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      Polyphosphate: A Multifunctional Metabolite in Cyanobacteria and Algae

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          Abstract

          Polyphosphate (polyP), a polymer of orthophosphate (PO 4 3-) of varying lengths, has been identified in all kingdoms of life. It can serve as a source of chemical bond energy (phosphoanhydride bond) that may have been used by biological systems prior to the evolution of ATP. Intracellular polyP is mainly stored as granules in specific vacuoles called acidocalcisomes, and its synthesis and accumulation appear to impact a myriad of cellular functions. It serves as a reservoir for inorganic PO 4 3- and an energy source for fueling cellular metabolism, participates in maintaining adenylate and metal cation homeostasis, functions as a scaffold for sequestering cations, exhibits chaperone function, covalently binds to proteins to modify their activity, and enables normal acclimation of cells to stress conditions. PolyP also appears to have a role in symbiotic and parasitic associations, and in higher eukaryotes, low polyP levels seem to impact cancerous proliferation, apoptosis, procoagulant and proinflammatory responses and cause defects in TOR signaling. In this review, we discuss the metabolism, storage, and function of polyP in photosynthetic microbes, which mostly includes research on green algae and cyanobacteria. We focus on factors that impact polyP synthesis, specific enzymes required for its synthesis and degradation, sequestration of polyP in acidocalcisomes, its role in cellular energetics, acclimation processes, and metal homeostasis, and then transition to its potential applications for bioremediation and medical purposes.

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          Widespread occurrence of a unicellular, marine, planktonic, cyanobacterium

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            Phosphonate utilization by the globally important marine diazotroph Trichodesmium.

            The factors that control the growth and nitrogen fixation rates of marine diazotrophs such as Trichodesmium have been intensively studied because of the role that these processes have in the global cycling of carbon and nitrogen, and in the sequestration of carbon to the deep sea. Because the phosphate concentrations of many ocean gyres are low, the bioavailability of the larger, chemically heterogeneous pool of dissolved organic phosphorus could markedly influence Trichodesmium physiology. Here we describe the induction, by phosphorus stress, of genes from the Trichodesmium erythraeum IMS101 genome that are predicted to encode proteins associated with the high-affinity transport and hydrolysis of phosphonate compounds by a carbon-phosphorus lyase pathway. We show the importance of these genes through expression analyses with T. erythraeum from the Sargasso Sea. Phosphonates are known to be present in oligotrophic marine systems, but have not previously been considered to be bioavailable to marine diazotrophs. The apparent absence of genes encoding a carbon-phosphorus lyase pathway in the other marine cyanobacterial genomes suggests that, relative to other phytoplankton, Trichodesmium is uniquely adapted for scavenging phosphorus from organic sources. This adaptation may help to explain the prevalence of Trichodesmium in low phosphate, oligotrophic systems.
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              The Pho regulon: a huge regulatory network in bacteria

              One of the most important achievements of bacteria is its capability to adapt to the changing conditions of the environment. The competition for nutrients with other microorganisms, especially in the soil, where nutritional conditions are more variable, has led bacteria to evolve a plethora of mechanisms to rapidly fine-tune the requirements of the cell. One of the essential nutrients that are normally found in low concentrations in nature is inorganic phosphate (Pi). Bacteria, as well as other organisms, have developed several systems to cope for the scarcity of this nutrient. To date, the unique mechanism responding to Pi starvation known in detail is the Pho regulon, which is normally controlled by a two component system and constitutes one of the most sensible and efficient regulatory mechanisms in bacteria. Many new members of the Pho regulon have emerged in the last years in several bacteria; however, there are still many unknown questions regarding the activation and function of the whole system. This review describes the most important findings of the last three decades in relation to Pi regulation in bacteria, including: the PHO box, the Pi signaling pathway and the Pi starvation response. The role of the Pho regulon in nutritional regulation cross-talk, secondary metabolite production, and pathogenesis is discussed in detail.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                26 June 2020
                2020
                : 11
                : 938
                Affiliations
                [1] 1 Department of Plant Biology, The Carnegie Institution for Science , Stanford, CA, United States
                [2] 2 Department of Biochemistry and Molecular Biology, University of Cordoba , Cordoba, Spain
                Author notes

                Edited by: Tatsuhiro Ezawa, Graduate School of Agriculture, Hokkaido University, Japan

                Reviewed by: Katsuharu Saito, Shinshu University, Japan; Adolfo Saiardi, University College London, United Kingdom

                *Correspondence: Emanuel Sanz-Luque, q92salue@ 123456uco.es

                This article was submitted to Plant Metabolism and Chemodiversity, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2020.00938
                7332688
                32670331
                643d4d3d-aaac-4970-851a-fb21b25bf93d
                Copyright © 2020 Sanz-Luque, Bhaya and Grossman

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 29 April 2020
                : 09 June 2020
                Page count
                Figures: 2, Tables: 0, Equations: 0, References: 315, Pages: 21, Words: 10403
                Funding
                Funded by: H2020 Marie Skłodowska-Curie Actions 10.13039/100010665
                Funded by: U.S. Department of Energy 10.13039/100000015
                Funded by: National Science Foundation 10.13039/100000001
                Categories
                Plant Science
                Review

                Plant science & Botany
                polyphosphate,microalgae,cyanobacteria,acidocalcisome,stress responses,phosphate metabolism,metal toxicity,bioremediation

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