Prokaryotic multicellularity: a nanopore array for bacterial cell communication - PubMed (original) (raw)
. 2013 Jun;27(6):2293-300.
doi: 10.1096/fj.12-225854. Epub 2013 Feb 26.
Affiliations
- PMID: 23444428
- DOI: 10.1096/fj.12-225854
Prokaryotic multicellularity: a nanopore array for bacterial cell communication
Josef Lehner et al. FASEB J. 2013 Jun.
Abstract
The transition from unicellular to multicellular life, which occurred several times during evolution, requires tight interaction and communication of neighboring cells. The multicellular cyanobacterium Nostoc punctiforme ATCC 29133 forms filaments of hundreds of interacting cells exchanging metabolites and signal molecules and is able to differentiate specialized cells in response to environmental stimuli. Mutation of cell wall amidase AmiC2 leads to a severe phenotype with formation of aberrant septa in the distorted filaments, which completely lack cell communication and potential for cell differentiation. Here we demonstrate the function of the amidase AmiC2 in formation of cell-joining structures. The AmiC2 protein localizes to the young septum between cells and shows bona fide amidase activity in vivo and in vitro. Vancomycin staining identified the overall septum morphology in living cells. By electron microscopy of isolated peptidoglycan sacculi, the submicroscopic structure of the cell junctions could be visualized, revealing a novel function for a cell wall amidase: AmiC2 drills holes into the cross-walls, forming an array of ~155 nanopores with a diameter of ~20 nm each. These nanopores seem to constitute a framework for cell-joining proteins, penetrating the cell wall. The entire array of junctional nanopores appears as a novel bacterial organelle, establishing multicellularity in a filamentous prokaryote.
Keywords: amidase; cyanobacteria.
Similar articles
- Role of Two Cell Wall Amidases in Septal Junction and Nanopore Formation in the Multicellular Cyanobacterium Anabaena sp. PCC 7120.
Bornikoel J, Carrión A, Fan Q, Flores E, Forchhammer K, Mariscal V, Mullineaux CW, Perez R, Silber N, Wolk CP, Maldener I. Bornikoel J, et al. Front Cell Infect Microbiol. 2017 Sep 5;7:386. doi: 10.3389/fcimb.2017.00386. eCollection 2017. Front Cell Infect Microbiol. 2017. PMID: 28929086 Free PMC article. - Enabling cell-cell communication via nanopore formation: structure, function and localization of the unique cell wall amidase AmiC2 of Nostoc punctiforme.
Büttner FM, Faulhaber K, Forchhammer K, Maldener I, Stehle T. Büttner FM, et al. FEBS J. 2016 Apr;283(7):1336-50. doi: 10.1111/febs.13673. Epub 2016 Feb 27. FEBS J. 2016. PMID: 26833702 - The morphogene AmiC2 is pivotal for multicellular development in the cyanobacterium Nostoc punctiforme.
Lehner J, Zhang Y, Berendt S, Rasse TM, Forchhammer K, Maldener I. Lehner J, et al. Mol Microbiol. 2011 Mar;79(6):1655-69. doi: 10.1111/j.1365-2958.2011.07554.x. Epub 2011 Feb 10. Mol Microbiol. 2011. PMID: 21244533 - A nanopore array in the septal peptidoglycan hosts gated septal junctions for cell-cell communication in multicellular cyanobacteria.
Kieninger AK, Forchhammer K, Maldener I. Kieninger AK, et al. Int J Med Microbiol. 2019 Dec;309(8):151303. doi: 10.1016/j.ijmm.2019.03.007. Epub 2019 Mar 26. Int J Med Microbiol. 2019. PMID: 31521503 Review. - Cellular differentiation in the cyanobacterium Nostoc punctiforme.
Meeks JC, Campbell EL, Summers ML, Wong FC. Meeks JC, et al. Arch Microbiol. 2002 Dec;178(6):395-403. doi: 10.1007/s00203-002-0476-5. Epub 2002 Sep 18. Arch Microbiol. 2002. PMID: 12420158 Review.
Cited by
- The role of FraI in cell-cell communication and differentiation in the hormogonia-forming cyanobacterium Nostoc punctiforme.
Janović A, Maldener I, Menzel C, Parrett GA, Risser DD. Janović A, et al. mSphere. 2024 Aug 28;9(8):e0051024. doi: 10.1128/msphere.00510-24. Epub 2024 Jul 22. mSphere. 2024. PMID: 39037261 Free PMC article. - Role of Two Cell Wall Amidases in Septal Junction and Nanopore Formation in the Multicellular Cyanobacterium Anabaena sp. PCC 7120.
Bornikoel J, Carrión A, Fan Q, Flores E, Forchhammer K, Mariscal V, Mullineaux CW, Perez R, Silber N, Wolk CP, Maldener I. Bornikoel J, et al. Front Cell Infect Microbiol. 2017 Sep 5;7:386. doi: 10.3389/fcimb.2017.00386. eCollection 2017. Front Cell Infect Microbiol. 2017. PMID: 28929086 Free PMC article. - The Peptidoglycan-Binding Protein SjcF1 Influences Septal Junction Function and Channel Formation in the Filamentous Cyanobacterium Anabaena.
Rudolf M, Tetik N, Ramos-León F, Flinner N, Ngo G, Stevanovic M, Burnat M, Pernil R, Flores E, Schleiff E. Rudolf M, et al. mBio. 2015 Jun 30;6(4):e00376. doi: 10.1128/mBio.00376-15. mBio. 2015. PMID: 26126850 Free PMC article. - FurC (PerR) contributes to the regulation of peptidoglycan remodeling and intercellular molecular transfer in the cyanobacterium Anabaena sp. strain PCC 7120.
Sarasa-Buisan C, Nieves-Morión M, Arévalo S, Helm RF, Sevilla E, Luque I, Fillat MF. Sarasa-Buisan C, et al. mBio. 2024 Mar 13;15(3):e0323123. doi: 10.1128/mbio.03231-23. Epub 2024 Feb 9. mBio. 2024. PMID: 38334377 Free PMC article. - The Integrity of the Cell Wall and Its Remodeling during Heterocyst Differentiation Are Regulated by Phylogenetically Conserved Small RNA Yfr1 in Nostoc sp. Strain PCC 7120.
Brenes-Álvarez M, Vioque A, Muro-Pastor AM. Brenes-Álvarez M, et al. mBio. 2020 Jan 21;11(1):e02599-19. doi: 10.1128/mBio.02599-19. mBio. 2020. PMID: 31964726 Free PMC article.
Publication types
MeSH terms
Substances
LinkOut - more resources
Full Text Sources
Other Literature Sources