A storage-based model of heterocyst commitment and patterning in cyanobacteria

Abstract

When deprived of fixed nitrogen (fN), certain filamentous cyanobacteria differentiate nitrogen-fixing heterocysts. There is a large and dynamic fraction of stored fN in cyanobacterial cells, but its role in directing heterocyst commitment has not been identified. We present an integrated computational model of fN transport, cellular growth, and heterocyst commitment for filamentous cyanobacteria. By including fN storage proportional to cell length, but without any explicit cell-cycle effect, we are able to recover a broad and late range of heterocyst commitment times and we observe a strong indirect cell-cycle effect. We propose that fN storage is an important component of heterocyst commitment and patterning in filamentous cyanobacteria. The model allows us to explore both initial and steady-state heterocyst patterns. The developmental model is hierarchical after initial commitment: our only source of stochasticity is observed growth rate variability. Explicit lateral inhibition allows us to examine ΔpatS, ΔhetN, and ΔpatN phenotypes. We find that ΔpatS leads to adjacent heterocysts of the same generation, while ΔhetN leads to adjacent heterocysts only of different generations. With a shortened inhibition range, heterocyst spacing distributions are similar to those in experimental ΔpatN systems. Step-down to non-zero external fN concentrations is also investigated.

Dynamic, mechanistic, molecular‐level modelling of cyanobacteria: Anabaena and nitrogen interaction

“…Recent observations of N storage in cyanophycin granules in Anabaena heterocysts (Burnat et al ., ) are consistent with this finding. Other models also suggest a role for storage in timing of heterocyst development (Brown and Rutenberg, ). Figure C shows N fluxes in heterocysts and adjacent vegetative cells.…”

Morphological and isotopic changes of heterocystous cyanobacteria in response to N2 partial pressure

“…Nitrogenase expression and heterocyst development likely begin when photosynthetic vegetative cells become starved of bioavailable nitrogen beyond a threshold (Brown & Rutenberg, 2014;Fleming & Haselkorn, 1973;Kulasooriya, Lang, & Fay, 1972). Thus, heterocysts spatially separate the two incompatible processes that operate in Anabaena sp.…”

“…: photosynthesis and nitrogen fixation. Nitrogenase expression and heterocyst development likely begin when photosynthetic vegetative cells become starved of bioavailable nitrogen beyond a threshold (Brown & Rutenberg, 2014;Fleming & Haselkorn, 1973;Kulasooriya, Lang, & Fay, 1972). Some vegetative cells then undergo a series of structural and biochemical changes during differentiation into heterocysts, including developing multiple envelope layers (Murry & Wolk, 1989), increasing their respiration rate (Dalton & Postgate, 1969), and degrading the photosystem II complex (Thomas, 1970), that minimize the amount of oxygen present inside the cell.…”

“…Developmental controls undeniably play an important role in heterocyst development through the expression of regulatory genes that promote differentiation, such as ntcA and hetR (Buikema & Haselkorn, 1991;Wei, Ramasubramanian, & Golden, 1994), as well as the synthesis of inhibitory molecules that prevent differentiation, such as PatS and HetN (Callahan & Buikema, 2001;Yoon & Golden, 2001). Furthermore, several studies (Adams & Carr, 1989;Brown & Rutenberg, 2014;Meeks & Elhai, 2002) have suggested that heterocyst differentiation may be influenced by cell cycle timing, so it is possible that the variation in heterocyst spacing observed within identical pN 2 cultures is a consequence of filament cell cycles. Though this phenomenon was not investigated at the individual cellular level here, the slight differences in heterocyst spacing between growth stages highlight the possible macroinfluence of culture growth phase on heterocyst differentiation.…”

HetL provides immunity to HetR against PatS inhibition, and promotes pattern formation in the cyanobacteriumNostocPCC 7120

“…The HetR/PatS regulatory loop fits the local activation (HetR)/long range inhibition (PatS) module that 101 characterizes the Turing-adapted model of patterning (Brown & Rutenberg, 2014; A. Turing, 1952;A.…”