Table 2 - Safe use of genetically modified lactic acid bacteria in food. Bridging the gap between consumers, green groups, and industry

Table 2. Overview of lactic acid bacteria with controlled or uncontrolled genetic alterations.

Host strain	Donor strain	Gene involved	Intended effect	Modification technique	Reference
Lb. bulgaricus	Not applicable	lacZ	limited lactose fermentation	IS mediated deletion	Mollet and Delley, 1990
L. lactis	Not applicable	ldh and others	increased carbon dioxide production	spontaneous and induced random mutagenesis	El Attar et al. 2000
L. lactis	Not applicable	ldh and others	increased acetoin and diacetyl production	NNG induced random mutagenesis	Boumerdassi et al. 1997
L. lactis	Not applicable	aldB	increased diacetyl production	NNG induced random mutagenesis,	Monnet et al. 2000
L. lactis	Not applicable	aldB	increased diacetyl production	Spontaneous random mutagenesis	Goupil et al. 1996
L. lactis	Not applicable	ribC	increased riboflavin production	induced random mutagenesis	Burgess et al. 2003
S. thermophilus	Not applicable	gal operon	fermentation of galactose	spontaneous random mutagenesis	Vaughan et al. 2001
L. lactis	Not applicable	glk, eII^man/glc	no glucose fermenting capacity	spontaneous random mutagenesis	Thompson et al. 1985.
L. lactis	L. lactis	aldB	increased diacetyl production	double crossover homologous recombination	Swindell et al. 1996
L. lactis	Lb. helveticus	pepN, pepX, pepC, pepI	modulation of proteolytic system for enhancement cheese ripening	food grade vector cloning	Joutsjoki et al. 2002
L. lactis	L. delbrueckii	pepI, pepL, pepW, pepG	modulation of proteolytic system for enhancement cheese ripening	NICE System	Wegmann et al. 1999
L. lactis	Peptostreptococcus asaccharolyticus	Gdh	increased production of alpha-ketoglutarate	Vector cloning	Rijnen et al. 2000
L. lactis	lytic phage phi31	phage inducible promoter	expression of lethal three-gene restriction cassette LlaIR+,	Vector cloning	Djordjevic et al.1997
L. lactis	lytic phage phi31	anti sense phage RNA	silencing of phage genes	Vector cloning	Walker and Klaenhammer, 1998
L. lactis	lytic phage	anti sense phage RNA	silencing of phage genes encoding structural genes	Vector cloning	Kim et al. 1992
L. lactis	Not applicable	pip	inactivation of phage infection protein	double crossover homologous recombination	Monteville et al. 1994
L. lactis strains	L. lactis strains	lacticin encoding genes	lacticin production	Conjugation	O’Sullivan et al. 2003
L. lactis strains	L. lactis strains	lacticin encoding gene	lacticin production	conjugation (plasmid stacking)	Mills et al. 2002
L. lactis	S. thermophilus	abiA, abiG	abortion of cells upon phage induction	Vector cloning	Tangney and Fitzgerald, 2002
L. lactis and others	Pediococcus acidilactici and others	lcnC, lcnD	lantibiotic production	Vector cloning	Horn et al. 1999
L. lactis	phage	lytA, lytH	production of lysin and holin	NICE	de Ruyter et al. 1997
L. lactis	S. thermophilus Sfi6	EPS gene cluster	altered EPS production	Vector cloning	Stingele et al. 1999
L. lactis	S. thermophilus Sfi39	EPS gene cluster	altered EPS production	Vector cloning	Germond et al. 2001
Lb. gasseri	L. lactis	folate gene cluster	introduction folate biosynthesis pathway	Vector cloning	Wegkamp et al. 2004
S. thermophilus	Not applicable	pgmA, gal U	inactivation of phosphoglucomutase	double crossover homologous recombination and vector cloning	Levander et al. 2002
L. lactis	B. sphaericus	ldh, alaD, alr	rerouting of pyruvate to L-alanine	double crossover homologous recombination, vector cloning	Hols et al. 1999
L. lactis	L. lactis	riboflavin gene cluster	overexpression riboflavin biosynthesis pathway	Vector cloning	Burgess et al. 2003
L. lactis	L. lactis	folate gene cluster	overexpression folate biosynthesis pathway	Vector cloning	Sybesma et al. 2003b
L. lactis	L. lactis	glk, pfnABCD, pfcBA, genes lactose-PTS and tagatose-6P	inactivation of glucose fermenting system and introduction of lactose fermentation	double crossover homologous recombination, vector cloning	Pool et al. 2003
L. lactis	L. lactis	galA, aga	introduction a-galactosidase activity	food grade vector cloning	Boucher et al. 2002
Lb. plantarum	B. subtilis	phyC	introduction phytase activity	Vector cloning	Kerovuo and Tynkkynen, 2000
Lb. plantarum	L. amylovorus	amyA	introduction a-amylase activity	chromosomal integration	Fitzsimons et al. 1994
Lb. plantarum	B. stearothermophilus, C. thermocellum	α-amylase gene, celA	introduction a-amylase and cellulase activity	single homologous recombination	Scheirlinck et al. 1989
S. thermophilus	S. thermophilus	glyA	increased acetaldehyde production	Vector cloning	Chaves et al. 2002
Lb. fermentum	Not applicable	ldhD, ldhL	increased mannitol production	double crossover homologous recombination	Aarnikunnas et al. 2003
Lb. helveticus	Not applicable	ldhD	production of pure L-(+) lactic acid	double crossover homologous recombination	Kyla-Nikkila et al. 2000
Lb. delbrueckii	Not applicable	EPS genes	altered EPS production	Chemically induced random mutagenesis	Welman et al. 2003
S. thermophilus	S. thermophilus bacteriophage	anti sense phage RNA, helicase gene	silencing of phage genes	Vector cloning	Sturino and Klaenhammer, 2002
Streptococcus mutans	Zymomonas mobilis	ldh, adh	prevention of dental caries	double crossover homologous recombination, gene replacement	Hillman, 2002
Lb. delbrueckii	Not applicable	β-galactosidase gene	Increased b-galactosidase activity	EMS or NNG induced random mutagenesis	Ibrahim and O'Sullivan, 2000
L. lactis	Eimeria tenella, L. plantarum	M1Pase gene, MtlD	increased mannitol production	NICE	Wisselink et al. 2005
L. casei ATCC 334	L. casei LC202	dhic	increased alpha-keto acid dehydrogenase activity	Vector cloning	Broadbent et al. 2004
L. plantarum	Lactobacillus sake	promotors and regulatory genes	increased gene expression	Vector cloning	Mathiesen et al. 2004
L. lactis	L. lactis	Prt+- and Lac+-derivatives of L. lactis MG1363	increased proteolytic and acidifying activity	conjugation	Picon et al. 2005
L. lactis	S. simulans	Lss	production of lysostaphin	NICE	Mierau et al. 2005
L. lactis	P. stipitis	XYL1	production of xylitol	Vector cloning	Nyyssölä et al. 2005
L. lactis	Not applicable	unknown	increased oxidative-stress tolerance	spontaneous mutations (natural selection)	Rochat et al. 2005
L. lactis	L. lactis	nisRK, nisFEG	increased nisn Z production	Vector cloning	Cheigh et al. 2005
L. lactis	Z. mobilis, L. lactis	pdc, nox	increased acetaldehyde production	NICE	Bongers et al. 2005
L. lactis	G. stearothermophilus, L. Brevis, L. lactis	sgsE, slpA, usp	production of excreted S-layer protein	NICE	Novotny et al.2005
L. lactis	E. coli	gshA, gshB	increased glutathion production	NICE	Li et al.2005
L. lactis, L. paracasei	L. paracasei	groEL	increased stress tolerance	NICE	Desmond et al. 2004
L. lactis	Not applicable	unknown	increased L(+)-actate production	random mutagenesis	Bai et al. 2004
S. thermophilus	Not applicable	deoB, gst, rggC, and unknown	increased oxidative-stress tolerance	random insertional mutagenesis	Fernandez et al. 2004
EMS: ethyl methanesulfonate; NNG: N-methyl-N'-nitro-N-nitrosoguanidine