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- Title
Interacting bactofilins impact cell shape of the MreB-less multicellular Rhodomicrobium vannielii.
- Authors
Richter, Pia; Melzer, Brigitte; Müller, Frank D.
- Abstract
Most non-spherical bacteria rely on the actin-like MreB cytoskeleton to control synthesis of a cell-shaping and primarily rod-like cell wall. Diverging from simple rod shape generally requires accessory cytoskeletal elements, which locally interfere with the MreB-guided cell wall synthesis. Conserved and widespread representatives of this accessory cytoskeleton are bactofilins that polymerize into static, non-polar bundles of filaments. Intriguingly, many species of the Actinobacteria and Rhizobiales manage to grow rod-like without MreB by tip extension, yet some of them still possess bactofilin genes, whose function in cell morphogenesis is unknown. An intricate representative of these tip-growing bacteria is Rhodomicrobium vannielii; a member of the hitherto genetically not tractable and poorly studied Hyphomicrobiaceae within the MreB-less Rhizobiales order. R. vannielii displays complex asymmetric cell shapes and differentiation patterns including filamentous hyphae to produce offspring and to build dendritic multicellular arrays. Here, we introduce techniques to genetically access R. vannielii, and we elucidate the role of bactofilins in its sophisticated morphogenesis. By targeted mutagenesis and fluorescence microscopy, protein interaction studies and peptidoglycan incorporation analysis we show that the R. vannielii bactofilins are associated with the hyphal growth zones and that one of them is essential to form proper hyphae. Another paralog is suggested to represent a novel hybrid and co-polymerizing bactofilin. Notably, we present R. vannielii as a powerful new model to understand prokaryotic cell development and control of multipolar cell growth in the absence of the conserved cytoskeletal element, MreB. Author summary: Bacteria are often considered as relatively simple, single celled organisms that are spherical or rod-shaped, divide by splitting at midcell and lack elaborate cell differentiation. In fact, however, various intricate species exhibit true multicellularity and differentiate into cell types of distinct shape and function, reminiscent to multicellular eukaryotes. These bacteria are heavily understudied because of missing culturing methods or fastidiousness, the lack of genetic techniques, and because they are rarely pathogenic. A well-known representative is Rhodomicrobium vannielii, which is characterized by complex life cycles and branching cell appendices that give rise to dendritic, tissue-like cell assemblies. Despite its obscure appearance, R. vannielii lacks core components that are essential to steer cell shape in most non-spherical bacteria. Here we describe techniques to genetically access R. vannielii, and we show that a cytoskeletal bactofilin is crucially involved in its complex morphogenesis. Thereby, we shed more light on processes that allow for the development of multicellular bacteria.
- Subjects
CELL morphology; CELL differentiation; GENETIC techniques; TRACE elements; FLUORESCENCE microscopy
- Publication
PLoS Genetics, 2023, Vol 19, Issue 5, p1
- ISSN
1553-7390
- Publication type
Article
- DOI
10.1371/journal.pgen.1010788