:3389–98
    [Google Scholar]
  87. 85. 
    Selifonova O, Burlage R, Barkay T 1993. Bioluminescent sensors for detection of bioavailable Hg(II) in the environment. Appl. Environ. Microbiol. 59:93083–90
    [Google Scholar]
  88. 86. 
    Shapiro MG, Goodwill PW, Neogy A, Yin M, Foster FS et al. 2014. Biogenic gas nanostructures as ultrasonic molecular reporters. Nat. Nanotechnol. 9:4311–16
    [Google Scholar]
  89. 87. 
    Sharma P, Asad S, Ali A 2013. Bioluminescent bioreporter for assessment of arsenic contamination in water samples of India. J. Biosci. 38:2251–58
    [Google Scholar]
  90. 88. 
    Sheth RU, Yim SS, Wu FL, Wang HH 2017. Multiplex recording of cellular events over time on CRISPR biological tape. Science 358:63691457–61
    [Google Scholar]
  91. 89. 
    Shipman SL, Nivala J, Macklis JD, Church GM 2016. Molecular recordings by directed CRISPR spacer acquisition. Science 353:6298aaf1175
    [Google Scholar]
  92. 90. 
    Shis DL, Hussain F, Meinhardt S, Swint-Kruse L, Bennett MR 2014. Modular, multi-input transcriptional logic gating with orthogonal LacI/GalR family chimeras. ACS Synth. Biol. 3:9645–51
    [Google Scholar]
  93. 91. 
    Siuti P, Yazbek J, Lu TK 2013. Synthetic circuits integrating logic and memory in living cells. Nat. Biotechnol. 31:5448–52
    [Google Scholar]
  94. 92. 
    Strimbu K, Tavel JA. 2010. What are biomarkers. Curr. Opin. HIV AIDS 5:6463–66
    [Google Scholar]
  95. 93. 
    Tabor JJ, Groban ES, Voigt CA 2009. Performance characteristics for sensors and circuits used to program E. coli. Systems Biology and Biotechnology of Escherichia coli SY Lee 401–39 New York: Springer
    [Google Scholar]
  96. 94. 
    Tabor JJ, Salis HM, Simpson ZB, Chevalier AA, Levskaya A et al. 2009. A synthetic genetic edge detection program. Cell 137:71272–81
    [Google Scholar]
  97. 95. 
    Tang W, Liu DR. 2018. Rewritable multi-event analog recording in bacterial and mammalian cells. Science 360:6385eaap8992
    [Google Scholar]
  98. 96. 
    Teixeira AP, Fussenegger M. 2017. Synthetic biology-inspired therapies for metabolic diseases. Curr. Opin. Biotechnol. 47:59–66
    [Google Scholar]
  99. 97. 
    Toso JF, Gill VJ, Hwu P, Marincola FM, Restifo NP et al. 2002. Phase I study of the intravenous administration of attenuated Salmonellatyphimurium to patients with metastatic melanoma. J. Clin. Oncol. 20:1142–52
    [Google Scholar]
  100. 98. 
    Vargas AJ, Harris CC. 2016. Biomarker development in the precision medicine era: lung cancer as a case study. Nat. Rev. Cancer 16:8525–37
    [Google Scholar]
  101. 99. 
    Wang B, Barahona M, Buck M 2013. A modular cell-based biosensor using engineered genetic logic circuits to detect and integrate multiple environmental signals. Biosens. Bioelectron. 40:1368–76
    [Google Scholar]
  102. 100. 
    Watanabe L, Nguyen T, Zhang M, Zundel Z, Zhang Z et al. 2019. iBioSim 3: a tool for model-based genetic circuit design. ACS Synth. Biol. 8:71560–63
    [Google Scholar]
  103. 101. 
    Winkler JD, Garcia C, Olson M, Callaway E, Kao KC 2014. Evolved osmotolerant Escherichia coli mutants frequently exhibit defective N-acetylglucosamine catabolism and point mutations in cell shape-regulating protein MreB. Appl. Environ. Microbiol. 80:123729–40
    [Google Scholar]
  104. 102. 
    Xu P, Wang W, Li L, Bhan N, Zhang F, Koffas MAG 2014. Design and kinetic analysis of a hybrid promoter-regulator system for malonyl-CoA sensing in Escherichia coli. ACS Chem. Biol 9:2451–58
    [Google Scholar]
  105. 103. 
    Zhang J, Barajas JF, Burdu M, Ruegg TL, Dias B, Keasling JD 2017. Development of a transcription factor-based lactam biosensor. ACS Synth. Biol. 6:3439–45
    [Google Scholar]
/content/journals/10.1146/annurev-micro-022620-081059
Loading
/content/journals/10.1146/annurev-micro-022620-081059
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error