The impact of insertion sequences on bacterial genome plasticity and adaptability

Figures & data

Figure 1. Possible effects of IS transposition in the function and expression of a target gene. The IS is shown as a blue rectangle delimited by short terminal inverted repeats (IR; blue triangles) and flanked by directed repeats (DR; yellow rectangles) and the target gene as a green rectangle. mRNA transcripts are represented by straight arrows, the target gene promoter sequence is represented by a curved arrow and detailed by −35 and −10 components, and transcriptional start site (+1). For IS elements carrying a complete outward-directed promoter (P_out), the target gene transcription start is altered and denoted as < +1>.

Table 1. IS-mediated gene inactivation affecting virulence, resistance, and metabolism.

Phenotype affected	Gene	IS element	IS family	Organism	Reference
Antibiotic/xenobiotic resistance
β-lactam^R	ampD	IS1669	IS5	P. aeruginosa	Bagge et al. (2002)
	mexR	IS21	IS2	P. aeruginosa	Boutoille et al. (2004)
Carbapenem^R	carO	ISAba125	IS30	A. baumannii	Mussi et al. (2005)
		ISAba825	IS982	A. baumannii	Mussi et al. (2005)
	ompE36	IS903-like	IS903	E. aerogenes	Chen et al. (2008b)
	ompK36	IS5	IS5	K. pneumoniae	Lee et al. (2007)
	oprD	ISPa133	IS13	P. aeruginosa	Ruiz-Martinez et al. (2011)
		ISPa1328	IS256	P. aeruginosa	Al-Bayssari et al. (2015) and Wolter et al. (2004)
		ISPa46	IS256	P. aeruginosa	Diene et al. (2013)
		ISPpu22	IS3	P. putida	Kalantar-Neyestanaki et al. (2015)
		ISPa1635	IS4	P. aeruginosa	Wolter et al. (2004)
		ISPa45	IS4	P. aeruginosa	Rojo-Bezares et al. (2014)
		ISPa26	IS5	P. aeruginosa	Evans and Segal (2007)
		ISPa8	IS5	P. aeruginosa	Fowler and Hanson (2014)
		ISPre2-like	IS5	P. aeruginosa	Al Bayssari et al. (2014)
Cefoxitin^R	ompK36	IS26	IS6	K. pneumoniae	Hernandez-Alles et al. (1999)
		IS903	IS5	K. pneumoniae	Hernandez-Alles et al. (1999)
		IS1	IS1	K. pneumoniae	Hernandez-Alles et al. (1999)
		IS5	IS5	K. pneumoniae	Hernandez-Alles et al. (1999)
Colistin^R	lpxA/lpxC	ISAba11	IS701	A. baumannii	Moffatt et al. (2011)
	mgrB	IS1F-like	IS1	K. pneumoniae	Cannatelli et al. (2014)
		ISKpn14	IS1	K. pneumoniae	Cannatelli et al. (2014), Poirel et al. (2015)
		IS5-like	IS5	K. pneumoniae	Cannatelli et al. (2014) and Poirel et al. (2015)
		ISKpn13	IS5	K. pneumoniae	Poirel et al. (2015)
		ISKpn26-like	IS5	K. oxytoca	Jayol et al. (2015)
Methicillin^R	lytH	IS1182	IS1182	S. aureus	Fujimura and Murakami (2008)
Silver^R	ompR	IS3	IS3	E. coli	Graves et al. (2015)
Solvents^S	acrB	IS30	IS30	E. coli	Kobayashi et al. (2001)
Streptomycin^R	rsmG	ISTth7	IS5	T. thermophilus	Gregory and Dahlberg (2008)
Trimethoprim^R	thyA	ISDra2	IS200/IS605	D. radiodurans	Mennecier et al. (2006)
Toluene^R	srpS	ISS12	IS21	P. putida	Sun and Dennis (2009) and Wery et al. (2001)
Zinc^R	cnrYX	IS1086	IS30	C. metallidurans	Vandecraen et al. (2016)
		IS1087B	IS3	C. metallidurans	Collard et al. (1993), Tibazarwa et al. (2000), Vandecraen et al. (2016)
		IS1088	IS30	C. metallidurans	Vandecraen et al. (2016)
		IS1090	IS256	C. metallidurans	Vandecraen et al. (2016)
		ISRme3	IS3	C. metallidurans	Vandecraen et al. (2016)
		ISRme5	IS481	C. metallidurans	Vandecraen et al. (2016)
		ISRme15	IS3	C. metallidurans	Vandecraen et al. (2016)
Virulence
Biofilm formation	icaC	IS256	IS256	S. aureus	Kiem et al. (2004)
	icaC	IS256	IS256	S. epidermidis	Ziebuhr et al. (1999)
	rsbU	IS256	IS256	S. epidermidis	Conlon et al. (2004)
	sarA	IS256	IS256	S. epidermidis	Conlon et al. (2004)
Capsule biosynthesis	siaA	IS1301	IS5	N. meningitidis	Hammerschmidt et al. (1996)
Capsule O-acetylation	oatWY	IS1301	IS5	N. meningitidis	Claus et al. (2003)
Cell adhesion	rickA	ISRpe1	IS481	R. peacockii	Simser et al. (2005)
Cytotoxin expression	rot	IS256	IS256	S. aureus	Benson et al. (2014)
Eps biosynthesis	gumM	ISXo2	IS1595	X. oryzae	Rajeshwari and Sonti (2000)
		ISXo1	IS5	X. oryzae	Rajeshwari and Sonti (2000)
Gelatinase (biofilm)	fsrC	IS256	IS256	E. faecalis	Perez et al. (2015)
Pneumolysin	ply	IS1515	IS5	S. pneumoniae	Garnier et al. (2007)
Porin (antigen)	porA	IS1301	IS5	N. meningitidis	Newcombe et al. (1998)
Protease	prtP	IS195	IS982	P. gingivalis	Lewis and Macrina (1998)
Metabolism
Cellulose production	cel1	IS1031	IS5	A. xylinum	Coucheron (1991)
Fe^2+ oxidation	resB	ISTfe1	ISL3	T. ferrooxidans	Cabrejos et al. (1999)
Glucose utilization	rpoS	IS1	IS1	E. coli	Gaffe et al. (2011)
Indole production	tna operon	IS1	IS1	Shigella	Rezwan et al. (2004)
Lactocin S production	las operon	IS1163	IS3	L. sakei	Skaugen and Nes (1994)
		IS1520	IS3	L. sakei	Skaugen and Nes (2000)
Lactose utilization	lac operon	ISL4	IS110	L. delbrueckii	Lapierre et al. (2002)
Lipid A biosynthesis	lpxA/lpxC	ISAba11	IS701	A. baumannii	Moffatt et al. (2011)
Naphthalene dissimilation	nahH	ISPst9	ISL3	P. stutzeri	Christie-Oleza et al. (2008)
Poly-γ-glutamate production	comP	IS4Bsu1	IS4	B. subtilis	Nagai et al. (2000)
Protocatechuate catabolism	pcaH pobR	IS1236	IS3	A. calcoaceticus	Gerischer et al. (1996)
o-, m-, p-xylene catabolism	xyl/tou	ISPst2	ISL3	P. stutzeri	Bolognese et al. (1999)

Table 2. Modulation of expression of neighbouring genes by IS elements carrying a complete outward-directed promoter.

IS family	IS element	IRx^a	Phenotype affected	Gene	Organism	Reference
IS1380	ISEcp1	R	β-Lactam^R	blaCTX-M-15	Enterobacteriaceae	Karim et al. (2001)
				blaCTX-M-17	K. pneumoniae	Cao et al. (2002)
				blaCTX-M-19	K. pneumoniae	Poirel et al. (2003)
				blaCTX-M-2	K. ascorbata	Lartigue et al. (2006)
			Aminoglycoside^R	rmtC	E. coli	Wachino et al. (2006)
	IS1170	L	5-Nitroimidazole^R	nimC	Bacteroides	Soki et al. (2006) and Trinh et al. (1995)
	IS1188	L	Carbapenem^R	cfiA	B. fragilis	Podglajen et al. (2001)
	IS612	L		cfiA	B. fragilis	Kato et al. (2003)
	IS613	L		cfiA	B. fragilis	Kato et al. (2003)
	IS614	L		cfiA	B. fragilis	Kato et al. (2003)
	IS942	L		cfiA	B. fragilis	Podglajen et al. (2001)
IS3	ISPst4	R	Effective host range expression	oriV	P. stutzeri	Coleman et al. (2014)
	IS3	R	Arginine biosynthesis	argE	E. coli	Charlier et al. (1982)
		R	Citrate utilization	citT		Blount et al. (2012)
		R	Acetate utilization	acs		Treves et al. (1998)
	IS407	R	Lactose utilization	lac	B. cepacia	Wood et al. (1991)
	IS6110	R	Genes activated during infection	Rv2280/Rv1468c	M. tuberculosis	Safi et al. (2004)
IS4	ISAba1	L	Ceftazidime^R	blaampC	A. baumannii	Corvec et al. (2003), Heritier et al. (2006) and Segal et al. (2004)
			Carbapenem^R	blaOXA-51-like	A. baumannii	Turton et al. (2006)
				blaOXA-23	A. baumannii	Turton et al. (2006)
	ISPa12	L	Ceftazidime^R	blaPER-1	A. baumannii	Poirel et al. (2005a)
					P. aeruginosa	Poirel et al. (2005a)
					S. enterica	Poirel et al. (2005a)
	IS10	L	Fluoroquinolone^R	acrEF pump	S. enterica	Olliver et al. (2005)
			Histidine biosynthesis	hisD	S. enterica	Wang and Roth (1988)
	IS1999	L	Ceftazidime^R	blaVEB-1	P. aeruginosa	Aubert et al. (2003, 2006)
				blaOXA-48	K. pneumoniae	Aubert et al. (2003, 2006)
	IS942	L	β -lactam^R	ccrA	B. fragilis	Rasmussen and Kovacs (1991)
IS481	ISRme5	R	Zinc^R	cnrCBAT	C. metallidurans	Vandecraen et al. (2016)
	IS481a	L	Catalase activity	katA	B. pertussis	DeShazer et al. (1994)
			Type III cytotoxic effector protein	bteA	B. pertussis	Han et al. (2011)
IS5	ISBf6	L	5-nitroimidazole^R	nimE	Bacteroides	Soki et al. (2006)
	IS1168	R		nimA nimB	Bacteroides	Haggoud et al. (1994), Soki et al. (2006)
	IS1169	R		nimD	B. fragilis	Trinh et al. (1995)
	IS1186	R	Carbapenem^R	cfiA	B. fragilis	Podglajen et al. (1994, 1995)
IS6	ISS1	L	Restriction-Modification system	abi-416	Lactobacillus lactis	Cluzel et al. (1991)
	IS257	L	Tetracycline^R	tetA(K)	S. aureus	Simpson et al. (2000)
IS982	IS1187	L	Carbapenem^R	cfiA	B. fragilis	Podglajen et al. (2001)
ISL3	IS1411	L	Phenol degradation	pheBA	P. putida	Kallastu et al. (1998)

^a Orientation of the outward-direct promoter oriented, with R (IRR) right inverted repeat and L (IRL) left inverted repeat.

Phenotype affected, R: resistance.

Table 3. Modulation of expression of neighbouring genes by IS elements carrying an outward-directed -35 promoter component.

IS family	IS element	Phenotype affected	Gene	Organism	Reference
IS1	IS1	Erythromycin^R		E. coli	Barany et al. (1982)
		Extended-spectrum β-lactamase	blaTEM-1		Prentki et al. (1986)
	IS1	Fluoroquinolone^R	acrEF pump	S. enterica	Olliver et al. (2005)
	IS1-like	Extended-spectrum β-lactamase	blaT-6	E. coli	Goussard et al. (1991)
IS21	ISBf1	High-level β-lactam ^R	cepA	B. fragilis	Rogers et al. (1994)
	ISKpn7	Extended-spectrum β-lactamase	blaKPC	K. pneumoniae	Naas et al. (2012)
IS256	IS1490	2,4,5-trichlorophenoxyacetic acid catabolism	tftA	B. cepacia	Hubner and Hendrickson (1997)
	IS256	Methicillin^R	llm	S. aureus	Maki and Murakami (1997)
			mecA	S. sciuri	Couto et al. (2003)
	IS406	Lactose utilization	lac	B. cepacia	Wood et al. (1991)
IS3	IS2	Ampicillin^R	ampC	E. coli	Jaurin and Normark (1983)
		Fluoroquinolone^R	acrEF pump	E. coli	Jellen-Ritter and Kern (2001)
		Erythromycin^R			Barany et al. (1982)
		Galactose utilization	gal	E. coli	Saedler et al. (1974)
		Arginine biosynthesis	argE		Nevers and Saedler (1977) Glansdorff et al. (1981)
			xis/int	Bacteriophage λ	Mosharrafa et al. (1976), Pilacinski et al. (1977)
	IS981	Lactate production	ldhB	L. lactis	Bongers et al. (2003)
IS30	IS18	Aminoglycoside^R	aac(6’)-lj	Acinetobacter	Rudant et al. (1998)
	IS30	Spectinomycin^S	cmr/mdfA	E. coli	Bohn and Bouloc (1998)
		Galactose utilization	galK	E. coli	Dalrymple (1987), Dalrymple and Arber (1985)
IS6	IS1008	Carbapenem^R	blaOXA-58	A. baumannii	Chen et al. (2008a)
	IS140	Gentamycin^R	aac(3)-III and IV		Brau et al. (1984b)
	IS257	Tetracycline^R	tetA(K)	S. aureus	Simpson et al. (2000)
		Trimethoprim^R	thyE-dfrA-orf140	S. aureus	Leelaporn et al. (1994)
	IS26	Aminoglycoside^R	aphA7, blaSHV-2a	K. pneumoniae	Jones et al. (2005) and Lee et al. (1990)
		SHV-type extended-spectrum β-lactamase	blaSHV-2a	P. aeruginosa	Naas et al. (1999)
IS5	ISVa1	Ferric anguibactin transport and biosynthesis	fatDCBAangRT	V. anguilarum	Di Lorenzo et al. (2003), Tolmasky and Crosa (1995)
IS982	IS982	Citrate transport	citQRP	L. lactis	Lopez de Felipe et al. (1996)

R : resistance;

S : sensitivity.

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