Coexistence of Communicating and Noncommunicating Cells in the Filamentous Cyanobacterium Anabaena

Abstract

In filamentous heterocyst-forming (N₂-fixing) cyanobacteria, septal junctions join adjacent cells, mediating intercellular communication, and are thought to traverse the septal peptidoglycan through nanopores. Fluorescence recovery after photobleaching (FRAP) analysis with the fluorescent marker calcein showed that cultures of Anabaena sp. strain PCC 7120 grown in the presence of combined nitrogen contained a substantial fraction of noncommunicating cells (58% and 80% of the tested vegetative cells in nitrate- and ammonium-grown cultures, respectively), whereas cultures induced for nitrogen fixation contained far fewer noncommunicating cells (16%). A single filament could have communicating and noncommunicating cells. These observations indicate that all (or most of) the septal junctions in a cell can be coordinately regulated and are coherent with the need for intercellular communication, especially under diazotrophic conditions. Consistently, intercellular exchange was observed to increase in response to N deprivation and to decrease rapidly in response to the presence of ammonium in the medium or to nitrate assimilation. Proteins involved in the formation of septal junctions have been identified in Anabaena and include SepJ, FraC, and FraD. Here, we reevaluated rates of intercellular transfer of calcein and the number of nanopores in mutants lacking these proteins and found a strong positive correlation between the two parameters only in cultures induced for nitrogen fixation. Thus, whereas the presence of a substantial number of noncommunicating cells appears to impair the correlation, data obtained in diazotrophic cultures support the idea that the nanopores are the structures that hold the septal junctions.IMPORTANCE Multicellularity is found in bacteria as well as in eukaryotes, and the filamentous heterocyst-forming (N₂-fixing) cyanobacteria represent a simple and ancient paradigm of multicellular organisms. Multicellularity generally involves cell-cell adhesion and communication. The cells in the cyanobacterial filaments are joined by proteinaceous septal junctions that mediate molecular diffusion. The septal junctions traverse the septal peptidoglycan, which bears holes termed nanopores. Our results show that the septal junctions can be coordinately regulated in a cell and emphasize the relationship between septal junctions and nanopores to build intercellular communication structures, which are essential for the multicellular behavior of heterocyst-forming cyanobacteria.

Keywords: cyanobacteria; intercellular communication; septal junctions.