SepN is a septal junction component required for gated cell–cell communication in the filamentous cyanobacterium Nostoc

Kieninger, Ann-Katrin; Tokarz, Piotr; Janović, Ana; Pilhofer, Martin; Weiss, Gregor L.; Maldener, Iris

doi:10.1038/s41467-022-34946-7

Cited by 3 publications

(7 citation statements)

References 68 publications

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“…The relation to septal junction proteins and the Δ fraI phenotype 10,11,43 , prompted us to investigate cell-cell communication and septal junction gating ability in the Δ fraI mutant of N. punctiforme 8,36 . The study of cell-cell communication was performed by FRAP experiments…”

Section: Resultsmentioning

confidence: 99%

“…The relation to septal junction proteins together with the Δ fraI phenotype 10,11,44 prompted us to investigate cell-cell communication and septal junction gating ability in the Δ fraI mutant of N. punctiforme 8,9 . The study of cell-cell communication was performed by FRAP experiments 10,45 , where filaments were first stained with a fluorescent dye, subsequently, a single cell is laser-bleached, and finally the recovery of fluorescence, resulting from the diffusion of the dye through septal junctions, was monitored over time 10,45 .…”

Section: Resultsmentioning

confidence: 99%

“…Septal peptidoglycan was isolated as described 36 . First, vegetative filaments of Nostoc punctiforme WT and Δ fraI grew for 5 days in liquid BG11 medium supplemented with 4 mM sucralose to supress hormogonia development.…”

Section: Methodsmentioning

confidence: 99%

“…A three-day-old liquid culture of vegetative filaments from both the N. punctiforme wild type and the Δ fraI mutant strains was utilized for CCCP-FRAP, following previously established protocols 8,36 . Briefly, 2 ml of culture underwent triple washing with BG11 medium and were then resuspended in 500 μL of medium.…”

Section: Methodsmentioning

confidence: 99%

“…Its homologue in Nostoc sp. 7120 that we previously named FraI 40 (Kieninger 2023) was shown to be highly abundant in a co-immunoprecipitation experiment against septal junction proteins FraD and SepN 36 and displayed a fragmentation phenotype 40 . Based on this, and the data presented below, we have designated the gene name for Npun_F4142 as fraI.…”

Section: Frai Deletion Affects Hormogonia Motility Filament Length An...mentioning

confidence: 99%

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The role of FraI in cell-cell communication and differentiation in the hormogonia-forming cyanobacterium Nostoc punctiforme

Janović,

Maldener,

Menzel

et al. 2024

Preprint

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Multicellular cyanobacteria, likeNostoc punctiforme, rely on septal junctions for cell-cell communication, which is crucial for coordinating various physiological processes including differentiation of N2-fixing heterocysts, spore-like akinetes and hormogonia - short, motile filaments important for dispersal. In this study we functionally characterize a protein, encoded by gene NpF4142, which in a random mutagenesis approach, initially showed a motility-related function. The reconstructed NpF4142 knockout mutant exhibits further distinct phenotypic traits, including altered hormogonia formation with significant reduced motility, inability to differentiate heterocysts and filament fragmentation. For that reason, we named the protein FraI (fragmentation phenotype). The mutant displays severely impaired cell-cell communication, due to almost complete absence of the nanopore array in the septal cell wall, which is an essential part of the septal junctions. Despite lack of communication, hormogonia in the ΔfraImutant maintain motility and phototactic behavior, even though less pronounced than the wild type. This suggests an alternative mechanism for coordinated movement beyond septal junctions. Our study underscores the significance of FraI in nanopore formation and cell differentiation and provides additional evidence for the importance of septal junction formation and communication in various differentiation traits of cyanobacteria. The findings contribute to a deeper understanding of the regulatory networks governing multicellular cyanobacterial behaviour, with implications for broader insights into microbial multicellularity.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Frai Deletion Affects Hormogonia Motility Filament Length An...mentioning

confidence: 99%

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The role of FraI in cell-cell communication and differentiation in the hormogonia-forming cyanobacterium Nostoc punctiforme

Janović,

Maldener,

Menzel

et al. 2024

Preprint

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SepT, a novel protein specific to multicellular cyanobacteria, influences peptidoglycan growth and septal nanopore formation in Anabaena sp. PCC 7120

Velázquez-Suárez,

Springstein,

Nieves-Morión

et al. 2023

mBio

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Anabaena sp. PCC 7120 grows by forming filaments of communicating cells and is considered a paradigm of bacterial multicellularity. Molecular exchanges between contiguous cells in the filament take place through multiprotein channels that traverse the septal peptidoglycan through nanopores connecting their cytoplasms. Besides, the septal-junction complexes contribute to strengthen the filament. In search for proteins with coiled-coil domains that could provide for cytoskeletal functions in Anabaena , we identified SepT (All2460). SepT is characteristic of the phylogenetic clade of filamentous cyanobacteria with the ability to undergo cell differentiation. SepT-GFP fusions indicate that the protein is located at the cell periphery and, conspicuously, in the intercellular septa. During cell division, the protein is found at midcell resembling the position of the divisome. The bacterial adenylate cyclase two-hybrid analysis shows SepT interactions with itself and putative elongasome (MreB, RodA), divisome (FtsW, SepF, ZipN), and septal-junction (SepJ)-related proteins. Thus, SepT appears to rely on the divisome for localization at mature intercellular septa to form part of intercellular protein complexes. Two independently obtained mutants lacking SepT showed alterations in cell size and impaired septal and peripheral peptidoglycan incorporation during cell growth and division. Notably, both mutants showed conspicuous alterations in the array of nanopores present in the intercellular peptidoglycan disks, including aberrant nanopore morphology, number, and distribution. SepT appears, therefore, to be involved in the control of peptidoglycan growth and the formation of cell-cell communication structures that are at the basis of the multicellular character of this group of cyanobacteria. IMPORTANCE Multicellular organization is a requirement for the development of complex organisms, and filamentous cyanobacteria such as Anabaena represent a paradigmatic case of bacterial multicellularity. The Anabaena filament can include hundreds of communicated cells that exchange nutrients and regulators and, depending on environmental conditions, can include different cell types specialized in distinct biological functions. Hence, the specific features of the Anabaena filament and how they are propagated during cell division represent outstanding biological issues. Here, we studied SepT, a novel coiled-coil-rich protein of Anabaena that is located in the intercellular septa and influences the formation of the septal specialized structures that allow communication between neighboring cells along the filament, a fundamental trait for the performance of Anabaena as a multicellular organism.

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The role of FraI in cell–cell communication and differentiation in the hormogonia-forming cyanobacterium Nostoc punctiforme

Janović,

Maldener,

Menzel

et al. 2024

mSphere

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Multicellular cyanobacteria, like Nostoc punctiforme, rely on septal junctions for cell–cell communication, which is crucial for coordinating various physiological processes including differentiation of N 2 -fixing heterocysts, spore-like akinetes, and hormogonia—short, motile filaments important for dispersal. In this study, we functionally characterize a protein, encoded by gene Npun_F4142, which in a random mutagenesis approach, initially showed a motility-related function. The reconstructed Npun_F4142 knockout mutant exhibits further distinct phenotypic traits, including altered hormogonia formation with significant reduced motility, inability to differentiate heterocysts and filament fragmentation. For that reason, we named the protein FraI (fragmentation phenotype). The mutant displays severely impaired cell–cell communication, due to almost complete absence of the nanopore array in the septal cell wall, which is an essential part of the septal junctions. Despite lack of communication, hormogonia in the Δ fraI mutant maintain motility and phototactic behavior, even though less pronounced than the wild type (WT). This suggests an alternative mechanism for coordinated movement beyond septal junctions. Our study underscores the significance of FraI in nanopore formation and cell differentiation, and provides additional evidence for the importance of septal junction formation and communication in various differentiation traits of cyanobacteria. The findings contribute to a deeper understanding of the regulatory networks governing multicellular cyanobacterial behavior, with implications for broader insights into microbial multicellularity. IMPORTANCE The filament-forming cyanobacterium Nostoc punctiforme serves as a valuable model for studying cell differentiation, including the formation of nitrogen-fixing heterocysts and hormogonia. Hormogonia filaments play a crucial role in dispersal and plant colonization, providing a nitrogen source through atmospheric nitrogen fixation, thus holding promise for fertilizer-free agriculture. The coordination among the hormogonia cells enabling uniform movement toward the positive signal remains poorly understood. This study investigates the role of septal junction-mediated communication in hormogonia differentiation and motility, by studying a Δ fraI mutant with significantly impaired communication. Surprisingly, impaired communication does not abolish synchronized filament movement, suggesting an alternative coordination mechanism. These findings deepen our understanding of cyanobacterial biology and have broader implications for multicellular behavior in prokaryotes.

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SepN is a septal junction component required for gated cell–cell communication in the filamentous cyanobacterium Nostoc

Cited by 3 publications

References 68 publications

The role of FraI in cell-cell communication and differentiation in the hormogonia-forming cyanobacterium Nostoc punctiforme

The role of FraI in cell-cell communication and differentiation in the hormogonia-forming cyanobacterium Nostoc punctiforme

SepT, a novel protein specific to multicellular cyanobacteria, influences peptidoglycan growth and septal nanopore formation in Anabaena sp. PCC 7120

The role of FraI in cell–cell communication and differentiation in the hormogonia-forming cyanobacterium Nostoc punctiforme

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