Insertion sequence distribution bias in Archaea

Insertion sequences (IS) are common transposable elements in Archaea. Intergenic IS elements are usually less harmful than intragenic ISs, simply because they are less likely to disrupt host gene function. However, because regulatory sequences are intergenic and upstream of genes, we hypothesized that not all intergenic regions are selectively equivalent for IS insertion. We tested this hypothesis by analyzing the distributions of intergenic IS elements within 155 fully sequenced archaeal genomes. Of the 22 genomes with enough IS elements for statistical analysis, five have significantly fewer ISs between divergently oriented neighboring genes than expected by chance, and seven have significantly more ISs between convergently oriented genes. Furthermore, of the 85 genomes with at least one expected IS within each of the three possible neighboring gene orientations (i.e., divergent, convergent, and tandem), 73 genomes have fewer ISs between divergently oriented genes than expected, and 60 have more ISs between convergently oriented genes than expected (both values deviate significantly from binomial probabilities of random distribution). We suspect that these non-random IS distributions are molded by natural selection resulting from differential disruption of neighboring gene regulation, and that this selective pressure has affected transposable element distributions in prokaryotes for billions of years.

[1]  W. G. Cochran Some Methods for Strengthening the Common χ 2 Tests , 1954 .

[2]  Tatiana Tatusova,et al.  NCBI Reference Sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins , 2004, Nucleic Acids Res..

[3]  C. Fraser,et al.  Recombination and the Nature of Bacterial Speciation , 2007, Science.

[4]  Robert A. Edwards,et al.  Transposases are the most abundant, most ubiquitous genes in nature , 2010, Nucleic acids research.

[5]  J. Soppa Initiation and Regulation of Translation in Halophilic Archaea , 2011 .

[6]  Eduardo P C Rocha,et al.  Causes of insertion sequences abundance in prokaryotic genomes. , 2007, Molecular biology and evolution.

[7]  C. Monsempès,et al.  Multiple Mobile Promoter Regions for the Rare Carbapenem Resistance Gene of Bacteroides fragilis , 2001, Journal of bacteriology.

[8]  Alan M. Lambowitz,et al.  Mobile DNA III , 2002 .

[9]  Mark M. Tanaka,et al.  The distribution of insertion sequences in the genome of Shigella flexneri strain 2457T. , 2007, FEMS microbiology letters.

[10]  P. Siguier,et al.  Insertion Sequence Diversity in Archaea , 2007, Microbiology and Molecular Biology Reviews.

[11]  A. Agresti An introduction to categorical data analysis , 1997 .

[12]  M. Borodovsky,et al.  Leaderless transcripts of the crenarchaeal hyperthermophile Pyrobaculum aerophilum. , 2001, Journal of molecular biology.

[13]  Gordon R. Plague,et al.  Intergenic Transposable Elements Are Not Randomly Distributed in Bacteria , 2010, Genome biology and evolution.

[14]  Erik Kaestner,et al.  The Origins Of Genome Architecture , 2016 .

[15]  Jacques Mahillon,et al.  Insertion Sequences revisited , 2002 .

[16]  Yanhe Ma,et al.  Halophiles and hypersaline environments , 2011 .

[17]  M. Lynch Streamlining and simplification of microbial genome architecture. , 2006, Annual review of microbiology.

[18]  P. Nordmann,et al.  Cephalosporinase over-expression resulting from insertion of ISAba1 in Acinetobacter baumannii. , 2006, Clinical microbiology and infection : the official publication of the European Society of Clinical Microbiology and Infectious Diseases.

[19]  C. Sensen,et al.  Two different and highly organized mechanisms of translation initiation in the archaeon Sulfolobus solfataricus , 2000, Extremophiles.

[20]  W. Doolittle,et al.  Selfish genes, the phenotype paradigm and genome evolution , 1980, Nature.

[21]  Tatiana A. Tatusova,et al.  NCBI Reference Sequence (RefSeq): a curated non-redundant sequence database of genomes, transcripts and proteins , 2004, Nucleic Acids Res..

[22]  Z. She,et al.  Leaderless genes in bacteria: clue to the evolution of translation initiation mechanisms in prokaryotes , 2011, BMC Genomics.

[23]  T. Jukes,et al.  The neutral theory of molecular evolution. , 2000, Genetics.

[24]  M. G. Kidwell,et al.  PERSPECTIVE: TRANSPOSABLE ELEMENTS, PARASITIC DNA, AND GENOME EVOLUTION , 2001, Evolution; international journal of organic evolution.

[25]  Patricia Siguier,et al.  ISfinder: the reference centre for bacterial insertion sequences , 2005, Nucleic Acids Res..

[26]  K. Holsinger The neutral theory of molecular evolution , 2004 .