Table II.5 Control of bacterial protein synthesis (phase variation) and modification of protein structure (antigenic variation) by natural genetic engineering. (Expanded from (Wisniewski-Dye and Vial 2008))

Phase variation by site-specific recombination

Escherichia coli (Gammaproteobacteria intestinal flora), type I pili

(Abraham, Freitag et al. 1985; Klemm 1986)

Moraxella bovis (Gammaproteobacteria bovine pathogen), type I pili

(Marrs, Ruehl et al. 1988; Heinrich and Glasgow 1997)

Moraxella lacunata (Gammaproteobacteria human pathogen), type I pili

(Heinrich and Glasgow 1997)

Mycoplasma pulmonis (Mollicute mouse pathogen), DNA restriction and modification

(Dybvig and Yu 1994)

Pseudomonas fluorescens (Gammaproteobacteria plant pathogen), root colonization

(Dekkers, Phoelich et al. 1998; Sanchez-Contreras, Martin et al. 2002; Martinez-Granero, Capdevila et al. 2005)

Salmonella enterica serovar Typhimurium (Gammaproteobacteria mouse pathogen), flagella

 (Silverman, Zieg et al. 1979; Heichman and Johnson 1990)

Clostridium difficile (Firmicute human intestinal pathogen), major cell wall protein

 (Emerson, Reynolds et al. 2009)

Campylobacter fetus (Epsilonprotebacteria human pathogen), surface layer protein

 (Tu, Ray et al. 2001)

Developmental activation of expression by site-specific excision from interrupted coding sequences in terminally differentiated cells

Bacillus subtilis SigK expression in spore mother cell

 (Stragier, Kunkel et al. 1989; Popham and Stragier 1992; Sato, Harada et al. 1996; Hilbert and Piggot 2004)

Anabaena (Nostoc) NifD and FdxN expression in nitrogen-fixing heterocysts

 (Carrasco, Ramaswamy et al. 1994; Carrasco, Buettner et al. 1995; Carrasco and Golden 1995; Carrasco, Holliday et al. 2005); (Ramaswamy, Carrasco et al. 1997; Henson, Pennington et al. 2008)

Phase variation by transposon insertion and excision

Acidithiobacillus ferrooxidans (Gammaproteobacteria soil bacteria), iron oxidation & swarming,

(Cabrejos, Zhao et al. 1999)

Pseudoalteromonas atlanticus (Gammaproteobacteria marine biofilm organism), extracellular polysaccharide synthesis (IS492 insertion & excision)

(Bartlett, Wright et al. 1988; Bartlett and Silverman 1989) (Perkins-Balding, Duval-Valentin et al. 1999; Higgins, Carpenter et al. 2007; Higgins, Popkowski et al. 2009)

Citrobacter freundii (Gammaproteobacteria opportunistic human pathogen), capsule synthesis

 (Ou, Baron et al. 1988)

Legionella pneumophila (Gammaproteobacteria human respiratory pathogen), lipopolysaccharides

 (Luneberg, Zahringer et al. 1998; Luneberg, Mayer et al. 2001)

Neisseria meningitides (Betaproteobacteria human pathogen), capsule synthesis

 (Hammerschmidt, Muller et al. 1996)

Shigella flexneri (Gammaproteobacterial human dysentery pathogen), cell surface markers

 (Mills, Venkatesan et al. 1992)

Staphylococcus aureus (Firmicute human pathogen), extracellular polysaccharide & biofilm formation

 (Kiem, Oh et al. 2004; Valle, Vergara-Irigaray et al. 2007)

Staphylococcus epidermidis  (Firmicute human pathogen), extracellular polysaccharide & biofilm formation

 (Ziebuhr, Krimmer et al. 1999; Conlon, Humphreys et al. 2004),

Xanthomonas oryzae  (Gammaproteobacteria plant pathogen), extracellular polysaccharide & virulence

 (Rajeshwari and Sonti 2000)

Phase variation by cassette-based recombination

Geobacillus stearothermophilus (Firmicute soil bacterium), S-Layer proteins

 (Scholz, Riedmann et al. 2001)

Antigenic variation by cassette-based recombination

Borrelia burgdorferi (lyme disease Spirochaete), surface  lipoproteins

 (Zhang and Norris 1998)

Borrelia hermsi (relapsing fever Spirochaete) ), surface  lipoproteins

 (Plasterk, Simon et al. 1985; Restrepo, Carter et al. 1994)

Helicobacter pylori (Epsilonproteobacteria gastric pathogen), outer membrane proteins

 (Pride and Blaser 2002; Solnick, Hansen et al. 2004)

Mycoplasma genitalium (Mollicute human pathogen), surface lipoproteins

 (Iverson-Cabral, Astete et al. 2007)

Mycoplasma synoviae (Mollicute avian pathogen), surface lipoproteins

 (Noormohammadi, Markham et al. 2000)

Neisseria gonorrhoea (Betaproteobacteria human pathogen), opacity proteins (Opa)

 (Stern, Brown et al. 1986)

Neisseria gonorrhoea (Betaproteobacteria human pathogen), type IV pili

 (Howell-Adams and Seifert 2000)

Treponema pallidum (syphilis Spirochaete), major surface antigen

 (Centurion-Lara, LaFond et al. 2004)

Anaplasma marginale (intracellular Rickettsial pathogen ), immunodominant outer membrane protein

 (Barbet, Lundgren et al. 2000; Brayton, Palmer et al. 2002)

Antigenic variation by site-specific recombination

Bacteroides fragilis (intestinal microflora), polysaccharides

(Krinos, Coyne et al. 2001; Cerdeno-Tarraga, Patrick et al. 2005)

Campylobacter fetus (Epsilonprotebacteria opportunistic human pathogen), surface proteins

(Dworkin and Blaser 1996)

Dichelobacter nodosus (Gammaproteobacteria sheep pathogen), outer membrane proteins

 (Moses, Good et al. 1995)

Mycoplasma bovis (Mollicute cattle pathogen), surface lipoproteins

 (Lysnyansky, Rosengarten et al. 1996; Lysnyansky, Ron et al. 2001)

Mycoplasma penetrans (Mollicute opportunistic human pathogen), surface lipoproteins

(Horino, Sasaki et al. 2003; Horino, Kenri et al. 2009)

Mycoplasma pulmonis (Mollicute mouse pathogen), surface lipoproteins

(Bhugra, Voelker et al. 1995)

Bacteriophage Mu G tail protein

(Grundy and Howe 1984; Mertens, Klippel et al. 1988)

Plasmid R64 conjugative pilus shufflon

(Komano, Kim et al. 1994)

Other shufflons in genome sequences

 (Komano 1999; Tam, Hackett et al. 2004; Tam, Hackett et al. 2005)

Antigenic variation by diversity-generating retroelements (DGRs)

Bordetella bronchiseptica bacteriophage tail fiber

(Liu, Deora et al. 2002; Liu, Gingery et al. 2004; Guo, Tse et al. 2008)

Other DGRs in the genomes of a marine Vibrio virus and also in the chromosomes of a commensal “probiotic” Bifidobacterium, the dental spirochete Treponema denticola, and five different cyanobacteria.

(Doulatov, Hodes et al. 2004; Medhekar and Miller 2007)





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