Difference between revisions of "General Information/ Impact of IS on Genome Evolution - The Importance of Time Scale"

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'''<big>I</big>'''Ss have had an important impact on genome structure and function. Several of these effects are considered in the following sections. In this context it is useful to understand the time scales involved in these processes since they are often confounded. Evolutionary time is used to compare species (106 years), historical time in comparisons within or between populations (102 - 104 years), variety time in selection experiments (1 - 102 years), and laboratory time for ongoing events such as experimental measurement of transposition frequencies or in biochemical analyses (10-3 - 1 years) ([https://researchportal.helsinki.fi/en/persons/alan-schulman/publications/ Alan Schulman], pers comm.). Thus a “burst” of transposition in evolutionary time is many orders of magnitude longer than a “burst” of transposition in experimental biology. <br />
+
'''<big>I</big>'''Ss have had an important impact on genome structure and function. Several of these effects are considered in the following sections. In this context it is useful to understand the time scales involved in these processes since they are often confounded. Evolutionary time is used to compare species (10<sup>6</sup> years), '''historical time''' in comparisons within or between populations (10<sup>2</sup> - 10<sup>4</sup> years), '''variety time''' in selection experiments (1 - 10<sup>2</sup> years), and '''laboratory time''' for ongoing events such as experimental measurement of transposition frequencies or in biochemical analyses (10<sup>-3</sup> - 1 years) ([https://researchportal.helsinki.fi/en/persons/alan-schulman/publications/ Alan Schulman], pers comm.). Thus a “'''burst'''” of transposition in evolutionary time is many orders of magnitude longer than a “'''burst'''” of transposition in experimental biology. <br />
  
 
===IS expansion, elimination and genome streamlining===
 
===IS expansion, elimination and genome streamlining===
[[Image:1.21.1.png|thumb|510x510px|'''Fig 1.21.1.''' IS expansion and genome streamlining schema.|alt=|border]]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<ref><nowiki><pubmed>16138097</pubmed></nowiki></ref><ref><nowiki><pubmed>18974066</pubmed></nowiki></ref><ref><nowiki><pubmed>18268509</pubmed></nowiki></ref><ref><nowiki><pubmed>11672844</pubmed></nowiki></ref>.
+
[[Image:1.21.1.png|thumb|620x620px|'''Fig.15.1.''' IS expansion and genome streamlining schema.IS expansion, elimination, and genome ‘streamlining’. The figure shows schematically from left to right events leading to the evolution of host-dependence in bacteria.  
  
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 <ref><nowiki><pubmed>16138097</pubmed></nowiki></ref><ref><nowiki><pubmed>18268509</pubmed></nowiki></ref>).
+
'''(i)''' The parental (ancestral) chromosome including a low number of resident IS (red arcs). Note that the entire genome might also include transmissible plasmids carrying their own IS load, which can in principle undergo transposition into the chromosome.
  
One view is that IS expansion is an early step in this genome reduction process<ref><nowiki><pubmed>17981967</pubmed></nowiki></ref><ref><nowiki><pubmed>15531157</pubmed></nowiki></ref><ref><nowiki><pubmed>17251179</pubmed></nowiki></ref><ref><nowiki><pubmed>18683631</pubmed></nowiki></ref> [[:Image:1.21.1.png|(Fig.1.21.1]]; <ref><nowiki><pubmed>24499397</pubmed></nowiki></ref><ref><nowiki><pubmed>26104715</pubmed></nowiki></ref>). This results from a decrease in strength and efficacy of purifying selection due to the shift from free to intracellular lifestyles<ref><nowiki><pubmed>15531157</pubmed></nowiki></ref>. It is reinforced by a phenomenon known as Muller’s ratchet which leads to the irreversible accumulation of mutations in a confined intracellular environment<ref><nowiki><pubmed>8610134</pubmed></nowiki></ref><ref><nowiki><pubmed>9717214</pubmed></nowiki></ref><ref><nowiki><pubmed>12683967</pubmed></nowiki></ref>. 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<ref><nowiki><pubmed>11585665</pubmed></nowiki></ref><ref><nowiki><pubmed>11790257</pubmed></nowiki></ref>. 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<ref><nowiki><pubmed>9717214</pubmed></nowiki></ref><ref><nowiki><pubmed>11585665</pubmed></nowiki></ref><ref><nowiki><pubmed>10607609</pubmed></nowiki></ref><ref><nowiki><pubmed>11825713</pubmed></nowiki></ref> by their capacities to generate deletions (see <ref><nowiki><pubmed>9729608</pubmed></nowiki></ref>). Such deletions would also eventually lead to complete or partial elimination of the ISs themselves. These processes are shown schematically in [[:Image:1.21.1.png|Fig.1.21.1]].
+
'''(ii)''' IS expansion occurs as a result of isolation and the formation of population bottlenecks within a host organism. This is accompanied by mutation promoted by the insertion of new IS copies and by their related transposition activities of deletion and rearrangement. These genome rearrangements can also occur by homologous recombination between identical IS copies.  
  
There are many striking examples of IS expansions in bacterial genomes. The first to be identified was ''Shigella'' from the pre-genomics era<ref><nowiki><pubmed>6258088</pubmed></nowiki></ref><ref><nowiki><pubmed>6265806</pubmed></nowiki></ref>. 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. This has been particularly well documented in the Bordetellae<ref><nowiki><pubmed>12910271</pubmed></nowiki></ref><ref><nowiki><pubmed>15100691</pubmed></nowiki></ref>.
+
'''(iii)''' With time IS will have a tendency to undergo deletion with adjacent DNA sequences in the absence of direct selection. This leads to a reduction in genome size.  
  
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<ref><nowiki><pubmed>21940637</pubmed></nowiki></ref>. 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  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<ref><nowiki><pubmed>10955956</pubmed></nowiki></ref><ref><nowiki><pubmed>12682364</pubmed></nowiki></ref> and conjugative elements<ref><nowiki><pubmed>17916642</pubmed></nowiki></ref> 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)<ref><nowiki><pubmed>12871232</pubmed></nowiki></ref><ref><nowiki><pubmed>15046567</pubmed></nowiki></ref><ref><nowiki><pubmed>16391090</pubmed></nowiki></ref><ref><nowiki><pubmed>17347521</pubmed></nowiki></ref>.
+
'''(iv)''' Eventually, extensive deletion will lead to the generation of non-autonomous IS fragments and their elimination.  
  
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<ref><nowiki><pubmed>23781067</pubmed></nowiki></ref>. 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<ref><nowiki><pubmed>21943072</pubmed></nowiki></ref>. 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.
+
'''(v)''' This gives rise to streamlined, IS ‘free’ genomes which may become ‘reinfected’ by IS on rare contact with other, IS-carrying strains or infection by IS-carrying bacteriophage.|alt=|border]]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<ref><pubmed>16138097</pubmed></ref><ref><pubmed>18974066</pubmed></ref><ref name=":0"><pubmed>18268509</pubmed>
  
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<ref><nowiki><pubmed>7911771</pubmed></nowiki></ref><ref><nowiki><pubmed>7700149</pubmed></nowiki></ref>.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.
+
</ref><ref><pubmed>11672844</pubmed></ref>.
 +
 
 +
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. ''[[wikipedia:Wigglesworthia_glossinidia|Wigglesworthia]]'' in the [[wikipedia:Tsetse_fly|Tsetse fly]]; ''[[wikipedia:Buchnera_(bacterium)|Buchnera aphidicola]]'' in the aphid; ''[[wikipedia:Blochmannia|Blochmannia floridanus]]'' in the ant) tend to possess small streamlined genomes with few pseudogenes or MGEs (see <ref><pubmed>16138097</pubmed></ref><ref name=":0" />).
 +
 
 +
One view is that IS expansion is an early step in this genome reduction process<ref><pubmed>17981967</pubmed></ref><ref name=":1"><pubmed>15531157</pubmed>
 +
 
 +
</ref><ref><pubmed>17251179</pubmed></ref><ref><pubmed>18683631</pubmed></ref> [[:Image:1.21.1.png|(Fig.15.1]]; <ref><pubmed>24499397</pubmed></ref><ref><pubmed>26104715</pubmed></ref>). This results from a decrease in strength and efficacy of purifying selection due to the shift from free to intracellular lifestyles<ref name=":1" />. It is reinforced by a phenomenon known as Muller’s ratchet which leads to the irreversible accumulation of mutations in a confined intracellular environment<ref><pubmed>8610134</pubmed></ref><ref name=":2"><pubmed>9717214</pubmed>
 +
 
 +
</ref><ref><pubmed>12683967</pubmed></ref>. 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<ref name=":3"><pubmed>11585665</pubmed>
 +
 
 +
</ref><ref><pubmed>11790257</pubmed></ref>. 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<ref name=":2" /><ref name=":3" /><ref><pubmed>10607609</pubmed></ref><ref><pubmed>11825713</pubmed></ref> by their capacities to generate deletions (see <ref><pubmed>9729608</pubmed></ref>). Such deletions would also eventually lead to complete or partial elimination of the ISs themselves. These processes are shown schematically in [[:Image:1.21.1.png|Fig.15.1]].
 +
 
 +
There are many striking examples of IS expansions in bacterial genomes. The first to be identified was ''[[wikipedia:Shigella|Shigella]]'' from the pre-genomics era<ref><pubmed>6258088</pubmed></ref><ref><pubmed>6265806</pubmed></ref>. But IS expansion identified from sequenced genomes has been implicated in generating the present day ''[[wikipedia:Bordetella|Bordetella]]'' pertussis and ''[[wikipedia:Bordetella_parapertussis|B. parapertusis]]'', ''[[wikipedia:Yersinia_pestis|Yersinia pestis]]'', ''[[wikipedia:Enterococcus_faecium|Enterococcus faecium]]'', ''[[wikipedia:Mycobacterium_ulcerans|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. This has been particularly well documented in the Bordetellae<ref><pubmed>12910271</pubmed></ref><ref><pubmed>15100691</pubmed></ref>.
 +
 
 +
The phenomenon is also common among endosymbionts such as ''[[wikipedia:Wolbachia|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<ref><pubmed>21940637</pubmed></ref>. 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 ''[[wikipedia:Orientia_tsutsugamushi|Orientia tsutsugamushi]]'', various ''[[wikipedia:Rickettsia|Rickettsia]]'', ''[[wikipedia:Sodalis_glossinidius|Sodalis glossinidius]]'', [https://www.uniprot.org/proteomes/UP000001227 ''Amoebophilus asiaticus'' 5a2], the  symbiont of the marine oligochaete ''[[wikipedia:Olavius_algarvensis|Olavius algarvensis]]'', the Bacteroidete ''[[wikipedia:Cardinium|Cardinium hertigii]]'', a symbiont of the parasitic wasp ''[[wikipedia:Encarsia|Encarsia pergandiella]]'', and the primary symbionts of grain weevils. These obligate intracellular bacteria may carry intercellular MGEs such as phage<ref><pubmed>10955956</pubmed></ref><ref><pubmed>12682364</pubmed></ref> and conjugative elements<ref><pubmed>17916642</pubmed></ref> 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. ''[[wikipedia:Sulfolobus_solfataricus|Sulfolobus solfataricus]]'' and certain cyanobacteria)<ref><pubmed>12871232</pubmed></ref><ref><pubmed>15046567</pubmed></ref><ref><pubmed>16391090</pubmed></ref><ref><pubmed>17347521</pubmed></ref>.
 +
 
 +
Although IS expansion is generally assumed to occur stochastically over periods of evolutionary time, it has recently been observed that the ''[[wikipedia:Olavius_algarvensis|Olavius algarvensis]]'' symbionts express significant levels of transposase<ref><pubmed>23781067</pubmed></ref>. This raises the possibility that transposase expression is deregulated in this symbiont system. However, another symbiont, ''[https://www.uniprot.org/proteomes/UP000001227 Amoebophilus asiaticus]'', with a high IS load, shows no evidence of recent transposition activity in spite of extensive IS transcription<ref><pubmed>21943072</pubmed></ref>. 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<ref><pubmed>7911771</pubmed></ref><ref><pubmed>7700149</pubmed></ref>.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.
  
 
==Bibliography==
 
==Bibliography==
 
<references />
 
<references />

Latest revision as of 21:20, 9 August 2021

ISs have had an important impact on genome structure and function. Several of these effects are considered in the following sections. In this context it is useful to understand the time scales involved in these processes since they are often confounded. Evolutionary time is used to compare species (106 years), historical time in comparisons within or between populations (102 - 104 years), variety time in selection experiments (1 - 102 years), and laboratory time for ongoing events such as experimental measurement of transposition frequencies or in biochemical analyses (10-3 - 1 years) (Alan Schulman, pers comm.). Thus a “burst” of transposition in evolutionary time is many orders of magnitude longer than a “burst” of transposition in experimental biology.

IS expansion, elimination and genome streamlining

Fig.15.1. IS expansion and genome streamlining schema.IS expansion, elimination, and genome ‘streamlining’. The figure shows schematically from left to right events leading to the evolution of host-dependence in bacteria. (i) The parental (ancestral) chromosome including a low number of resident IS (red arcs). Note that the entire genome might also include transmissible plasmids carrying their own IS load, which can in principle undergo transposition into the chromosome. (ii) IS expansion occurs as a result of isolation and the formation of population bottlenecks within a host organism. This is accompanied by mutation promoted by the insertion of new IS copies and by their related transposition activities of deletion and rearrangement. These genome rearrangements can also occur by homologous recombination between identical IS copies. (iii) With time IS will have a tendency to undergo deletion with adjacent DNA sequences in the absence of direct selection. This leads to a reduction in genome size. (iv) Eventually, extensive deletion will lead to the generation of non-autonomous IS fragments and their elimination. (v) This gives rise to streamlined, IS ‘free’ genomes which may become ‘reinfected’ by IS on rare contact with other, IS-carrying strains or infection by IS-carrying bacteriophage.

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[1][2][3][4].

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 [5][3]).

One view is that IS expansion is an early step in this genome reduction process[6][7][8][9] (Fig.15.1; [10][11]). This results from a decrease in strength and efficacy of purifying selection due to the shift from free to intracellular lifestyles[7]. It is reinforced by a phenomenon known as Muller’s ratchet which leads to the irreversible accumulation of mutations in a confined intracellular environment[12][13][14]. 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[15][16]. 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[13][15][17][18] by their capacities to generate deletions (see [19]). Such deletions would also eventually lead to complete or partial elimination of the ISs themselves. These processes are shown schematically in Fig.15.1.

There are many striking examples of IS expansions in bacterial genomes. The first to be identified was Shigella from the pre-genomics era[20][21]. 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. This has been particularly well documented in the Bordetellae[22][23].

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[24]. 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 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[25][26] and conjugative elements[27] 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)[28][29][30][31].

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[32]. 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[33]. 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[34][35].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.

Bibliography

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  3. 3.0 3.1 Moya A, Peretó J, Gil R, Latorre A . Learning how to live together: genomic insights into prokaryote-animal symbioses. - Nat Rev Genet: 2008 Mar, 9(3);218-29 [PubMed:18268509] [DOI]
  4. Silva FJ, Latorre A, Moya A . Genome size reduction through multiple events of gene disintegration in Buchnera APS. - Trends Genet: 2001 Nov, 17(11);615-8 [PubMed:11672844] [DOI]
  5. Bordenstein SR, Reznikoff WS . Mobile DNA in obligate intracellular bacteria. - Nat Rev Microbiol: 2005 Sep, 3(9);688-99 [PubMed:16138097] [DOI]
  6. Plague GR, Dunbar HE, Tran PL, Moran NA . Extensive proliferation of transposable elements in heritable bacterial symbionts. - J Bacteriol: 2008 Jan, 190(2);777-9 [PubMed:17981967] [DOI]
  7. 7.0 7.1 Moran NA, Plague GR . Genomic changes following host restriction in bacteria. - Curr Opin Genet Dev: 2004 Dec, 14(6);627-33 [PubMed:15531157] [DOI]
  8. Touchon M, Rocha EP . Causes of insertion sequences abundance in prokaryotic genomes. - Mol Biol Evol: 2007 Apr, 24(4);969-81 [PubMed:17251179] [DOI]
  9. Gil R, Belda E, Gosalbes MJ, Delaye L, Vallier A, Vincent-Monégat C, Heddi A, Silva FJ, Moya A, Latorre A . Massive presence of insertion sequences in the genome of SOPE, the primary endosymbiont of the rice weevil Sitophilus oryzae. - Int Microbiol: 2008 Mar, 11(1);41-8 [PubMed:18683631]
  10. Siguier P, Gourbeyre E, Chandler M . Bacterial insertion sequences: their genomic impact and diversity. - FEMS Microbiol Rev: 2014 Sep, 38(5);865-91 [PubMed:24499397] [DOI]
  11. Siguier P, Gourbeyre E, Varani A, Ton-Hoang B, Chandler M . Everyman's Guide to Bacterial Insertion Sequences. - Microbiol Spectr: 2015 Apr, 3(2);MDNA3-0030-2014 [PubMed:26104715] [DOI]
  12. Moran NA . Accelerated evolution and Muller's rachet in endosymbiotic bacteria. - Proc Natl Acad Sci U S A: 1996 Apr 2, 93(7);2873-8 [PubMed:8610134] [DOI]
  13. 13.0 13.1 Andersson SG, Kurland CG . Reductive evolution of resident genomes. - Trends Microbiol: 1998 Jul, 6(7);263-8 [PubMed:9717214] [DOI]
  14. Silva FJ, Latorre A, Moya A . Why are the genomes of endosymbiotic bacteria so stable? - Trends Genet: 2003 Apr, 19(4);176-80 [PubMed:12683967] [DOI]
  15. 15.0 15.1 Mira A, Ochman H, Moran NA . Deletional bias and the evolution of bacterial genomes. - Trends Genet: 2001 Oct, 17(10);589-96 [PubMed:11585665] [DOI]
  16. Moran NA, Mira A . The process of genome shrinkage in the obligate symbiont Buchnera aphidicola. - Genome Biol: 2001, 2(12);RESEARCH0054 [PubMed:11790257] [DOI]
  17. Andersson JO, Andersson SG . Insights into the evolutionary process of genome degradation. - Curr Opin Genet Dev: 1999 Dec, 9(6);664-71 [PubMed:10607609] [DOI]
  18. Lawrence JG, Hendrix RW, Casjens S . Where are the pseudogenes in bacterial genomes? - Trends Microbiol: 2001 Nov, 9(11);535-40 [PubMed:11825713] [DOI]
  19. Mahillon J, Chandler M . Insertion sequences. - Microbiol Mol Biol Rev: 1998 Sep, 62(3);725-74 [PubMed:9729608]
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