Photorhabdus phase variants express a novel fimbrial locus, mad, essential for symbiosis.
Fimbriae are adhesive organelles known to enable pathogens to colonize animal tissue, but little is known of their function in mutualistic symbioses. Photorhabdus colonization of Heterorhabditis bacteriophora nematodes is essential for the pair's insect pathogenic lifestyle. Maternal nematodes acquire Photorhabdus symbionts as a persistent intestinal biofilm prior to transmission to infective juvenile (IJ) stage offspring developing inside the maternal body. Screening 8000 Photorhabdus mutants for defects in IJ colonization revealed that a single fimbrial locus, named mad for maternal adhesion defective, is essential. The mad genes encode a novel usher/chaperone assembled fimbria regulated by an ON/OFF invertible promoter switch. Adherent Photorhabdus cells in maternal nematode intestines had the switch ON opposite to the OFF orientation of most other cells. A ΔmadA mutant failed to adhere to maternal intestines and be transmitted to the IJs. Mad fimbriae were detected on TT01 phase ON cells but not on ΔmadA phase ON cells. Also required for transmission is madJ, predicted to encode a transcriptional activator related to GrlA. Expression of madA-K or madIJK restored the ability of madJ mutant to adhere. The Mad fimbriae were not required for insect pathogenesis, indicating the specialized function of Mad fimbriae for symbiosis.
Somvanshi
Vishal S
VS
Department of Microbiology and Molecular Genetics and the Center for Microbial Pathogenesis, Michigan State University, East Lansing, MI 48824, USA.
Kaufmann-Daszczuk
Bettina
B
Department of Microbiology and Molecular Genetics and the Center for Microbial Pathogenesis, Michigan State University, East Lansing, MI 48824, USA.
Kim
Kwi-Suk
KS
Department of Microbiology and Molecular Genetics and the Center for Microbial Pathogenesis, Michigan State University, East Lansing, MI 48824, USA.
Mallon
Shane
S
Department of Microbiology and Molecular Genetics and the Center for Microbial Pathogenesis, Michigan State University, East Lansing, MI 48824, USA.
Ciche
Todd A
TA
Department of Microbiology and Molecular Genetics and the Center for Microbial Pathogenesis, Michigan State University, East Lansing, MI 48824, USA.
D000818:Animals; D001422:Bacterial Adhesion; D018441:Biofilms / Q000254:growth & development; D036781:Fimbriae Proteins / Q000235:genetics / Q000378:metabolism*; D041981:Gastrointestinal Tract / Q000382:microbiology; D017353:Gene Deletion; D015964:Gene Expression Regulation, Bacterial; D005798:Genes, Bacterial; D056426:Genetic Loci; D005810:Multigene Family; D009876:Operon; D020637:Photorhabdus / Q000235:genetics / Q000502:physiology*; D011401:Promoter Regions, Genetic; D017172:Rhabditoidea / Q000254:growth & development / Q000382:microbiology*; D013559:Symbiosis
D036781:Fimbriae Proteins