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
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.
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