Abstract
PII signal transduction proteins are widely spread among all domains of life where they regulate a multitude of carbon and nitrogen metabolism related processes. Non-diazotrophic cyanobacteria can utilize a high variety of organic and inorganic nitrogen sources. In recent years, several physiological studies indicated an involvement of the cyanobacterial PII protein in regulation of ammonium, nitrate/nitrite, and cyanate uptake. However, direct interaction of PII has not been demonstrated so far. In this study, we used biochemical, molecular genetic and physiological approaches to demonstrate that PII regulates all relevant nitrogen uptake systems in Synechocystis sp. strain PCC 6803: PII controls ammonium uptake by interacting with the Amt1 ammonium permease, probably similar to the known regulation of E. coli ammonium permease AmtB by the PII homolog GlnK. We could further clarify that PII mediates the ammonium- and dark-induced inhibition of nitrate uptake by interacting with the NrtC and NrtD subunits of the nitrate/nitrite transporter NrtABCD. We further identified the ABC-type urea transporter UrtABCDE as novel PII target. PII interacts with the UrtE subunit without involving the standard interaction surface of PII interactions. The deregulation of urea uptake in a PII deletion mutant causes ammonium excretion when urea is provided as nitrogen source. Furthermore, the urea hydrolyzing urease enzyme complex appears to be coupled to urea uptake. Overall, this study underlines the great importance of the PII signal transduction protein in the regulation of nitrogen utilization in cyanobacteria.
Highlights
The emergence of the oxygenic photosynthesis by ancestors of present cyanobacteria (Soo et al, 2017) laid the ground for the evolution of present days life on planet earth
PII-Venus perfectly complemented the nitrite excretion phenotype. These results indicated that the Bordetella pertussis adenylate cyclase two-hybrid system (BACTH) interactions of PII with the NrtC and NtcD subunits are physiologically meaningful
It is highly probable that the same holds true for other cyanobacteria
Summary
The emergence of the oxygenic photosynthesis by ancestors of present cyanobacteria (Soo et al, 2017) laid the ground for the evolution of present days life on planet earth. Cyanobacteria occupy a high variety of illuminated habitats, where they represent one of the most abundant primary producers (Whitton, 2012). PII Controls Nitrogen Uptake in Cyanobacteria (Herrero and Flores, 2008). Nitrogen represents a necessary macronutrient for all living organisms and constitutes an important growth-limiting factor in most ecosystems (Vitousek and Howarth, 1991). The regulation of nitrogen metabolism in cyanobacteria mainly depends on the fine-tuned network of the signal transduction protein PII, the global nitrogen transcription factor NtcA and the NtcA co-activator PipX (Vegapalas et al, 1992; Espinosa et al, 2006, 2007, 2014; Forchhammer, 2008; Luque and Forchhammer, 2008; Forcada-Nadal et al, 2018)
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