Energy taxis drives Campylobacter jejuni toward the most favorable conditions for growth

TY - JOUR

T1 - Energy taxis drives Campylobacter jejuni toward the most favorable conditions for growth

AU - Vegge, Christina S

AU - Brøndsted, Lone

AU - Li, Yi-Ping

AU - Bang, Dang D.

AU - Ingmer, Hanne

N1 - Keywords: Animals; Bacterial Proteins; Campylobacter jejuni; Carbon; Cell Line, Tumor; Cells, Cultured; Chemotaxis; Chick Embryo; Chickens; Colon; Electron Transport; Epithelial Cells; Gene Deletion; Humans; Intestines; Membrane Proteins; Movement; Sodium Azide

PY - 2009

Y1 - 2009

N2 - Campylobacter jejuni is a serious food-borne bacterial pathogen in the developed world. Poultry is a major reservoir, and C. jejuni appears highly adapted to the gastrointestinal tract of birds. Several factors are important for chicken colonization and virulence, including a taxis mechanism for environmental navigation. To explore the mechanism of chemotaxis in C. jejuni, we constructed mutants with deletions of five putative mcp (methyl-accepting chemotaxis protein) genes (tlp1, tlp2, tlp3, docB, and docC). Surprisingly, the deletions did not affect the chemotactic behavior of the mutants compared to that of the parental strain. However, the tlp1, tlp3, docB, and docC mutant strains displayed a 10-fold decrease in the ability to invade human epithelial and chicken embryo cells, hence demonstrating that the corresponding proteins affect the host interaction. L-Asparagine, formate, D-lactate, and chicken mucus were identified as new attractants of C. jejuni, and we observed that chemical substances promoting tactic attraction are all known to support the growth of this organism. The attractants could be categorized as carbon sources and electron donors and acceptors, and we furthermore observed a correlation between an attractant's potency and its efficiency as an energy source. The tactic attraction was inhibited by the respiratory inhibitors HQNO (2-n-heptyl-4-hydroxyquinoline N-oxide) and sodium azide, which significantly reduce energy production by oxidative phosphorylation. These findings strongly indicate that energy taxis is the primary force in environmental navigation by C. jejuni and that this mechanism drives the organism toward the optimal chemical conditions for energy generation and colonization.

AB - Campylobacter jejuni is a serious food-borne bacterial pathogen in the developed world. Poultry is a major reservoir, and C. jejuni appears highly adapted to the gastrointestinal tract of birds. Several factors are important for chicken colonization and virulence, including a taxis mechanism for environmental navigation. To explore the mechanism of chemotaxis in C. jejuni, we constructed mutants with deletions of five putative mcp (methyl-accepting chemotaxis protein) genes (tlp1, tlp2, tlp3, docB, and docC). Surprisingly, the deletions did not affect the chemotactic behavior of the mutants compared to that of the parental strain. However, the tlp1, tlp3, docB, and docC mutant strains displayed a 10-fold decrease in the ability to invade human epithelial and chicken embryo cells, hence demonstrating that the corresponding proteins affect the host interaction. L-Asparagine, formate, D-lactate, and chicken mucus were identified as new attractants of C. jejuni, and we observed that chemical substances promoting tactic attraction are all known to support the growth of this organism. The attractants could be categorized as carbon sources and electron donors and acceptors, and we furthermore observed a correlation between an attractant's potency and its efficiency as an energy source. The tactic attraction was inhibited by the respiratory inhibitors HQNO (2-n-heptyl-4-hydroxyquinoline N-oxide) and sodium azide, which significantly reduce energy production by oxidative phosphorylation. These findings strongly indicate that energy taxis is the primary force in environmental navigation by C. jejuni and that this mechanism drives the organism toward the optimal chemical conditions for energy generation and colonization.

KW - Former LIFE faculty

KW - Animals

KW - Bacterial Proteins

KW - Campylobacter jejuni

KW - Carbon

KW - Cell Line

KW - Tumor

KW - Cultured

KW - Chemotaxis

KW - Chick Embryo

KW - Chickens

KW - Colon

KW - Electron Transport

KW - Epithelial Cells

KW - Gene Deletion

KW - Humans

KW - Intestines

KW - Membrane Proteins

KW - Movement

KW - Sodium Azide

U2 - 10.1128/AEM.00287-09

DO - 10.1128/AEM.00287-09

M3 - Journal article

C2 - 19542337

SN - 0099-2240

VL - 75

SP - 5308

EP - 5314

JO - Applied and Environmental Microbiology

JF - Applied and Environmental Microbiology

IS - 16

ER -