New candidates for regulated gene integrity revealed through precise mapping of integrative genetic elements
Abstract
Abstract Integrative genetic elements (IGEs) are mobile multigene DNA units that integrate into and excise from host bacterial genomes. Each IGE usually targets a specific site within a conserved host gene, integrating in a manner that preserves target gene function. However, a small number of bacterial genes are known to be inactivated upon IGE integration and reactivated upon excision, regulating phenotypes of virulence, mutation rate, and terminal differentiation in multicellular bacteria. The list of regulated gene integrity (RGI) cases has been slow-growing because IGEs have been challenging to precisely and comprehensively locate in genomes. We present software (TIGER) that maps IGEs with unprecedented precision and without attB site bias. TIGER uses a comparative genomic, ping-pong BLAST approach, based on the principle that the IGE integration module (i.e. its int-attP region) is cohesive. The resultant IGEs from 2168 genomes, along with integrase phylogenetic analysis and gene inactivation tests, revealed 19 new cases of genes whose integrity is regulated by IGEs (including dut, eccCa1, gntT, hrpB, merA, ompN, prkA, tqsA, traG, yifB, yfaT and ynfE), as well as recovering previously known cases (in sigK, spsM, comK, mlrA and hlb genes). It also recovered known clades of site-promiscuous integrases and identified possible new ones.
- Authors:
-
[1]
- Sandia National Laboratories, Systems Biology Department, Livermore, CA 94551-0969, USA
- Publication Date:
- Research Org.:
- Sandia National Lab. (SNL-CA), Livermore, CA (United States)
- Sponsoring Org.:
- USDOE National Nuclear Security Administration (NNSA); USDOE Laboratory Directed Research and Development (LDRD) Program; Defense Advanced Research Projects Agency (DARPA)
- OSTI Identifier:
- 1605044
- Alternate Identifier(s):
- OSTI ID: 1815571
- Grant/Contract Number:
- NA0003525; HR0011-17-2-0043
- Resource Type:
- Published Article
- Journal Name:
- Nucleic Acids Research
- Additional Journal Information:
- Journal Name: Nucleic Acids Research Journal Volume: 48 Journal Issue: 8; Journal ID: ISSN 0305-1048
- Publisher:
- Oxford University Press
- Country of Publication:
- United Kingdom
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Computational Methods; Genomics
Citation Formats
Mageeney, Catherine M., Lau, Britney Y., Wagner, Julian M., Hudson, Corey M., Schoeniger, Joseph S., Krishnakumar, Raga, and Williams, Kelly P. New candidates for regulated gene integrity revealed through precise mapping of integrative genetic elements. United Kingdom: N. p., 2020.
Web. doi:10.1093/nar/gkaa156.
Mageeney, Catherine M., Lau, Britney Y., Wagner, Julian M., Hudson, Corey M., Schoeniger, Joseph S., Krishnakumar, Raga, & Williams, Kelly P. New candidates for regulated gene integrity revealed through precise mapping of integrative genetic elements. United Kingdom. https://doi.org/10.1093/nar/gkaa156
Mageeney, Catherine M., Lau, Britney Y., Wagner, Julian M., Hudson, Corey M., Schoeniger, Joseph S., Krishnakumar, Raga, and Williams, Kelly P. Tue .
"New candidates for regulated gene integrity revealed through precise mapping of integrative genetic elements". United Kingdom. https://doi.org/10.1093/nar/gkaa156.
@article{osti_1605044,
title = {New candidates for regulated gene integrity revealed through precise mapping of integrative genetic elements},
author = {Mageeney, Catherine M. and Lau, Britney Y. and Wagner, Julian M. and Hudson, Corey M. and Schoeniger, Joseph S. and Krishnakumar, Raga and Williams, Kelly P.},
abstractNote = {Abstract Integrative genetic elements (IGEs) are mobile multigene DNA units that integrate into and excise from host bacterial genomes. Each IGE usually targets a specific site within a conserved host gene, integrating in a manner that preserves target gene function. However, a small number of bacterial genes are known to be inactivated upon IGE integration and reactivated upon excision, regulating phenotypes of virulence, mutation rate, and terminal differentiation in multicellular bacteria. The list of regulated gene integrity (RGI) cases has been slow-growing because IGEs have been challenging to precisely and comprehensively locate in genomes. We present software (TIGER) that maps IGEs with unprecedented precision and without attB site bias. TIGER uses a comparative genomic, ping-pong BLAST approach, based on the principle that the IGE integration module (i.e. its int-attP region) is cohesive. The resultant IGEs from 2168 genomes, along with integrase phylogenetic analysis and gene inactivation tests, revealed 19 new cases of genes whose integrity is regulated by IGEs (including dut, eccCa1, gntT, hrpB, merA, ompN, prkA, tqsA, traG, yifB, yfaT and ynfE), as well as recovering previously known cases (in sigK, spsM, comK, mlrA and hlb genes). It also recovered known clades of site-promiscuous integrases and identified possible new ones.},
doi = {10.1093/nar/gkaa156},
journal = {Nucleic Acids Research},
number = 8,
volume = 48,
place = {United Kingdom},
year = {Tue Mar 17 00:00:00 EDT 2020},
month = {Tue Mar 17 00:00:00 EDT 2020}
}
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1093/nar/gkaa156
https://doi.org/10.1093/nar/gkaa156
Other availability
Search WorldCat to find libraries that may hold this journal
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.
Works referenced in this record:
A new perspective on lysogeny: prophages as active regulatory switches of bacteria
journal, September 2015
- Feiner, Ron; Argov, Tal; Rabinovich, Lev
- Nature Reviews Microbiology, Vol. 13, Issue 10
Challenging a Paradigm: the Role of DNA Homology in Tyrosine Recombinase Reactions
journal, June 2009
- Rajeev, L.; Malanowska, K.; Gardner, J. F.
- Microbiology and Molecular Biology Reviews, Vol. 73, Issue 2
Control of Recombination Directionality by the Listeria Phage A118 Protein Gp44 and the Coiled-Coil Motif of Its Serine Integrase
journal, March 2017
- Mandali, Sridhar; Gupta, Kushol; Dawson, Anthony R.
- Journal of Bacteriology, Vol. 199, Issue 11
ϕSa3mw Prophage as a Molecular Regulatory Switch of Staphylococcus aureus β-Toxin Production
journal, April 2019
- Tran, Phuong M.; Feiss, Michael; Kinney, Kyle J.
- Journal of Bacteriology, Vol. 201, Issue 14
A Novel Method to Predict Genomic Islands Based on Mean Shift Clustering Algorithm
journal, January 2016
- de Brito, Daniel M.; Maracaja-Coutinho, Vinicius; de Farias, Savio T.
- PLOS ONE, Vol. 11, Issue 1
Efficient sporulation in Clostridium difficile requires disruption of the σK gene: Gene disruption essential for sporulation
journal, April 2003
- Haraldsen, Jeralyn D.; Sonenshein, Abraham L.
- Molecular Microbiology, Vol. 48, Issue 3
Identification of compositionally distinct regions in genomes using the centroid method
journal, August 2007
- Rajan, I.; Aravamuthan, S.; Mande, S. S.
- Bioinformatics, Vol. 23, Issue 20
Detecting pathogenicity islands and anomalous gene clusters by iterative discriminant analysis
journal, April 2003
- Tu, Qiang; Ding, Dafu
- FEMS Microbiology Letters, Vol. 221, Issue 2
Phage-Associated Mutator Phenotype in Group A Streptococcus
journal, August 2008
- Scott, J.; Thompson-Mayberry, P.; Lahmamsi, S.
- Journal of Bacteriology, Vol. 190, Issue 19
Detecting genomic islands using bioinformatics approaches
journal, May 2010
- Langille, Morgan G. I.; Hsiao, William W. L.; Brinkman, Fiona S. L.
- Nature Reviews Microbiology, Vol. 8, Issue 5
Identification and analysis of integrons and cassette arrays in bacterial genomes
journal, April 2016
- Cury, Jean; Jové, Thomas; Touchon, Marie
- Nucleic Acids Research, Vol. 44, Issue 10
Improved genomic island predictions with IslandPath-DIMOB
journal, February 2018
- Bertelli, Claire; Brinkman, Fiona S. L.
- Bioinformatics, Vol. 34, Issue 13
TnpPred: A Web Service for the Robust Prediction of Prokaryotic Transposases
journal, January 2012
- Riadi, Gonzalo; Medina-Moenne, Cristobal; Holmes, David S.
- Comparative and Functional Genomics, Vol. 2012
FastTree 2 – Approximately Maximum-Likelihood Trees for Large Alignments
journal, March 2010
- Price, Morgan N.; Dehal, Paramvir S.; Arkin, Adam P.
- PLoS ONE, Vol. 5, Issue 3
Analysis of suppressor mutations of spoIVCA mutations: occurrence of DNA rearrangement in the absence of site-specific DNA recombinase SpoIVCA in Bacillus subtilis.
journal, January 1996
- Sato, T.; Harada, K.; Kobayashi, Y.
- Journal of bacteriology, Vol. 178, Issue 11
Tn4371:A Modular Structure Encoding a Phage-like Integrase, aPseudomonas-like Catabolic Pathway, and RP4/Ti-like Transfer Functions
journal, January 1999
- Merlin, Christophe; Springael, Dirk; Toussaint, Ariane
- Plasmid, Vol. 41, Issue 1
A highly specific phage defense system is a conserved feature of the Vibrio cholerae mobilome
journal, June 2017
- O’Hara, Brendan J.; Barth, Zachary K.; McKitterick, Amelia C.
- PLOS Genetics, Vol. 13, Issue 6
Islander: a database of precisely mapped genomic islands in tRNA and tmRNA genes
journal, November 2014
- Hudson, Corey M.; Lau, Britney Y.; Williams, Kelly P.
- Nucleic Acids Research, Vol. 43, Issue D1
Transfer RNA genes frequently serve as integration sites for prokaryotic genetic elements
journal, January 1989
- Reiter, Wolf-Dieter; Palm, Peter; Yeats, Siobhan
- Nucleic Acids Research, Vol. 17, Issue 5
Interpolated variable order motifs for identification of horizontally acquired DNA: revisiting the Salmonella pathogenicity islands
journal, July 2006
- Vernikos, Georgios S.; Parkhill, Julian
- Bioinformatics, Vol. 22, Issue 18
Evolution and variation of the nifD and hupL elements in the heterocystous cyanobacteria
journal, January 2011
- Henson, B. J.; Hartman, L.; Watson, L. E.
- INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 61, Issue 12
Complete nucleotide sequence, molecular analysis and genome structure of bacteriophage A118 of Listeria monocytogenes : implications for phage evolution
journal, January 2000
- Loessner, Martin J.; Inman, Ross B.; Lauer, Peter
- Molecular Microbiology, Vol. 35, Issue 2
SigHunt: horizontal gene transfer finder optimized for eukaryotic genomes
journal, December 2013
- Jaron, K. S.; Moravec, J. C.; Martinkova, N.
- Bioinformatics, Vol. 30, Issue 8
Integration specificities of two lambdoid phages (21 and e14) that insert at the same attB site.
journal, January 1997
- Wang, H.; Yang, C. H.; Lee, G.
- Journal of bacteriology, Vol. 179, Issue 18
Microbial genomic island discovery, visualization and analysis
journal, June 2018
- Bertelli, Claire; Tilley, Keith E.; Brinkman, Fiona S. L.
- Briefings in Bioinformatics, Vol. 20, Issue 5
Traffic at the tmRNA Gene
journal, February 2003
- Williams, K. P.
- Journal of Bacteriology, Vol. 185, Issue 3
GI-SVM: A sensitive method for predicting genomic islands based on unannotated sequence of a single genome
journal, February 2016
- Lu, Bingxin; Leong, Hon Wai
- Journal of Bioinformatics and Computational Biology, Vol. 14, Issue 01
Evaluation of genomic island predictors using a comparative genomics approach
journal, January 2008
- Langille, Morgan GI; Hsiao, William WL; Brinkman, Fiona SL
- BMC Bioinformatics, Vol. 9, Issue 1
Variations on the tmRNA gene
journal, September 2009
- Mao, Chunhong; Bhardwaj, Kanchan; Sharkady, Stephen M.
- RNA Biology, Vol. 6, Issue 4
Prokka: rapid prokaryotic genome annotation
journal, March 2014
- Seemann, T.
- Bioinformatics, Vol. 30, Issue 14
Analysis of six prophages in Lactococcus lactis IL1403: different genetic structure of temperate and virulent phage populations
journal, February 2001
- Chopin, A.
- Nucleic Acids Research, Vol. 29, Issue 3
The Pfam protein families database in 2019
journal, October 2018
- El-Gebali, Sara; Mistry, Jaina; Bateman, Alex
- Nucleic Acids Research, Vol. 47, Issue D1
IslandViewer 4: expanded prediction of genomic islands for larger-scale datasets
journal, May 2017
- Bertelli, Claire; Laird, Matthew R.; Williams, Kelly P.
- Nucleic Acids Research, Vol. 45, Issue W1
Mechanism of bacterial gene rearrangement: SprA-catalyzed precise DNA recombination and its directionality control by SprB ensure the gene rearrangement and stable expression of spsM during sporulation in Bacillus subtilis
journal, May 2017
- Abe, Kimihiro; Takamatsu, Takuo; Sato, Tsutomu
- Nucleic Acids Research, Vol. 45, Issue 11
Detection of genomic islands via segmental genome heterogeneity
journal, July 2009
- Arvey, Aaron J.; Azad, Rajeev K.; Raval, Alpan
- Nucleic Acids Research, Vol. 37, Issue 16
A sensitive, support-vector-machine method for the detection of horizontal gene transfers in viral, archaeal and bacterial genomes
journal, July 2005
- Tsirigos, A.
- Nucleic Acids Research, Vol. 33, Issue 12
Making serine integrases work for us
journal, August 2017
- Stark, W. Marshall
- Current Opinion in Microbiology, Vol. 38
Mobile DNAs as Ecologically and Evolutionarily Independent Units of Life
journal, November 2018
- Ghaly, Timothy M.; Gillings, Michael R.
- Trends in Microbiology, Vol. 26, Issue 11
Programmed DNA rearrangement of a cyanobacterial hupL gene in heterocysts.
journal, January 1995
- Carrasco, C. D.; Buettner, J. A.; Golden, J. W.
- Proceedings of the National Academy of Sciences, Vol. 92, Issue 3
A Theory of Modular Evolution for Bacteriophages
journal, November 1980
- Botstein, David
- Annals of the New York Academy of Sciences, Vol. 354, Issue 1 Genetic Varia
ICEberg 2.0: an updated database of bacterial integrative and conjugative elements
journal, November 2018
- Liu, Meng; Li, Xiaobin; Xie, Yingzhou
- Nucleic Acids Research, Vol. 47, Issue D1
A novel non prophage(-like) gene-intervening element within gerE that is reconstituted during sporulation in Bacillus cereus ATCC10987
journal, September 2017
- Abe, Kimihiro; Shimizu, Shin-ya; Tsuda, Shuhei
- Scientific Reports, Vol. 7, Issue 1
Integration sites for genetic elements in prokaryotic tRNA and tmRNA genes: sublocation preference of integrase subfamilies
journal, February 2002
- Williams, K. P.
- Nucleic Acids Research, Vol. 30, Issue 4
INDeGenIUS, a new method for high-throughput identification of specialized functional islands in completely sequenced organisms
journal, August 2010
- Shrivastava, Sakshi; Siva Kumar Reddy, Ch. V.; Mande, Sharmila S.
- Journal of Biosciences, Vol. 35, Issue 3
Rearrangement of nitrogen fixation genes during heterocyst differentiation in the cyanobacterium Anabaena
journal, April 1985
- Golden, James W.; Robinson, Steven J.; Haselkorn, Robert
- Nature, Vol. 314, Issue 6010
Filamentous phage integration requires the host recombinases XerC and XerD
journal, June 2002
- Huber, Kathryn E.; Waldor, Matthew K.
- Nature, Vol. 417, Issue 6889
Stx 1 prophage excision in Escherichia coli strain PA20 confers strong curli and biofilm formation by restoring native mlrA
journal, May 2016
- Uhlich, Gaylen A.; Chen, Chin-Yi; Cottrell, Bryan J.
- FEMS Microbiology Letters, Vol. 363, Issue 13
High throughput ANI analysis of 90K prokaryotic genomes reveals clear species boundaries
journal, November 2018
- Jain, Chirag; Rodriguez-R, Luis M.; Phillippy, Adam M.
- Nature Communications, Vol. 9, Issue 1
Cryptic inoviruses revealed as pervasive in bacteria and archaea across Earth’s biomes
journal, July 2019
- Roux, Simon; Krupovic, Mart; Daly, Rebecca A.
- Nature Microbiology
Deletion of a 55-kilobase-pair DNA element from the chromosome during heterocyst differentiation of Anabaena sp. strain PCC 7120.
journal, January 1988
- Golden, J. W.; Carrasco, C. D.; Mulligan, M. E.
- Journal of Bacteriology, Vol. 170, Issue 11
Resolvase-like serine recombinase mediates integration/excision in the bacteriophage ϕRSM
journal, February 2011
- Askora, Ahmed; Kawasaki, Takeru; Fujie, Makoto
- Journal of Bioscience and Bioengineering, Vol. 111, Issue 2
A proposed mechanism for IS607-family serine transposases
journal, January 2013
- Boocock, Martin R.; Rice, Phoebe A.
- Mobile DNA, Vol. 4, Issue 1
Pneumococcal prophages are diverse, but not without structure or history
journal, February 2017
- Brueggemann, Angela B.; Harrold, Caroline L.; Rezaei Javan, Reza
- Scientific Reports, Vol. 7, Issue 1