The genetic mechanisms for multiseriate filament formation in cyanobacteria

• Applicant: Professorin Dr. Tal Dagan, since 7/2016
• Subject Area: Metabolism, Biochemistry and Genetics of Microorganisms ; Parasitology and Biology of Tropical Infectious Disease Pathogens ; Cell Biology
• Term: from 2014 to 2018
• Project identifier: Deutsche Forschungsgemeinschaft (DFG) - Project number 256949312

• Final Report Year: 2019

Final Report Abstract

Bacterial cell shape is an important determinant of the organism physiology, its interaction with the environment and the coordination of myriad intracellular processes. The cell shape is determined by peptidoglycan (PG) biogenesis and its spatial distribution, which is coordinated by components of the bacterial cytoskeleton. Those proteins typically selfassociate into polymers and interlink into higher-order structures in the cell. The determinants of bacterial cell shape are extensively studied in unicellular forms; examples are MreB that functions in cell wall synthesis or FtsZ, which functions in cell division. Nonetheless, the mechanisms that shape bacterial multicellular forms remain understudied. The phylum Cyanobacteria is characterized by a large morphological diversity, ranging from coccoid or rod-shaped unicellular species to complex filamentous multicellular species. Many species of multicellular cyanobacteria can undergo cell differentiation and changes in their cell shape. The diverse colony morphologies and cell types in cyanobacteria suggest the presence of a rich cytoskeletal proteins repertoire. Our aim in this project was to identify novel cytoskeletal proteins in cyanobacteria and characterize their function. For the identification of novel cytoskeletal proteins we focused on coiled-coil rich proteins (CCRPs) encoded in cyanobacterial genomes, which were identified using a computational approach. Identified CCRPs were further studied experimentally using in vitro polymerization essays, in vivo localization, and phenotypic characterization of knockout mutants. This revealed several novel filament-forming proteins in diverse cyanobacterial species. The highlight of our work is the finding of a novel cytoskeletal network that determines filament shape and viability in the multicellular cyanobacterium Anabaena sp. PCC 7120 (Anabaena). The network includes four proteins that interact with each other, and with SepJ and MreB; thus they form a proteinaceous network that stabilizes the Anabaena multicellular filament through direct interactions with the septal junctions and the cell wall. We propose that this cytoskeletal network is essential for the manifestation of a multicellular phenotype in Anabaena. Our study highlights a function of bacterial cytoskeleton in the maintenance of multicellular forms in prokaryotes.

Publications

• 2017. Evolution of chaperonin gene duplication in Stigonematalean Cyanobacteria (Subsection V). Genome Biol Evol 9:241–252
  Weissenbach J, Ilhan J, Bogumil D, Hülter N, Stucken K, Dagan T
  
• 2017. Plasticity first: molecular signatures of a complex morphological trait in filamentous cyanobacteria. BMC Evol. Biol. 17:209
  Koch R, Kupczok A, Stucken K, Ilhan J, Hammerschmidt K, Dagan T
  
• 2019. A cytoskeletal network maintains filament shape in the multicellular cyanobacterium Anabaena sp. PCC 7120
  Springstein BL, Nürnberg DJ, Kieninger A-K, Woehle C, Weissenbach J, Theune M, Helbig AO, Tholey A, Maldener I, Dagan T, Stucken K