The morphogene AmiC2 is pivotal for multicellular development in the cyanobacterium Nostoc punctiforme.
Filamentous cyanobacteria of the order Nostocales are primordial multicellular organisms, a property widely considered unique to eukaryotes. Their filaments are composed of hundreds of mutually dependent vegetative cells and regularly spaced N(2)-fixing heterocysts, exchanging metabolites and signalling molecules. Furthermore, they may differentiate specialized spore-like cells and motile filaments. However, the structural basis for cellular communication within the filament remained elusive. Here we present that mutation of a single gene, encoding cell wall amidase AmiC2, completely changes the morphology and abrogates cell differentiation and intercellular communication. Ultrastructural analysis revealed for the first time a contiguous peptidoglycan sacculus with individual cells connected by a single-layered septal cross-wall. The mutant forms irregular clusters of twisted cells connected by aberrant septa. Rapid intercellular molecule exchange takes place in wild-type filaments, but is completely abolished in the mutant, and this blockage obstructs any cell differentiation, indicating a fundamental importance of intercellular communication for cell differentiation in Nostoc. AmiC2-GFP localizes in the cell wall with a focus in the cross walls of dividing cells, implying that AmiC2 processes the newly synthesized septum into a functional cell-cell communication structure during cell division. AmiC2 thus can be considered as a novel morphogene required for cell-cell communication, cellular development and multicellularity.
Interfaculty Institute for Microbiology and Infection Medicine, Division Organismic Interactions, University of Tübingen, 72076 Tübingen, Germany.
Josef
J
Lehner
Yao
Y
Zhang
Susanne
S
Berendt
Tobias M
TM
Rasse
Karl
K
Forchhammer
Iris
I
Maldener
D000581:Amidohydrolases / Q000235:genetics / Q000378:metabolism*; D001426:Bacterial Proteins / Q000235:genetics / Q000378:metabolism*; D002473:Cell Wall / Q000201:enzymology / Q000235:genetics; D015964:Gene Expression Regulation, Bacterial; D018507:Gene Expression Regulation, Developmental; D046937:Nostoc / Q000201:enzymology* / Q000235:genetics / Q000254:growth & development*; D021381:Protein Transport
D001426:Bacterial Proteins; D000581:Amidohydrolases; C019665:amidase