Molecular Diffusion through Cyanobacterial Septal Junctions

Nieves-Morión, Mercedes; Mullineaux, Conrad W.; Flores, Enrique

doi:10.1128/mbio.01756-16

Cited by 34 publications

(31 citation statements)

References 24 publications

(47 reference statements)

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“…Nonetheless, other (perhaps many) metabolites may also be translocated from vegetative cells to heterocysts, including alanine, which may serve as a source of reductant in the heterocysts (Jüttner, 1983;Pernil et al, 2010), and some reduced forms of sulfur (Giddings et al, 1981). Metabolite exchange between vegetative cells and heterocysts appears to take place by diffusion through proteinaceous structures known as septal junctions that are located in the intercellular septa and join the adjacent cells in the filament (Nürnberg et al, 2015;Flores et al, 2016;Nieves-Morión et al, 2017).…”

Section: Heterocyst Differentiation and Functionmentioning

confidence: 99%

Genetic responses to carbon and nitrogen availability in Anabaena

Herrero

Flores

2018

Environmental Microbiology

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Heterocyst-forming cyanobacteria are filamentous organisms that perform oxygenic photosynthesis and CO fixation in vegetative cells and nitrogen fixation in heterocysts, which are formed under deprivation of combined nitrogen. These organisms can acclimate to use different sources of nitrogen and respond to different levels of CO . Following work mainly done with the best studied heterocyst-forming cyanobacterium, Anabaena, here we summarize the mechanisms of assimilation of ammonium, nitrate, urea and N , the latter involving heterocyst differentiation, and describe aspects of CO assimilation that involves a carbon concentration mechanism. These processes are subjected to regulation establishing a hierarchy in the assimilation of nitrogen sources -with preference for the most reduced nitrogen forms- and a dependence on sufficient carbon. This regulation largely takes place at the level of gene expression and is exerted by a variety of transcription factors, including global and pathway-specific transcriptional regulators. NtcA is a CRP-family protein that adjusts global gene expression in response to the C-to-N balance in the cells, and PacR is a LysR-family transcriptional regulator (LTTR) that extensively acclimates the cells to oxygenic phototrophy. A cyanobacterial-specific transcription factor, HetR, is involved in heterocyst differentiation, and other LTTR factors are specifically involved in nitrate and CO assimilation.

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Section: Heterocyst Differentiation and Functionmentioning

confidence: 99%

Genetic responses to carbon and nitrogen availability in Anabaena

Herrero

Flores

2018

Environmental Microbiology

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“…The intercellular molecular exchange via these structures in various filamentous strains has been quantified using fluorescent tracer molecules; however, the participating proteins, of which the Fra proteins (FraC, FraD and FraG/SepJ) are candidates constituting the septal junctions, are not fully understood (Flores et al ., ; Mullineaux et al ., ; Lehner et al ., ; Merino‐Puerto et al ., ; Nürnberg et al ., ; Rudolf et al ., ; Nieves‐Morión et al ., ; Zheng et al ., ). It was shown that the intercellular molecular exchange is primarily temperature dependent, suggesting that the molecules move by diffusion from cell to cell (Nieves‐Morión et al ., ; Kang et al ., ).…”

Section: Introductionmentioning

confidence: 98%

LytM factor Alr3353 affects filament morphology and cell–cell communication in the multicellular cyanobacterium Anabaena sp. PCC 7120

Bornikoel

Staiger

Madlung

et al. 2018

Molecular Microbiology

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Heterocyst-forming cyanobacteria are organized as multicellular filaments of tightly interacting, functionally specialized cells. N -fixing heterocysts differentiate from vegetative cells under nitrogen limitation in a semi-regular pattern along the filament. Diazotrophic growth requires metabolite exchange between neighboring cells within the filament. This exchange occurs via cell-cell junction complexes that span the gap between the plasma membranes and thereby cross the septal peptidoglycan through an array of uniform nanopores formed by AmiC-type cell wall hydrolases. We investigated how the lytic hydrolase AmiC1 (Alr0092) from Anabaena sp. PCC 7120, whose activity needs to be tightly controlled to avoid cell lysis, is regulated by the LytM factor Alr3353. Inactivation of alr3353 resulted in significantly fewer nanopores and as a consequence, a lower rate of fluorescent tracer exchange between cells. The mutant was not able to grow with N as sole nitrogen source, although heterocysts were formed. Alr3353 localized mainly to fully developed intercellular septa of vegetative cells. The purified protein bound to peptidoglycan and enhanced the hydrolytic activity of AmiC1 in vitro. Our data show that the LytM factor Alr3353 regulates nanopore formation and cell-cell communication by directly interacting with AmiC1.

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“…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: 99%

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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Molecular Diffusion through Cyanobacterial Septal Junctions

Cited by 34 publications

References 24 publications

Genetic responses to carbon and nitrogen availability in Anabaena

Genetic responses to carbon and nitrogen availability in Anabaena

LytM factor Alr3353 affects filament morphology and cell–cell communication in the multicellular cyanobacterium Anabaena sp. PCC 7120

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

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