Impaired cell-cell communication in the multicellular cyanobacterium Anabaena affects carbon uptake, photosynthesis, and the cell wall

Camargo, S.S.; Leshkowitz, Dena; Dassa, Bareket; Mariscal, Vicente; Flores, Enrique; Stavans, Joel; Arbel-Goren, Rinat

doi:10.1016/j.isci.2020.101977

Cited by 9 publications

(11 citation statements)

References 59 publications

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“…nitrogen deprivation only at a low level. Thus, sepJ is induced approximately 1.5-fold to 2fold under nitrogen deprivation (31)(32)(33), whereas fraC and fraD have been reported to be expressed constitutively (15,33) or induced approximately 2-fold under nitrogen deprivation (32). These observations, together with the rapid response to combined N described here, are consistent with a rapid regulation of the septal junctions by a mechanism of gating, as previously suggested (16), rather than with strong induction/repression mechanisms.…”

Section: Discussionsupporting

confidence: 89%

Coexistence of Communicating and Noncommunicating Cells in the Filamentous Cyanobacterium Anabaena

Arévalo

Nenninger

Nieves-Morión

et al. 2021

mSphere

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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.

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Section: Discussionsupporting

confidence: 89%

Coexistence of Communicating and Noncommunicating Cells in the Filamentous Cyanobacterium Anabaena

Arévalo

Nenninger

Nieves-Morión

et al. 2021

mSphere

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“…In contrast to the WT, the fraC fraD mutant fixed CO 2 at high levels in spite of being deficient in N 2 fixation. This might be related to an altered regulation of C assimilation as recently observed by transcriptomic analysis ( 35 ), which showed increased expression of genes encoding carbon uptake systems and some photosynthetic components in Anabaena mutants lacking septal proteins, including FraCD. In summary, our results have revealed the metabolic heterogeneity of individual cells and filaments in an Anabaena culture under controlled laboratory conditions, highlighting the interplay between C and N 2 fixation and assimilation, which are highly regulated processes ( 32 ).…”

Section: Discussionmentioning

confidence: 54%

Single-Cell Measurements of Fixation and Intercellular Exchange of C and N in the Filaments of the Heterocyst-Forming Cyanobacterium Anabaena sp. Strain PCC 7120

Nieves-Morión

Flores

Whitehouse

et al. 2021

mBio

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“…These transcriptional changes should be taken with caution because it has recently revealed that plasmid genes may suffer genome rearrangements in mutant strains of Anabaena sp. PCC7120 (Camargo et al, 2021). The expression of seven selected genes belonging to different functional categories was analysed in the EB2770FurC strain related to Anabaena sp.…”

Section: Resultsmentioning

confidence: 99%

FurC (PerR) from Anabaena sp. PCC7120: a versatile transcriptional regulator engaged in the regulatory network of heterocyst development and nitrogen fixation

Sarasa‐Buisan

Guío

Broset

et al. 2021

Environmental Microbiology

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FurC (PerR) from Anabaena sp. PCC7120 was previously described as a key transcriptional regulator involved in setting off the oxidative stress response. In the last years, the cross-talk between oxidative stress, iron homeostasis and nitrogen metabolism is becoming more and more evident. In this work, the transcriptome of a furC-overexpressing strain was compared with that of a wild-type strain under both standard and nitrogen-deficiency conditions. The results showed that the overexpression of furC deregulates genes involved in several categories standing out photosynthesis, iron transport and nitrogen metabolism. The novel FurC-direct targets included some regulatory elements that control heterocyst development (hetZ and asr1734), genes directly involved in the heterocyst envelope formation (devBCA and hepC) and genes which participate in the nitrogen fixation process (nifHDK and nifH2, rbrA rubrerythrin and xisHI excisionase). Likewise, furC overexpression notably impacts the mRNA levels of patA encoding a key protein in the heterocyst pattern formation. The relevance of FurC in these processes is bringing out by the fact that the overexpression of furC impairs heterocyst development and cell growth under nitrogen stepdown conditions. In summary, this work reveals a new player in the complex regulatory network of heterocyst formation and nitrogen fixation.

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Impaired cell-cell communication in the multicellular cyanobacterium Anabaena affects carbon uptake, photosynthesis, and the cell wall

Cited by 9 publications

References 59 publications

Coexistence of Communicating and Noncommunicating Cells in the Filamentous Cyanobacterium Anabaena

Coexistence of Communicating and Noncommunicating Cells in the Filamentous Cyanobacterium Anabaena

Single-Cell Measurements of Fixation and Intercellular Exchange of C and N in the Filaments of the Heterocyst-Forming Cyanobacterium Anabaena sp. Strain PCC 7120

FurC (PerR) from Anabaena sp. PCC7120: a versatile transcriptional regulator engaged in the regulatory network of heterocyst development and nitrogen fixation

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