Promiscuous cross-seeding between bacterial amyloids promotes interspecies biofilms.
Amyloids are highly aggregated proteinaceous fibers historically associated with neurodegenerative conditions including Alzheimers, Parkinsons, and prion-based encephalopathies. Polymerization of amyloidogenic proteins into ordered fibers can be accelerated by preformed amyloid aggregates derived from the same protein in a process called seeding. Seeding of disease-associated amyloids and prions is highly specific and cross-seeding is usually limited or prevented. Here we describe the first study on the cross-seeding potential of bacterial functional amyloids. Curli are produced on the surface of many Gram-negative bacteria where they facilitate surface attachment and biofilm development. Curli fibers are composed of the major subunit CsgA and the nucleator CsgB, which templates CsgA into fibers. Our results showed that curli subunit homologs from Escherichia coli, Salmonella typhimurium LT2, and Citrobacter koseri were able to cross-seed in vitro. The polymerization of Escherichia coli CsgA was also accelerated by fibers derived from a distant homolog in Shewanella oneidensis that shares less than 30% identity in primary sequence. Cross-seeding of curli proteins was also observed in mixed colony biofilms with E. coli and S. typhimurium. CsgA was secreted from E. coli csgB- mutants assembled into fibers on adjacent S. typhimurium that presented CsgB on its surfaces. Similarly, CsgA was secreted by S. typhimurium csgB- mutants formed curli on CsgB-presenting E. coli. This interspecies curli assembly enhanced bacterial attachment to agar surfaces and supported pellicle biofilm formation. Collectively, this work suggests that the seeding specificity among curli homologs is relaxed and that heterogeneous curli fibers can facilitate multispecies biofilm development.
Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, Michigan 48109-1048.
Yizhou
Y
Zhou
Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, Michigan 48109-1048.
Daniel
D
Smith
Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, Michigan 48109-1048.
Bryan J
BJ
Leong
Medical Biochemistry and Biophysics, Umeå University, 901 87 Umeå, Sweden.
Kristoffer
K
Brännström
Department of Chemistry, Chemical Biological Center, Umeå University, 901 87 Umeå, Sweden; Umeå Center for Microbial Research, Umeå University, 901 87 Umeå, Sweden.
Fredrik
F
Almqvist
Department of Molecular, Cellular and Developmental Biology, University of Michigan, Ann Arbor, Michigan 48109-1048; Umeå Center for Microbial Research, Umeå University, 901 87 Umeå, Sweden. Electronic address: chapmanm@umich.edu.
Matthew R
MR
Chapman
D000682:Amyloid / Q000235:genetics / Q000378:metabolism*; D001422:Bacterial Adhesion / Q000502:physiology; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism*; D056226:Bacterial Structures / Q000235:genetics / Q000378:metabolism*; D018441:Biofilms / Q000254:growth & development*; D041041:Citrobacter koseri / Q000502:physiology*; D004926:Escherichia coli / Q000502:physiology*; D009154:Mutation; D012486:Salmonella typhimurium / Q000502:physiology*
D000682:Amyloid; D001426:Bacterial Proteins