Structure and function of a bacterial gap junction analog

Weiss, Gregor L.; Kieninger, Ann-Katrin; Maldener, Iris; Forchhammer, Karl; Pilhofer, Martin

doi:10.1101/462465

Cited by 22 publications

(82 citation statements)

References 38 publications

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“…The Anabaena septal junctions are putatively composed of several proteins, among which are SepJ, FraC and FraD, whose deletion abrogated intercellular molecular exchange, hence they were considered putative septal junction components (Flores et al, ; Merino‐Puerto, Mariscal, Mullineaux, Herrero, & Flores, ; Mullineaux et al, ; Nürnberg et al, ). The role of FraD in septal junctions recently gained additional support with the observation of septal junction structures that link the cytoplasms of neighboring cells and contain FraD (Weiss, Kieninger, Maldener, Forchhammer, & Pilhofer, ). Septal junctions mediate molecular diffusion between adjacent cells and are likely regulated by gating, thus predating the gated mechanism of eukaryotic gap junctions (Flores, Nieves‐Morión, & Mullineaux, ; Nieves‐Morión, Mullineaux, & Flores, ; Nürnberg et al, ; Weiss et al, ).…”

Section: Introductionmentioning

confidence: 90%

“…The role of FraD in septal junctions recently gained additional support with the observation of septal junction structures that link the cytoplasms of neighboring cells and contain FraD (Weiss, Kieninger, Maldener, Forchhammer, & Pilhofer, ). Septal junctions mediate molecular diffusion between adjacent cells and are likely regulated by gating, thus predating the gated mechanism of eukaryotic gap junctions (Flores, Nieves‐Morión, & Mullineaux, ; Nieves‐Morión, Mullineaux, & Flores, ; Nürnberg et al, ; Weiss et al, ). The Anabaena septal junctions traverse the septal PG through holes, termed “nanopores”, whose formation is dependent on PG amidases (AmiC) and the PG binding protein SjcF1 (Bornikoel et al, ; Rudolf et al, ).…”

Section: Introductionmentioning

confidence: 90%

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A novel septal protein of multicellular heterocystous cyanobacteria is associated with the divisome

Springstein

Arévalo

Helbig

et al. 2020

Molecular Microbiology

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Cyanobacteria are unique among the eubacteria as they possess a hybrid Gram phenotype, having an outer membrane but also a comparably thick peptidoglycan sheet. Furthermore, the cyanobacterial divisome includes proteins specific for both the Gram types as well as cyanobacteria‐specific proteins. Cells in multicellular cyanobacteria share a continuous periplasm and their cytoplasms are connected by septal junctions that enable communication between cells in the filament. The localization of septal junction proteins depends on interaction with the divisome, however additional yet unknown proteins may be involved in this process. Here, we characterized Alr3364 (termed SepI), a novel septal protein that interacts with the divisome in the multicellular heterocystous cyanobacterium Anabaena sp. strain PCC 7120. SepI localized to the Z‐ring and the intercellular septa but did not interact with FtsZ. Instead, SepI interacted with the divisome proteins ZipN, SepF and FtsI and with the septal protein SepJ. The inactivation of sepI led to a defect in cell filament integrity, colony and cell morphology, septum size, nanopore formation and peptidoglycan biogenesis, and inability to differentiate heterocysts. Our results show that SepI plays a role in intercellular communication and furthermore indicate that SepI functions in the coordination of septal junction localization during cell division.

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Section: Introductionmentioning

confidence: 90%

Section: Introductionmentioning

confidence: 90%

A novel septal protein of multicellular heterocystous cyanobacteria is associated with the divisome

Springstein

Arévalo

Helbig

et al. 2020

Molecular Microbiology

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“…4a, Supplementary Fig. 17), two other septal junction proteins 44 . Since coiled-coil motifs are well-known protein-protein interaction domains 45, 46 , they are putatively prone for false-positive results in the interaction assays.…”

Section: Resultsmentioning

confidence: 99%

Two novel heteropolymer-forming proteins maintain multicellular shape of the cyanobacteriumAnabaenasp. PCC 7120

Springstein

Nürnberg²,

Kieninger

et al. 2019

Preprint

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23The determinants of bacterial cell shape are extensively studied in unicellular forms. 24Nonetheless, the mechanisms that shape bacterial multicellular forms remain understudied. 25Here we study coiled-coil rich proteins (CCRPs) in the multicellular cyanobacterium Anabaena 26 sp. PCC 7120 (hereafter Anabaena). Our results reveal two CCPRs, termed LfiA and LfiB (for 27 linear filament), which assemble into a heteropolymer that traverses the longitudinal cell axis. 28Two additional CCRPs, CypS (for cyanobacterial polar scaffold) and CeaR (for cyanobacterial 29 elongasome activity regulator), form a polar proteinaceous scaffold and regulate MreB activity, 30 respectively. Deletion mutants of these CCRPs are characterized by impaired filament shape 31 and decreased viability. Our results indicate that the four CCRPs form a proteinaceous network 32 that stabilizes the Anabaena multicellular filament. We propose that this cytoskeletal network 33 is essential for the manifestation of the linear filament phenotype in Anabaena. 34 (a multi-enzyme complex), is a regulator of longitudinal PG biogenesis, and thus it plays a 49 crucial role in the adaption to different environments and prokaryotic multicellularity. 50The key hallmarks of permanent bacterial multicellularity are morphological 51 differentiation and a well-defined and reproducible shape, termed patterned multicellularity 3 . 52Unlike biofilms, patterned multicellular structures are the result of either coordinated swarming 53 or developmental aggregation behavior as in myxobacteria 9 . Additional factors include cell 54 division, proliferation and cell differentiation as in sporulating actinomycetes 10 and 55 cyanobacterial filaments 11,12 . In myxobacteria as well as in actinomycetes, it has been shown 56 that patterned multicellular traits are dependent on the coordinated function of different coiled-57 coil-rich proteins (CCRPs). Reminiscent of eukaryotic intermediate filaments (IFs) 13,14 , many 58 bacterial CCRPs were shown to perform analogous cytoskeletal functions through their ability 59 to self-assemble into distinct filaments in vitro and in vivo [15][16][17][18][19] . Unlike FtsZ or MreB 20,21 , 60 bacterial IF-like CCRPs do not require any additional co-factors for polymerization in vitro 22 . 61For example, in Myxococcus xanthus, the coordinated swarming and aggregation into fruiting 62 bodies is mediated by its gliding motility 23 , which strictly depends on the filament-forming 63 CCRP AglZ 24 . AglZ is organized in a large multi-protein complex that governs gliding motility 64 in synergy with MreB, which still retained its PG synthesis function but was also co-opted for 65 gliding motility in M. xanthus [25][26][27][28] . Actinobacteria, such as Streptomyces species, grow by 66 building new cell wall (i.e. PG) only at the cell poles, independent of MreB 29,30 , which is 67 strikingly different from how most other bacteria grow 31 . This characteristic polar growth mode 68 is organized by a cytoskeletal network of at least three CCRPs -DivIVA...

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“…Hence, HglK might influence the formation of septal junctions rather than constitute an independent type of junctions. The recently visualized FraD‐containing septal junctions evidently comprise additional proteins (Weiss et al, ). Whether HglK could be a component of the septal junctions or solely contribute to their assembly remains to be investigated.…”

Section: Discussionmentioning

confidence: 99%

“…Two types of septal junctions may be present in Anabaena , one related to SepJ and another related to FraC and FraD (Merino‐Puerto et al, ; Nürnberg et al, ). Septal junctions that contain FraD and require FraC for full assembly have been recently visualized by cryoET (Weiss, Kieninger, Maldener, Forchhammer, & Pilhofer, ). Because these junctions are still observed in a sepJ mutant, the structures responsible for specific sepJ intercellular communication phenotypes (Corrales‐Guerrero et al, ; Mariscal, Nürnberg, Herrero, Mullineaux, & Flores, ; Rivers, Videau, & Callahan, ) remain to be identified.…”

Section: Introductionmentioning

confidence: 99%

Pentapeptide‐repeat, cytoplasmic‐membrane protein HglK influences the septal junctions in the heterocystous cyanobacterium Anabaena

Arévalo

Flores

2020

Molecular Microbiology

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N 2 -fixing heterocystous cyanobacteria grow as chains of cells that are connected by proteinaceous septal junctions, which traverse the septal peptidoglycan through nanopores and mediate intercellular molecular transfer. In the model organism Anabaena sp. strain PCC 7120, proteins SepJ, FraC and FraD, which are localized at the cell poles in the intercellular septa, are needed to produce septal junctions.The pentapeptide-repeat, membrane-spanning protein HglK has been described to be involved in the deposition of the heterocyst-specific glycolipid layer, but the hglK mutant also showed intercellular septa broader than in the wild type. Here we found that hglK mutant of Anabaena is impaired in the expression of heterocyst-related genes coxB2A2C2 (cytochrome c oxidase) and nifHDK (nitrogenase), indicating a defect in heterocyst differentiation. HglK was predominantly localized at the intercellular septa and was required to make long filaments, produce a normal number of nanopores and express full intercellular molecular transfer activity. However, the effects of hglK inactivation were not additive to those of the inactivation of sepJ and/ or fraC-fraD. We suggest that HglK contributes to the architecture of the intercellular septa with an impact on the function of septal junctions. K E Y W O R D S bacterial development, cyanobacteria, heterocyst differentiation, intercellular communication, nitrogen fixation, pentapeptide-repeat protein, septal junctions | 795 ARÉVALO And FLORES

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Structure and function of a bacterial gap junction analog

Cited by 22 publications

References 38 publications

A novel septal protein of multicellular heterocystous cyanobacteria is associated with the divisome

A novel septal protein of multicellular heterocystous cyanobacteria is associated with the divisome

Two novel heteropolymer-forming proteins maintain multicellular shape of the cyanobacteriumAnabaenasp. PCC 7120

Pentapeptide‐repeat, cytoplasmic‐membrane protein HglK influences the septal junctions in the heterocystous cyanobacterium Anabaena

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