Starvation Induces Extracellular Accumulation of Polyphosphate in <i>Dictyostelium discoideum</i> to Inhibit Macropinocytosis, Phagocytosis, and Exocytosis
<i>Dictyostelium discoideum</i> is a soil-dwelling unicellular eukaryote that accumulates extracellular polyphosphate (polyP). At high cell densities, when the cells are about to overgrow their food supply and starve, the corresponding high extracellular concentrations of polyP allow the...
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| Format: | Article |
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MDPI AG
2023-03-01
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| Series: | International Journal of Molecular Sciences |
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| Online Access: | https://www.mdpi.com/1422-0067/24/6/5923 |
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| author | Ramesh Rijal Issam Ismail Shiyu Jing Richard H. Gomer |
| author_facet | Ramesh Rijal Issam Ismail Shiyu Jing Richard H. Gomer |
| author_sort | Ramesh Rijal |
| collection | DOAJ |
| description | <i>Dictyostelium discoideum</i> is a soil-dwelling unicellular eukaryote that accumulates extracellular polyphosphate (polyP). At high cell densities, when the cells are about to overgrow their food supply and starve, the corresponding high extracellular concentrations of polyP allow the cells to preemptively anticipate starvation, inhibit proliferation, and prime themselves to begin development. In this report, we show that starved <i>D. discoideum</i> cells accumulate cell surface and extracellular polyP. Starvation reduces macropinocytosis, exocytosis, and phagocytosis, and we find that these effects require the G protein-coupled polyP receptor (GrlD) and two enzymes, Polyphosphate kinase 1 (Ppk1), which is required for synthesizing intracellular polyP, cell surface polyP, and some of the extracellular polyP, and Inositol hexakisphosphate kinase (I6kA), which is required for cell surface polyP and polyP binding to cells, and some of the extracellular polyP. PolyP reduces membrane fluidity, and we find that starvation reduces membrane fluidity; this effect requires GrlD and Ppk1, but not I6kA. Together, these data suggest that in starved cells, extracellular polyP decreases membrane fluidity, possibly as a protective measure. In the starved cells, sensing polyP appears to decrease energy expenditure from ingestion, and decrease exocytosis, and to both decrease energy expenditures and retain nutrients. |
| first_indexed | 2024-03-11T06:24:02Z |
| format | Article |
| id | doaj.art-6c0e112e504c4dc99be0a0d3fce06d23 |
| institution | Directory Open Access Journal |
| issn | 1661-6596 1422-0067 |
| language | English |
| last_indexed | 2024-03-11T06:24:02Z |
| publishDate | 2023-03-01 |
| publisher | MDPI AG |
| record_format | Article |
| series | International Journal of Molecular Sciences |
| spelling | doaj.art-6c0e112e504c4dc99be0a0d3fce06d232023-11-17T11:41:01ZengMDPI AGInternational Journal of Molecular Sciences1661-65961422-00672023-03-01246592310.3390/ijms24065923Starvation Induces Extracellular Accumulation of Polyphosphate in <i>Dictyostelium discoideum</i> to Inhibit Macropinocytosis, Phagocytosis, and ExocytosisRamesh Rijal0Issam Ismail1Shiyu Jing2Richard H. Gomer3Department of Biology, Texas A&M University, College Station, TX 77843-3474, USADepartment of Biology, Texas A&M University, College Station, TX 77843-3474, USADepartment of Biology, Texas A&M University, College Station, TX 77843-3474, USADepartment of Biology, Texas A&M University, College Station, TX 77843-3474, USA<i>Dictyostelium discoideum</i> is a soil-dwelling unicellular eukaryote that accumulates extracellular polyphosphate (polyP). At high cell densities, when the cells are about to overgrow their food supply and starve, the corresponding high extracellular concentrations of polyP allow the cells to preemptively anticipate starvation, inhibit proliferation, and prime themselves to begin development. In this report, we show that starved <i>D. discoideum</i> cells accumulate cell surface and extracellular polyP. Starvation reduces macropinocytosis, exocytosis, and phagocytosis, and we find that these effects require the G protein-coupled polyP receptor (GrlD) and two enzymes, Polyphosphate kinase 1 (Ppk1), which is required for synthesizing intracellular polyP, cell surface polyP, and some of the extracellular polyP, and Inositol hexakisphosphate kinase (I6kA), which is required for cell surface polyP and polyP binding to cells, and some of the extracellular polyP. PolyP reduces membrane fluidity, and we find that starvation reduces membrane fluidity; this effect requires GrlD and Ppk1, but not I6kA. Together, these data suggest that in starved cells, extracellular polyP decreases membrane fluidity, possibly as a protective measure. In the starved cells, sensing polyP appears to decrease energy expenditure from ingestion, and decrease exocytosis, and to both decrease energy expenditures and retain nutrients.https://www.mdpi.com/1422-0067/24/6/5923polyphosphate<i>Dictyostelium</i>developmentmembrane fluiditynutrientscell mass |
| spellingShingle | Ramesh Rijal Issam Ismail Shiyu Jing Richard H. Gomer Starvation Induces Extracellular Accumulation of Polyphosphate in <i>Dictyostelium discoideum</i> to Inhibit Macropinocytosis, Phagocytosis, and Exocytosis International Journal of Molecular Sciences polyphosphate <i>Dictyostelium</i> development membrane fluidity nutrients cell mass |
| title | Starvation Induces Extracellular Accumulation of Polyphosphate in <i>Dictyostelium discoideum</i> to Inhibit Macropinocytosis, Phagocytosis, and Exocytosis |
| title_full | Starvation Induces Extracellular Accumulation of Polyphosphate in <i>Dictyostelium discoideum</i> to Inhibit Macropinocytosis, Phagocytosis, and Exocytosis |
| title_fullStr | Starvation Induces Extracellular Accumulation of Polyphosphate in <i>Dictyostelium discoideum</i> to Inhibit Macropinocytosis, Phagocytosis, and Exocytosis |
| title_full_unstemmed | Starvation Induces Extracellular Accumulation of Polyphosphate in <i>Dictyostelium discoideum</i> to Inhibit Macropinocytosis, Phagocytosis, and Exocytosis |
| title_short | Starvation Induces Extracellular Accumulation of Polyphosphate in <i>Dictyostelium discoideum</i> to Inhibit Macropinocytosis, Phagocytosis, and Exocytosis |
| title_sort | starvation induces extracellular accumulation of polyphosphate in i dictyostelium discoideum i to inhibit macropinocytosis phagocytosis and exocytosis |
| topic | polyphosphate <i>Dictyostelium</i> development membrane fluidity nutrients cell mass |
| url | https://www.mdpi.com/1422-0067/24/6/5923 |
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