Metabolic control of acclimation to nutrient deprivation dependent on polyphosphate synthesis

Abstract

Polyphosphate, an energy-rich polymer conserved in all kingdoms of life, is integral to many cellular stress responses, including nutrient deprivation, and yet, the mechanisms that underlie its biological roles are not well understood. In this work, we elucidate the physiological function of this polymer in the acclimation of the model alga Chlamydomonas reinhardtii to nutrient deprivation. Our data reveal that polyphosphate synthesis is vital to control cellular adenosine 5′-triphosphate homeostasis and maintain both respiratory and photosynthetic electron transport upon sulfur deprivation. Using both genetic and pharmacological approaches, we show that electron flow in the energy-generating organelles is essential to induce and sustain acclimation to sulfur deprivation at the transcriptional level. These previously unidentified links among polyphosphate synthesis, photosynthetic and respiratory electron flow, and the acclimation of cells to nutrient deprivation could unveil the mechanism by which polyphosphate helps organisms cope with a myriad of stress conditions in a fluctuating environment.

Responses of Chlamydomonas reinhardtii during the transition from P‐deficient to P‐sufficient growth (the P‐overplus response): The roles of the vacuolar transport chaperones and polyphosphate synthesis

“…In eukaryotes, the VTC complex drives the synthesis of polyP (Sanz‐Luque et al. 2020a,b). In Saccharomyces cerevisiae , the VTC complex is associated with vacuoles membrane and/or the endoplasmic reticulum, and it can be found either as a complex of VTC4/VTC2/VTC1 or VTC4/VTC3/VTC1 subunits.…”

“…2016, Dyhrman 2016, Samadani and Dewez 2018, Sanz‐luque et al. 2020a,b). PolyP was also recently associated with the responses of C. reinhardtii to nitrogen (N) and sulfur (S) starvation (Aksoy et al.…”

Polyphosphate affects cytoplasmic and chromosomal dynamics in nitrogen-starved Pseudomonas aeruginosa

“…In addition to viscoadaptation, another non-exclusive mechanism may be a direct effect on cellular bioenergetics via ATP. PolyP, which is synthesized by polyP kinase enzymes from ATP, may decrease available ATP pools, as has been suggested in studies in both E. coli during oxidative stress and Chlamydomonas reinhardtii during nitrogen starvation (26,27). Increased ATP would be expected to lead to more frequent cytoplasmic rearrangements and microagitations.…”

Insights of intracellular/intercellular phosphate transport and signaling in unicellular green algae and multicellular land plants

“…Under P deprivation, polyP chains are hydrolyzed by endo‐polyphosphatases to yield Pi in the vacuole, which is exported by Pho91, a transporter containing both an SPX domain and an SLC domain (Hürlimann et al ., 2007). Likewise, in unicellular green algae, taking Chlamydomonas as an example, SPX‐VTCs and SPX‐SLCs proteins take charge of vacuolar polyP synthesis/influx and Pi efflux, respectively (Sanz‐Luque et al ., 2020; Wang et al ., 2021) (Fig. 1a).…”

“…However, the mechanisms of vacuolar polyP homeostasis and relevant transporters in green algae are still unclear until recently. Two most recent studies show that SPX‐VTC (containing both SPX and VTC domain, VTC named after vacuolar transporter chaperone) and SPX‐SLC (containing both SPX and SLC domain, SLC named after permease solute carrier 13) proteins are responsible for vacuolar Pi synthesis/influx and efflux of vacuolar polyP in green algae, respectively, and transition of P storage forms might be a consequence of loss of these two gene families in the ancestor of later diverging streptophytes (Sanz‐Luque et al ., 2020; Wang et al ., 2021). In addition, despite the advances in understanding the role of inositol pyrophosphates (InsPs) in Pi signaling and homeostasis (Dong et al ., 2019; Zhu et al ., 2019; Ried et al ., 2021), there are still wide gaps in our knowledge of molecular mechanisms of intracellular Pi homeostasis, as well as intercellular Pi translocation in multicellular land plants.…”