General features and properties of insertion sequence elements

Previous ...

IS expansion, elimination and genome streamlining

IS can undergo massive expansion and loss accompanied by gene inactivation and decay, genome rearrangement and genome reduction. Clearly, host lifestyle strongly influences these IS-mediated effects on genome structure, presumably by determining the level of genetic isolation of the microbial population. Factors affecting this include: whether the bacteria are ectosymbionts, primary endosymbionts having long evolutionary histories with their hosts, or secondary endosymbionts with more recent associations; whether they are transmitted in a strictly vertical manner or pass through a step of horizontal transfer via reinfection or passage through a second host vector (Bordenstein & Reznikoff, 2005, Moya, et al., 2008).

IS expansion has been commonly observed in bacteria with recently adopted fastidious, host-restricted lifestyles. Those which may have more ancient host-restricted lifestyles (e.g. Wigglesworthia in the Tsetse fly; Buchnera aphidicola in the aphid; Blochmannia floridanus in the ant) tend to possess small streamlined genomes with few pseudogenes or MGEs (see (Bordenstein & Reznikoff, 2005, Moya, et al., 2008)).

One view is that IS expansion is an early step in this genome reduction process (Moran & Plague, 2004, Touchon & Rocha, 2007, Gil, et al., 2008, Plague, et al., 2008) (Fig 1.21.1; (Siguier, et al., 2014)). This results from a decrease in strength and efficacy of purifying selection due to the shift from free to intracellular lifestyles (Moran & Plague, 2004). It is reinforced by a phenomenon known as Muller's ratchet which leads to the irreversible accumulation of mutations in a confined intracellular environment (Moran, 1996, Andersson & Kurland, 1998, Silva, et al., 2003). In the nutritionally rich environment of the host, many genes of free-living bacteria are inessential. Enhanced genetic drift would allow fixation of slightly deleterious mutations in the population, facilitated by the occurrence of successive population bottlenecks. The more genetically isolated the bacterial population, the more acute would be the effect. Indeed, many examples of this can be found among intracellular endosymbionts. This initial stage of transition from free-living to host-dependence would therefore result in an accumulation of pseudogenes which will eventually be eliminated by so-called deletional bias (Mira, et al., 2001). Clearly, the activities of MGEs, and of ISs in particular, make them important instruments in these processes. IS expansion would contribute to pseudogenisation by IS-mediated intrachromosomal recombination and genome reduction (Andersson & Andersson, 1999, Lawrence, et al., 2001, Mira, et al., 2001) by their capacities to generate deletions (see (Mahillon & Chandler, 1998)). Such deletions would also eventually lead to complete or partial elimination of the ISs themselves. These processes are shown schematically in Fig 1.21.1.

There are many striking examples of IS expansions in bacterial genomes. The first to be identified was Shigella from the pre-genomics era (Nyman, et al., 1981, Ohtsubo, et al., 1981). But IS expansion identified from sequenced genomes has been implicated in generating the present day Bordetella pertussis and B. parapertusis, Yersinia pestis, Enterococcus faecium, Mycobacterium ulcerans and many others. In at least some of these cases it has been argued that large scale genome rearrangements and deletions associated with IS expansion have improved the ability of the bacterium to combat host defenses for example by changing surface antigens and regulatory circuitry (Parkhill & Thomson, 2003). This has been particularly well documented in the Bordetellae (Parkhill, et al., 2003, Preston, et al., 2004).

The phenomenon is also common among endosymbionts such as Wolbachia sp. These are considered ancient endosymbionts which might be expected to possess more streamlined genomes. However, evidence has been presented that they have been subjected to several waves of invasion and elimination of ISs (Cerveau, et al., 2011). This may be related to the fact that they are not strictly transmitted vertically but may also undergo relatively low levels of horizontal transmission and coinfection. Other symbionts or host-restricted bacteria also contain high IS loads. These include organisms such as Orientia tsutsugamushi, various Rickettsia, Sodalis glossinidius, Amoebophilus asiaticus 5a2, the γ1 symbiont of the marine oligochaete Olavius algarvensis, the Bacteroidete Cardinium hertigii, a symbiont of the parasitic wasp Encarsia pergandiella, and the primary symbionts of grain weevils. These obligate intracellular bacteria may carry intercellular MGEs such as phage (Hsia, et al., 2000 , Read, et al., 2000) and conjugative elements (Blanc, et al., 2007) capable of acting as IS vectors and motors of horizontal gene transfer. Similar arguments might be used for other niche-restricted prokaryotes to explain increased IS loads found in some extremophiles (e.g. Sulfolobus solfataricus and certain cyanobacteria) (Papke, et al., 2003, Brugger, et al., 2004, Allewalt, et al., 2006, Filee, et al., 2007).

Although IS expansion is generally assumed to occur stochastically over periods of evolutionary time, it has recently been observed that the Olavius algarvensis symbionts express significant levels of transposase (Kleiner, et al., 2013). This raises the possibility that transposase expression is deregulated in this symbiont system. However, another symbiont, Amoebophilus asiaticus, with a high IS load, shows no evidence of recent transposition activity in spite of extensive IS transcription (Schmitz-Esser, et al., 2011). In view of the time scales involved, only a very small but sustained increase in transposition activity might be needed to give rise to the high loads observed. Further exploration of the relationship between IS gene expression and transposition activity is clearly essential to understanding the dynamics of ISs in these and other systems.

Of course, different ISs are involved in different expansions and it is therefore important to understand IS diversity and properties. This is clearly evident in studies concerning the behavior of IS on storage of bacterial strains where certain IS appear more active than others (Naas, et al., 1994, Naas, et al., 1995).Their detailed effects on the host genome will depend on their particular transposition mechanisms. For example, IS target specificity will have profound effects on the way the host genome is shaped.

    References :
  • Allewalt JP, Bateson MM, Revsbech NP, Slack K & Ward DM (2006) Effect of temperature and light on growth of and photosynthesis by Synechococcus isolates typical of those predominating in the octopus spring microbial mat community of Yellowstone National Park. Appl Environ Microbiol 72: 544-550.
  • Andersson JO & Andersson SG (1999) Insights into the evolutionary process of genome degradation. Curr Opin Genet Dev 9: 664-671.
  • Andersson SG & Kurland CG (1998) Reductive evolution of resident genomes. Trends Microbiol 6: 263-268.
  • Blanc G, Ogata H, Robert C, Audic S, Claverie J-M & Raoult D (2007) Lateral gene transfer between obligate intracellular bacteria: Evidence from the Rickettsia massiliae genome. Genome Research 17: 1657-1664.
  • Bordenstein SR & Reznikoff WS (2005) Mobile DNA in obligate intracellular bacteria. Nat Rev Microbiol 3: 688-699.
  • Brugger K, Torarinsson E, Redder P, Chen L & Garrett RA (2004) Shuffling of Sulfolobus genomes by autonomous and non-autonomous mobile elements. Biochem Soc Trans 32: 179-183.
  • Cerveau N, Leclercq S, Leroy E, Bouchon D & Cordaux R (2011) Short- and Long-term Evolutionary Dynamics of Bacterial Insertion Sequences: Insights from Wolbachia Endosymbionts. Genome Biology and Evolution 3: 1175-1186.
  • Filee J, Siguier P & Chandler M (2007) Insertion sequence diversity in archaea. Microbiol Mol Biol Rev 71: 121-157.
  • Gil R, Belda E, Gosalbes MJ, et al. (2008) Massive presence of insertion sequences in the genome of SOPE, the primary endosymbiont of the rice weevil Sitophilus oryzae. Int Microbiol 11: 41-48.
  • Hsia R, Ohayon H, Gounon P, Dautry-Varsat A & Bavoil PM (2000) Phage infection of the obligate intracellular bacterium, Chlamydia psittaci strain guinea pig inclusion conjunctivitis. Microbes Infect 2: 761-772.
  • Kleiner M, Young JC, Shah M, VerBerkmoes NC & Dubilier N (2013) Metaproteomics reveals abundant transposase expression in mutualistic endosymbionts. MBio 4: e00223-00213.
  • Lawrence JG, Hendrix RW & Casjens S (2001) Where are the pseudogenes in bacterial genomes? Trends Microbiol 9: 535-540.
  • Mahillon J & Chandler M (1998) Insertion sequences. Microbiol Mol Biol Rev 62: 725-774.
  • Mira A, Ochman H & Moran NA (2001) Deletional bias and the evolution of bacterial genomes. Trends Genet 17: 589-596.
  • Moran NA (1996) Accelerated evolution and Muller's rachet in endosymbiotic bacteria. Proc Natl Acad Sci U S A 93: 2873-2878.
  • Moran NA & Plague GR (2004) Genomic changes following host restriction in bacteria. Current Opinion in Genetics & Development 14: 627-633.
  • Moya A, Pereto J, Gil R & Latorre A (2008) Learning how to live together: genomic insights into prokaryote-animal symbioses. Nat Rev Genet 9: 218-229.
  • Naas T, Blot M, Fitch WM & Arber W (1994) Insertion sequence-related genetic variation in resting Escherichia coli K-12. Genetics 136: 721-730.
  • Naas T, Blot M, Fitch WM & Arber W (1995) Dynamics of IS-related genetic rearrangements in resting Escherichia coli K-12. Mol.Biol.Evol. 12: 198-207.
  • Nyman K, Nakamura K, Ohtsubo H & Ohtsubo E (1981) Distribution of the insertion sequence IS1 in gram-negative bacteria. Nature 289: 609-612.
  • Ohtsubo H, Nyman K, Doroszkiewicz W & Ohtsubo E (1981) Multiple copies of iso-insertion sequences of IS1 in Shigella dysenteriae chromosome. Nature 292: 640-643.
  • Papke RT, Ramsing NB, Bateson MM & Ward DM (2003) Geographical isolation in hot spring cyanobacteria. Environ Microbiol 5: 650-659.
  • Parkhill J & Thomson N (2003) Evolutionary strategies of human pathogens. Cold Spring Harb Symp Quant Biol 68: 151-158.
  • Parkhill J, Sebaihia M, Preston A, et al. (2003) Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 35: 32-40.
  • Plague GR, Dunbar HE, Tran PL & Moran NA (2008) Extensive proliferation of transposable elements in heritable bacterial symbionts. J Bacteriol 190: 777-779.
  • Preston A, Parkhill J & Maskell DJ (2004) The Bordetellae: lessons from genomics. 2: 379-390.
  • Read TD, Fraser CM, Hsia RC & Bavoil PM (2000) Comparative analysis of Chlamydia bacteriophages reveals variation localized to a putative receptor binding domain. Microb Comp Genomics 5: 223-231.
  • Schmitz-Esser S, Penz T, Spang A & Horn M (2011) A bacterial genome in transition--an exceptional enrichment of IS elements but lack of evidence for recent transposition in the symbiont Amoebophilus asiaticus. BMC Evol Biol 11: 270.
  • Siguier P, Gourbeyre E & Chandler M (2014) Bacterial insertion sequences: their genomic impact and diversity. FEMS Microbiol Rev.
  • Silva FJ, Latorre A & Moya A (2003) Why are the genomes of endosymbiotic bacteria so stable? Trends Genet 19: 176-180.
  • Touchon M & Rocha EP (2007) Causes of insertion sequences abundance in prokaryotic genomes. Mol Biol Evol 24: 969-981.