1.V.1.  The Filamentous Cyanobacterial Septal Pore (C-Septum) Family 

In the diazotrophic filaments of heterocyst-forming cyanobacteria, two different cell types, the CO₂-fixing vegetative cells and the N₂-fixing heterocysts, exchange nutrients, including some amino acids. In Anabaena sp. strain PCC 7120, the SepJ protein, composed of periplasmic and integral membrane (permease) sections, is located at the intercellular septa joining adjacent cells in the filament. The unicellular cyanobacterium Synechococcus elongatus strain PCC 7942 bears a gene, Synpcc7942_1024 (dmeA), encoding a permease homologous to the SepJ permease domain. Synechococcus strains lacking dmeA or lacking dmeA and expressing Anabaena sepJ have been constructed (Escudero et al. 2015). The Synechococcus dmeA mutant showed a 22 to 32% decrease in the uptake of aspartate, glutamate, and glutamine, a phenotype that could be partially complemented by Anabaena sepJ. Synechococcus mutants of an ATP-binding-cassette (ABC)-type transporter for polar amino acids showed >98% decreased uptake of glutamate irrespective of the presence of dmeA or Anabaena sepJ in the same strain. Thus, Synechococcus DmeA or Anabaena SepJ is needed to observe full activity of the ABC transporter. An Anabaena sepJ deletion mutant was impaired in glutamate and aspartate uptake, which also in this cyanobacterium, requires the activity of an ABC-type transporter for polar amino acids. SepJ appears therefore to generally stimulate the activity of cyanobacterial ABC-type transporters for polar amino acids. Conversely, an Anabaena mutant of three ABC-type transporters for amino acids was impaired in the intercellular transfer of 5-carboxyfluorescein, a SepJ-related property (Escudero et al. 2015).

Nitrogen fixation in these complex multicellular bacteria depends on metabolite exchange between the two cell types, with the heterocysts supplying combined-nitrogen compounds but dependent on the vegetative cells for photosynthetically produced carbon compounds. Nürnberg et al. 2015 used a fluorescent tracer to probe intercellular metabolite exchange in the filamentous heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120. They showed that esculin, a fluorescent sucrose analog, is incorporated by a sucrose import system into the cytoplasm of Anabaena cells, and the cytoplasmic esculin is rapidly and reversibly exchanged across vegetative-vegetative and vegetative-heterocyst cell junctions.  This intercellular metabolic communication was lost in older heterocysts. SepJ, FraC, and FraD are proteins located at the intercellular septa and may form structures analogous to gap junctions. A ΔsepJ ΔfraC ΔfraD triple mutant showed an altered septum structure with thinner septa but a denser peptidoglycan layer. Intercellular diffusion of esculin and fluorescein derivatives was impaired in this mutant, which also showed a greatly reduced frequency of nanopores in the intercellular septal cross walls.  FraC, FraD, and SepJ may be important for the formation of junctional structures that constitute the major pathway for feeding heterocysts with sucrose (Nürnberg et al. 2015). In addition, two proteins, AmiC1 and AmiC2 of Anabaena PCC7120l, which perforate the septal peptidoglycan, crating an array ofnanopores, may provide the framework for septal junction formation because they are required for intercellular communication (Bornikoel et al. 2017). 

Heterocyst-forming cyanobacteria grow as chains of cells (filaments or trichomes) in which the cells exchange regulators and nutrients. Flores et al. 2018 reviewed the morphological, physiological and genetic data that have led to an understanding of intercellular communication in these organisms. Intercellular molecular exchange appears to take place by simple diffusion through proteinaceous  septal junctions, which connect the adjacent cells in the filament and traverse the septal peptidoglycan through perforations known as nanopores. Proteins that are necessary to produce, and that may be components of, the septal junctions - SepJ, FraC and FraD - have been identified in the heterocyst-forming cyanobacterium Anabaena sp. strain PCC 7120 model. Additionally, several proteins that are necessary to produce a normal number of nanopores and functional septal junctions have been identified, including AmiC-type amidases, peptidoglycan-binding proteins and some membrane transporters. Septal junctions may be regulated, possibly by a gating mechanism (Flores et al. 2018).