Transposases are the most abundant, most ubiquitous genes in nature

Aziz, Ramy K.; Breitbart, Mya; Edwards, Robert A.

doi:10.1093/nar/gkq140

Title: Transposases are the most abundant, most ubiquitous genes in nature

Journal Article · 08 March 2010 · Nucleic Acids Research

DOI: https://doi.org/10.1093/nar/gkq140 · OSTI ID:1625476

Aziz, Ramy K. ^[1]; Breitbart, Mya ^[2]; Edwards, Robert A. ^[3]

Univ. of Chicago, IL (United States). Computation Inst.; Cairo Univ. (Egypt). Faculty of Pharmacy. Dept. of Microbiology and Immunology; DOE/OSTI
Univ. of South Florida, Tampa, FL (United States). College of Marine Science
San Diego State Univ., CA (United States). Dept. of Computer Science; Argonne National Lab. (ANL), Argonne, IL (United States). Mathematics and Computer Science Division

Genes, like organisms, struggle for existence, and the most successful genes persist and widely disseminate in nature. The unbiased determination of the most successful genes requires access to sequence data from a wide range of phylogenetic taxa and ecosystems, which has finally become achievable thanks to the deluge of genomic and metagenomic sequences. Here, we analyzed 10 million protein-encoding genes and gene tags in sequenced bacterial, archaeal, eukaryotic and viral genomes and metagenomes, and our analysis demonstrates that genes encoding transposases are the most prevalent genes in nature. The finding that these genes, classically considered as selfish genes, outnumber essential or housekeeping genes suggests that they offer selective advantage to the genomes and ecosystems they inhabit, a hypothesis in agreement with an emerging body of literature. Their mobile nature not only promotes dissemination of transposable elements within and between genomes but also leads to mutations and rearrangements that can accelerate biological diversification and—consequently—evolution. By securing their own replication and dissemination, transposases guarantee to thrive so long as nucleic acid-based life forms exist.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER). Biological Systems Science Division

Grant/Contract Number:: AC02-06CH11357

OSTI ID:: 1625476

Journal Information:: Nucleic Acids Research, Journal Name: Nucleic Acids Research Journal Issue: 13 Vol. 38; ISSN 0305-1048

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

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TnpPred: A Web Service for the Robust Prediction of Prokaryotic Transposases Riadi, Gonzalo; Medina-Moenne, Cristobal; Holmes, David S. Comparative and Functional Genomics, Vol. 2012 https://doi.org/10.1155/2012/678761	journal	January 2012
Combining Strengths for Multi-genome Visual Analytics Comparison Diaz-del-Pino, Sergio; Rodriguez-Brazzarola, Pablo; Perez-Wohlfeil, Esteban Bioinformatics and Biology Insights, Vol. 13 https://doi.org/10.1177/1177932218825127	journal	January 2019
A bacterial genome in transition - an exceptional enrichment of IS elements but lack of evidence for recent transposition in the symbiont Amoebophilus asiaticus Schmitz-Esser, Stephan; Penz, Thomas; Spang, Anja BMC Evolutionary Biology, Vol. 11, Issue 1 https://doi.org/10.1186/1471-2148-11-270	journal	September 2011
A bioinformatic analysis of ribonucleotide reductase genes in phage genomes and metagenomes Dwivedi, Bhakti; Xue, Bingjie; Lundin, Daniel BMC Evolutionary Biology, Vol. 13, Issue 1 https://doi.org/10.1186/1471-2148-13-33	journal	January 2013
Crypton transposons: identification of new diverse families and ancient domestication events Kojima, Kenji K.; Jurka, Jerzy Mobile DNA, Vol. 2, Issue 1 https://doi.org/10.1186/1759-8753-2-12	journal	January 2011
ISsaga is an ensemble of web-based methods for high throughput identification and semi-automatic annotation of insertion sequences in prokaryotic genomes Varani, Alessandro M.; Siguier, Patricia; Gourbeyre, Edith Genome Biology, Vol. 12, Issue 3 https://doi.org/10.1186/gb-2011-12-3-r30	journal	January 2011
The complete genome sequence of Dickeya zeae EC1 reveals substantial divergence from other Dickeya strains and species Zhou, Jianuan; Cheng, Yingying; Lv, Mingfa BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-1545-x	journal	August 2015
Heritable gene expression differences between apomictic clone members in Taraxacum officinale: Insights into early stages of evolutionary divergence in asexual plants Ferreira de Carvalho, Julie; Oplaat, Carla; Pappas, Nikolaos BMC Genomics, Vol. 17, Issue 1 https://doi.org/10.1186/s12864-016-2524-6	journal	March 2016
Comparative genomic analysis of six new-found integrative conjugative elements (ICEs) in Vibrio alginolyticus Luo, Peng; He, Xiangyan; Wang, Yanhong BMC Microbiology, Vol. 16, Issue 1 https://doi.org/10.1186/s12866-016-0692-9	journal	May 2016
Firmicutes-enriched IS1447 represents a group of IS3-family insertion sequences exhibiting unique + 1 transcriptional slippage Liu, Ya-Jun; Qi, Kuan; Zhang, Jie Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1304-8	journal	November 2018
IS982 and kin: new insights into an old IS family Fayad, Nancy; Kallassy Awad, Mireille; Mahillon, Jacques Mobile DNA, Vol. 11, Issue 1 https://doi.org/10.1186/s13100-020-00221-z	journal	July 2020
Compensating for over-production inhibition of the Hsmar1 transposon in Escherichia coli using a series of constitutive promoters Tellier, Michael; Chalmers, Ronald Mobile DNA, Vol. 11, Issue 1 https://doi.org/10.1186/s13100-020-0200-5	journal	January 2020
Oral administration of antibiotics increased the potential mobility of bacterial resistance genes in the gut of the fish Piaractus mesopotamicus Sáenz, Johan S.; Marques, Tamires Valim; Barone, Rafael Simões Coelho Microbiome, Vol. 7, Issue 1 https://doi.org/10.1186/s40168-019-0632-7	journal	February 2019
The Transposon-Like Correia Elements Encode Numerous Strong Promoters and Provide a Potential New Mechanism for Phase Variation in the Meningococcus Siddique, Azeem; Buisine, Nicolas; Chalmers, Ronald PLoS Genetics, Vol. 7, Issue 1 https://doi.org/10.1371/journal.pgen.1001277	journal	January 2011
Hsmar1 Transposition Is Sensitive to the Topology of the Transposon Donor and the Target Claeys Bouuaert, Corentin; Chalmers, Ronald PLoS ONE, Vol. 8, Issue 1 https://doi.org/10.1371/journal.pone.0053690	journal	January 2013
Mobility and Generation of Mosaic Non-Autonomous Transposons by Tn3-Derived Inverted-Repeat Miniature Elements (TIMEs) Szuplewska, Magdalena; Ludwiczak, Marta; Lyzwa, Katarzyna PLoS ONE, Vol. 9, Issue 8 https://doi.org/10.1371/journal.pone.0105010	journal	August 2014
Characterization of Microbial Dysbiosis and Metabolomic Changes in Dogs with Acute Diarrhea Guard, Blake C.; Barr, James W.; Reddivari, Lavanya PLOS ONE, Vol. 10, Issue 5 https://doi.org/10.1371/journal.pone.0127259	journal	May 2015
Contig-Layout-Authenticator (CLA): A Combinatorial Approach to Ordering and Scaffolding of Bacterial Contigs for Comparative Genomics and Molecular Epidemiology Shaik, Sabiha; Kumar, Narender; Lankapalli, Aditya K. PLOS ONE, Vol. 11, Issue 6 https://doi.org/10.1371/journal.pone.0155459	journal	June 2016
Mobilizable antibiotic resistance genes are present in dust microbial communities Ben Maamar, Sarah; Glawe, Adam J.; Brown, Taylor K. PLOS Pathogens, Vol. 16, Issue 1 https://doi.org/10.1371/journal.ppat.1008211	journal	January 2020
Functional characterization of sugarcane mustang domesticated transposases and comparative diversity in sugarcane, rice, maize and sorghum Kajihara, Daniela; Godoy, Fabiana de; Hamaji, Thais Alves Genetics and Molecular Biology, Vol. 35, Issue 3 https://doi.org/10.1590/s1415-47572012005000038	journal	January 2012
The Intra-Dependence of Viruses and the Holobiont Grasis, Juris A. Frontiers in Immunology, Vol. 8 https://doi.org/10.3389/fimmu.2017.01501	journal	November 2017
The green impact: bacterioplankton response toward a phytoplankton spring bloom in the southern North Sea assessed by comparative metagenomic and metatranscriptomic approaches Wemheuer, Bernd; Wemheuer, Franziska; Hollensteiner, Jacqueline Frontiers in Microbiology, Vol. 6 https://doi.org/10.3389/fmicb.2015.00805	journal	August 2015
Metatranscriptomic Analysis Reveals Unexpectedly Diverse Microbial Metabolism in a Biogeochemical Hot Spot in an Alluvial Aquifer Jewell, Talia N. M.; Karaoz, Ulas; Bill, Markus Frontiers in Microbiology, Vol. 8, Article No. 40 https://doi.org/10.3389/fmicb.2017.00040	journal	January 2017
RNase H As Gene Modifier, Driver of Evolution and Antiviral Defense Moelling, Karin; Broecker, Felix; Russo, Giancarlo Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.01745	journal	September 2017
A Potential Role for Epigenetic Processes in the Acclimation Response to Elevated pCO2 in the Model Diatom Phaeodactylum tricornutum Huang, Ruiping; Ding, Jiancheng; Gao, Kunshan Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.03342	journal	January 2019
The Role of Transposable Elements in Speciation Serrato-Capuchina, Antonio; Matute, Daniel Genes, Vol. 9, Issue 5 https://doi.org/10.3390/genes9050254	journal	May 2018
RNase H As Gene Modifier, Driver of Evolution and Antiviral Defense Karin, Moelling,; Felix, Broecker,; Giancarlo, Russo, ETH Zurich https://doi.org/10.3929/ethz-b-000191353	text	January 2017
Gene copy number variation and its significance in cyanobacterial phylogeny Schirrmeister, Bettina E.; Dalquen, Daniel A.; Anisimova, Maria BioMed Central https://doi.org/10.5167/uzh-77627	text	January 2012
Sequencing at sea: Challenges and experiences in Ion Torrent PGM sequencing during the 2013 Southern Line Islands Research Expedition Lim, Yan Wei; Cuevas, Daniel A.; Silva, Genivaldo Gueiros Z. PeerJ Preprints https://doi.org/10.7287/peerj.preprints.433	posted_content	July 2014
Multiple serine transposase dimers assemble the transposon-end synaptic complex during IS607-family transposition Chen, Wenyang; Mandali, Sridhar; Hancock, Stephen P. eLife, Vol. 7 https://doi.org/10.7554/elife.39611	journal	October 2018
Casposase structure and the mechanistic link between DNA transposition and spacer acquisition by CRISPR-Cas Hickman, Alison B.; Kailasan, Shweta; Genzor, Pavol eLife, Vol. 9 https://doi.org/10.7554/elife.50004	journal	January 2020
Sequencing at sea: challenges and experiences in Ion Torrent PGM sequencing during the 2013 Southern Line Islands Research Expedition Lim, Yan Wei; Cuevas, Daniel A.; Silva, Genivaldo Gueiros Z. PeerJ, Vol. 2 https://doi.org/10.7717/peerj.520	journal	January 2014

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