Genomic Recoding Broadly Obstructs the Propagation of Horizontally Transferred Genetic Elements

Ma, Natalie Jing; Isaacs, Farren J.

doi:10.1016/j.cels.2016.06.009

Title: Genomic Recoding Broadly Obstructs the Propagation of Horizontally Transferred Genetic Elements

Journal Article · Wed Aug 24 00:00:00 EDT 2016 · Cell Systems

DOI:https://doi.org/10.1016/j.cels.2016.06.009· OSTI ID:1394715

Ma, Natalie Jing; Isaacs, Farren J.

Horizontally transferred genetic elements such as viruses and conjugative plasmids move DNA between organisms, increasing genetic diversity but destabilizing engineered biological systems. For this, we used a genomically recoded Escherichia coli strain lacking UAG stop codons and the recognition protein release factor 1 to study how an alternative genetic code influences horizontally transferred genetic element propagation. The alternative genetic code conferred resistance to multiple viruses (λ, M13, P1, MS2) at titers up to 10¹¹ PFU/ml and impaired conjugative plasmids (F and RK2) up to 10⁵-fold. By recoding UAG codons to UAA in viruses and plasmids, we restored viral infectivity and conjugative function. Propagating viruses on a mixed community of cells with standard and alternative genetic codes reduced viral titer, and over time viruses adapted to the alternative genetic code. This work demonstrates that altering the genetic code broadly obstructs the propagation of horizontally transferred genetic elements and supports the use of genomic recoding as a strategy to stabilize engineered biological systems.

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Research Organization:: Harvard Univ., Cambridge, MA (United States)

Sponsoring Organization:: USDOE; National Institutes of Health (NIH); Gruber Foundation; Defense Advanced Research Projects Agency (DARPA); Gen9, Cambridge, MA (United States); DuPont, Wilmington, DE (United States); Arnold and Mabel Beckman Foundation

Grant/Contract Number:: FG02-02ER63445; T32GM007499; T32GM007223; HR0011-15-C-0091; 1R01GM117230-01

OSTI ID:: 1394715

Alternate ID(s):: OSTI ID: 1466971

Journal Information:: Cell Systems, Journal Name: Cell Systems Vol. 3 Journal Issue: 2; ISSN 2405-4712

Publisher:: ElsevierCopyright Statement

Country of Publication:: Niger

Language:: English

Citation Metrics:

Cited by: 28 works

Citation information provided by
Web of Science

References (53)

Lateral gene transfer and the nature of bacterial innovation Ochman, Howard; Lawrence, Jeffrey G.; Groisman, Eduardo A. Nature, Vol. 405, Issue 6784 https://doi.org/10.1038/35012500	journal	May 2000
Estimating the biotech sector's contribution to the US economy Carlson, Robert Nature Biotechnology, Vol. 34, Issue 3 https://doi.org/10.1038/nbt.3491	journal	March 2016
Genome of Bacteriophage P1 Lobocka, M. B.; Rose, D. J.; Plunkett, G. Journal of Bacteriology, Vol. 186, Issue 21 https://doi.org/10.1128/JB.186.21.7032-7068.2004	journal	October 2004
The traY Gene Product and Integration Host Factor Stimulate Escherichia coli DNA Helicase I-catalyzed Nicking at the F Plasmid oriT Nelson, William C.; Howard, Michael T.; Sherman, Jonathan A. Journal of Biological Chemistry, Vol. 270, Issue 47 https://doi.org/10.1074/jbc.270.47.28374	journal	November 1995
Bacteriophage Mu genome sequence: analysis and comparison with Mu-like prophages in Haemophilus, Neisseria and Deinococcus Morgan, Gregory J.; Hatfull, Graham F.; Casjens, Sherwood Journal of Molecular Biology, Vol. 317, Issue 3 https://doi.org/10.1006/jmbi.2002.5437	journal	March 2002
Stop codon reassignments in the wild Ivanova, N. N.; Schwientek, P.; Tripp, H. J. Science, Vol. 344, Issue 6186, p. 909-913 https://doi.org/10.1126/science.1250691	journal	May 2014
Regulated programmed lysis of recombinant Salmonella in host tissues to release protective antigens and confer biological containment Kong, W.; Wanda, S.-Y.; Zhang, X. Proceedings of the National Academy of Sciences, Vol. 105, Issue 27, p. 9361-9366 https://doi.org/10.1073/pnas.0803801105	journal	July 2008
NCBI Viral Genomes Resource Brister, J. Rodney; Ako-adjei, Danso; Bao, Yiming Nucleic Acids Research, Vol. 43, Issue D1 https://doi.org/10.1093/nar/gku1207	journal	November 2014
Evolutionary Implications of Horizontal Gene Transfer Syvanen, Michael Annual Review of Genetics, Vol. 46, Issue 1 https://doi.org/10.1146/annurev-genet-110711-155529	journal	December 2012
Programming cells by multiplex genome engineering and accelerated evolution Wang, Harris H.; Isaacs, Farren J.; Carr, Peter A. Nature, Vol. 460, Issue 7257, p. 894-898 https://doi.org/10.1038/nature08187	journal	July 2009
Nucleotide sequence of the filamentous bacteriophage M13 DNA genome: comparison with phage fd van Wezenbeek, Peter M. G. F.; Hulsebos, Theo J. M.; Schoenmakers, John G. G. Gene, Vol. 11, Issue 1-2 https://doi.org/10.1016/0378-1119(80)90093-1	journal	October 1980
Rapid editing and evolution of bacterial genomes using libraries of synthetic DNA Gallagher, Ryan R.; Li, Zhe; Lewis, Aaron O. Nature Protocols, Vol. 9, Issue 10 https://doi.org/10.1038/nprot.2014.082	journal	September 2014
Precise manipulation of bacterial chromosomes by conjugative assembly genome engineering Ma, Natalie J.; Moonan, Daniel W.; Isaacs, Farren J. Nature Protocols, Vol. 9, Issue 10 https://doi.org/10.1038/nprot.2014.081	journal	September 2014
Transfer ribonucleic acid-mediated suppression of termination codons in Escherichia coli. Eggertsson, G.; Söll, D. Microbiological Reviews, Vol. 52, Issue 3 https://doi.org/10.1128/MR.52.3.354-374.1988	journal	January 1988
Mechanisms of, and Barriers to, Horizontal Gene Transfer between Bacteria Thomas, Christopher M.; Nielsen, Kaare M. Nature Reviews Microbiology, Vol. 3, Issue 9 https://doi.org/10.1038/nrmicro1234	journal	September 2005
A Bacteriophage Containing rna Loeb, T.; Zinder, N. D. Proceedings of the National Academy of Sciences, Vol. 47, Issue 3 https://doi.org/10.1073/pnas.47.3.282	journal	March 1961
An Mr 29 000 protein is essential for mini-F maintenance in E. coli Watson, L. A.; Phua, S. H.; Bergquist, P. L. Gene, Vol. 19, Issue 2 https://doi.org/10.1016/0378-1119(82)90003-8	journal	September 1982
Rates of spontaneous mutation among RNA viruses. Drake, J. W. Proceedings of the National Academy of Sciences, Vol. 90, Issue 9 https://doi.org/10.1073/pnas.90.9.4171	journal	May 1993
Influenza A Virus Attenuation by Codon Deoptimization of the NS Gene for Vaccine Development Nogales, A.; Baker, S. F.; Ortiz-Riano, E. Journal of Virology, Vol. 88, Issue 18 https://doi.org/10.1128/JVI.01565-14	journal	June 2014
Exploring the costs of horizontal gene transfer Baltrus, David A. Trends in Ecology & Evolution, Vol. 28, Issue 8 https://doi.org/10.1016/j.tree.2013.04.002	journal	August 2013
Rewiring the keyboard: evolvability of the genetic code Knight, Robin D.; Freeland, Stephen J.; Landweber, Laura F. Nature Reviews Genetics, Vol. 2, Issue 1 https://doi.org/10.1038/35047500	journal	January 2001
'Deadman' and 'Passcode' microbial kill switches for bacterial containment Chan, Clement T. Y.; Lee, Jeong Wook; Cameron, D. Ewen Nature Chemical Biology, Vol. 12, Issue 2 https://doi.org/10.1038/nchembio.1979	journal	December 2015
Complete nucleotide sequence of bacteriophage MS2 RNA: primary and secondary structure of the replicase gene Fiers, W.; Contreras, R.; Duerinck, F. Nature, Vol. 260, Issue 5551 https://doi.org/10.1038/260500a0	journal	April 1976
Stages in phage R17 infection Paranchych, W.; Ainsworth, S. K.; Dick, A. J. Virology, Vol. 45, Issue 3 https://doi.org/10.1016/0042-6822(71)90176-0	journal	September 1971
Complete genome sequence of bacteriophage T5 Wang, Jianbin; Jiang, Yan; Vincent, Myriam Virology, Vol. 332, Issue 1 https://doi.org/10.1016/j.virol.2004.10.049	journal	February 2005
Analysis of the sequence and gene products of the transfer region of the F sex factor. Frost, L. S.; Ippen-Ihler, K.; Skurray, R. A. Microbiological Reviews, Vol. 58, Issue 2 https://doi.org/10.1128/MR.58.2.162-210.1994	journal	January 1994
Engineering bacteria for bioremediation Pieper, Dietmar H.; Reineke, Walter Current Opinion in Biotechnology, Vol. 11, Issue 3 https://doi.org/10.1016/S0958-1669(00)00094-X	journal	June 2000
Evolution and classification of the CRISPR–Cas systems Makarova, Kira S.; Haft, Daniel H.; Barrangou, Rodolphe Nature Reviews Microbiology, Vol. 9, Issue 6, p. 467-477 https://doi.org/10.1038/nrmicro2577	journal	May 2011
Delineating the Site of Interaction on the pIII Protein of Filamentous Bacteriophage fd with the F-pilus of Escherichia coli Deng, Lih-Wen; Perham, Richard N. Journal of Molecular Biology, Vol. 319, Issue 3 https://doi.org/10.1016/S0022-2836(02)00260-7	journal	June 2002
Synthetic constructs in/for the environment: Managing the interplay between natural and engineered Biology Schmidt, Markus; de Lorenzo, Víctor FEBS Letters, Vol. 586, Issue 15 https://doi.org/10.1016/j.febslet.2012.02.022	journal	February 2012
Preparing synthetic biology for the world Moe-Behrens, Gerd H. G.; Davis, Rene; Haynes, Karmella A. Frontiers in Microbiology, Vol. 4 https://doi.org/10.3389/fmicb.2013.00005	journal	January 2013
λ N antitermination system: Functional analysis of phage interactions with the host NusA protein Schauer, Alan T.; Carver, Debra L.; Bigelow, Bradley Journal of Molecular Biology, Vol. 194, Issue 4 https://doi.org/10.1016/0022-2836(87)90245-2	journal	April 1987
Inhibition of Formation of Escherichia coli Mating Pairs by f1 and MS2 Bacteriophages as Determined with a Coulter Counter Ou, Jonathan T. Journal of Bacteriology, Vol. 114, Issue 3 https://doi.org/10.1128/JB.114.3.1108-1115.1973	journal	January 1973
Biocontainment of genetically modified organisms by synthetic protein design Mandell, Daniel J.; Lajoie, Marc J.; Mee, Michael T. Nature, Vol. 518, Issue 7537 https://doi.org/10.1038/nature14121	journal	January 2015
Virus stalls Genzyme plant Bethencourt, Victor Nature Biotechnology, Vol. 27, Issue 8 https://doi.org/10.1038/nbt0809-681a	journal	August 2009
Precise Manipulation of Chromosomes in Vivo Enables Genome-Wide Codon Replacement Isaacs, Farren J.; Carr, Peter A.; Wang, Harris H. Science, Vol. 333, Issue 6040, p. 348-353 https://doi.org/10.1126/science.1205822	journal	July 2011
Mechanisms of ribosome rescue in bacteria Keiler, Kenneth C. Nature Reviews Microbiology, Vol. 13, Issue 5 https://doi.org/10.1038/nrmicro3438	journal	April 2015
Probing the Limits of Genetic Recoding in Essential Genes Lajoie, M. J.; Kosuri, S.; Mosberg, J. A. Science, Vol. 342, Issue 6156 https://doi.org/10.1126/science.1241460	journal	October 2013
Dual System To Reinforce Biological Containment of Recombinant Bacteria Designed for Rhizoremediation Ronchel, M. C.; Ramos, J. L. Applied and Environmental Microbiology, Vol. 67, Issue 6 https://doi.org/10.1128/AEM.67.6.2649-2656.2001	journal	June 2001
Virus Attenuation by Genome-Scale Changes in Codon Pair Bias Coleman, J. R.; Papamichail, D.; Skiena, S. Science, Vol. 320, Issue 5884 https://doi.org/10.1126/science.1155761	journal	June 2008
Virus population extinction via ecological traps Dennehy, John J.; Friedenberg, Nicholas A.; Yang, Yul W. Ecology Letters, Vol. 10, Issue 3 https://doi.org/10.1111/j.1461-0248.2006.01013.x	journal	March 2007
Intrinsic biocontainment: Multiplex genome safeguards combine transcriptional and recombinational control of essential yeast genes Cai, Yizhi; Agmon, Neta; Choi, Woo Jin Proceedings of the National Academy of Sciences, Vol. 112, Issue 6 https://doi.org/10.1073/pnas.1424704112	journal	January 2015
The role of alternative genetic codes in viral evolution and emergence Shackelton, Laura A.; Holmes, Edward C. Journal of Theoretical Biology, Vol. 254, Issue 1 https://doi.org/10.1016/j.jtbi.2008.05.024	journal	September 2008
Complete Nucleotide Sequence of Birmingham IncPα Plasmids Pansegrau, Werner; Lanka, Erich; Barth, Peter T. Journal of Molecular Biology, Vol. 239, Issue 5 https://doi.org/10.1006/jmbi.1994.1404	journal	June 1994
Synthetic Fatty Acids Prevent Plasmid-Mediated Horizontal Gene Transfer Getino, María; Sanabria-Ríos, David J.; Fernández-López, Raúl mBio, Vol. 6, Issue 5 https://doi.org/10.1128/mBio.01032-15	journal	September 2015
Biological containment of genetically modified Lactococcus lactis for intestinal delivery of human interleukin 10 Steidler, Lothar; Neirynck, Sabine; Huyghebaert, Nathalie Nature Biotechnology, Vol. 21, Issue 7 https://doi.org/10.1038/nbt840	journal	June 2003
Incompatibility Group P Plasmids: Genetics, Evolution, and Use in Genetic Manipulation Thomas, C. M.; Smith, C. A. Annual Review of Microbiology, Vol. 41, Issue 1 https://doi.org/10.1146/annurev.mi.41.100187.000453	journal	October 1987
Recoded organisms engineered to depend on synthetic amino acids Rovner, Alexis J.; Haimovich, Adrian D.; Katz, Spencer R. Nature, Vol. 518, Issue 7537 https://doi.org/10.1038/nature14095	journal	January 2015
Transfer RNA Misidentification Scrambles Sense Codon Recoding Krishnakumar, Radha; Prat, Laure; Aerni, Hans-Rudolf ChemBioChem, Vol. 14, Issue 15 https://doi.org/10.1002/cbic.201300444	journal	September 2013
Genomically Recoded Organisms Expand Biological Functions Lajoie, M. J.; Rovner, A. J.; Goodman, D. B. Science, Vol. 342, Issue 6156, p. 357-360 https://doi.org/10.1126/science.1241459	journal	October 2013
Phage lambda gene Q antiterminator recognizes RNA polymerase near the promoter and accelerates it through a pause site Grayhack, E.; Yang, X.; Lau, L. Cell, Vol. 42, Issue 1 https://doi.org/10.1016/S0092-8674(85)80121-5	journal	August 1985
Multilayered genetic safeguards limit growth of microorganisms to defined environments Gallagher, Ryan R.; Patel, Jaymin R.; Interiano, Alexander L. Nucleic Acids Research, Vol. 43, Issue 3 https://doi.org/10.1093/nar/gku1378	journal	January 2015
Biology of DNA restriction. Bickle, T. A.; Krüger, D. H. Microbiological Reviews, Vol. 57, Issue 2 https://doi.org/10.1128/MR.57.2.434-450.1993	journal	January 1993

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