Response of cyanobacterial mats to ambient phosphate fluctuations: phosphorus cycling, polyphosphate accumulation and stoichiometric flexibility

Abstract Cyanobacterial mats inhabit a variety of aquatic habitats, including the most extreme environments on Earth. They can thrive in a wide range of phosphorus (P) levels and are thus important players for ecosystem primary production and P cycling at the sediment-water interface. Polyphosphate...

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Main Authors: Laura Jentzsch, Hans-Peter Grossart, Sascha Plewe, Dirk Schulze-Makuch, Tobias Goldhammer
Format: Article
Language:English
Published: Oxford University Press 2023-01-01
Series:ISME Communications
Online Access:https://doi.org/10.1038/s43705-023-00215-x
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author Laura Jentzsch
Hans-Peter Grossart
Sascha Plewe
Dirk Schulze-Makuch
Tobias Goldhammer
author_facet Laura Jentzsch
Hans-Peter Grossart
Sascha Plewe
Dirk Schulze-Makuch
Tobias Goldhammer
author_sort Laura Jentzsch
collection DOAJ
description Abstract Cyanobacterial mats inhabit a variety of aquatic habitats, including the most extreme environments on Earth. They can thrive in a wide range of phosphorus (P) levels and are thus important players for ecosystem primary production and P cycling at the sediment-water interface. Polyphosphate (polyP), the major microbial P storage molecule, is assigned a critical role in compensating for phosphate fluctuations in planktonic cyanobacteria, but little is known about potentially analogous mechanisms of mat-forming cyanobacteria. To investigate acclimation strategies of cyanobacterial mats to fluctuating phosphate concentrations, laboratory batch experiments were conducted, in which the cosmopolitan mat-forming, marine cyanobacterium Sodalinema stali was exposed to low dissolved P concentrations, followed by a P pulse. Our results show that the cyanobacteria dynamically adjusted cellular P content to ambient phosphate concentrations and that they had accumulated polyP during periods of high phosphate availability, which was subsequently recycled to sustain growth during phosphate scarcity. However, following the depletion of dispensable cellular P sources, including polyP, we observed a reallocation of P contained in DNA into polyP, accompanied by increasing alkaline phosphatase activity. This suggests a change of the metabolic focus from growth towards maintenance and the attempt to acquire organic P, which would be naturally contained in the sediment. P overplus uptake following a simulated P pulse further suggests that Sodalinema-dominated mats exhibit elaborated mechanisms to cope with severe P fluctuations to overcome unfavourable environmental conditions, and potentially modulate critical P fluxes in the aquatic cycle.
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spelling doaj.art-2180f5dd601142a8a3a65e3f1f41fc7e2024-04-02T03:57:48ZengOxford University PressISME Communications2730-61512023-01-013111010.1038/s43705-023-00215-xResponse of cyanobacterial mats to ambient phosphate fluctuations: phosphorus cycling, polyphosphate accumulation and stoichiometric flexibilityLaura Jentzsch0Hans-Peter Grossart1Sascha Plewe2Dirk Schulze-Makuch3Tobias Goldhammer4Department of Ecohydrology and Biogeochemistry, Leibniz Institute of Freshwater Ecology and Inland FisheriesDepartment of Plankton and Microbial Ecology, Leibniz Institute of Freshwater Ecology and Inland FisheriesDepartment of Marine Geology, Leibniz Institute for Baltic Sea Research WarnemündeAstrobiology Research Group, Zentrum für Astronomie und Astrophysik, Technische Universität BerlinDepartment of Ecohydrology and Biogeochemistry, Leibniz Institute of Freshwater Ecology and Inland FisheriesAbstract Cyanobacterial mats inhabit a variety of aquatic habitats, including the most extreme environments on Earth. They can thrive in a wide range of phosphorus (P) levels and are thus important players for ecosystem primary production and P cycling at the sediment-water interface. Polyphosphate (polyP), the major microbial P storage molecule, is assigned a critical role in compensating for phosphate fluctuations in planktonic cyanobacteria, but little is known about potentially analogous mechanisms of mat-forming cyanobacteria. To investigate acclimation strategies of cyanobacterial mats to fluctuating phosphate concentrations, laboratory batch experiments were conducted, in which the cosmopolitan mat-forming, marine cyanobacterium Sodalinema stali was exposed to low dissolved P concentrations, followed by a P pulse. Our results show that the cyanobacteria dynamically adjusted cellular P content to ambient phosphate concentrations and that they had accumulated polyP during periods of high phosphate availability, which was subsequently recycled to sustain growth during phosphate scarcity. However, following the depletion of dispensable cellular P sources, including polyP, we observed a reallocation of P contained in DNA into polyP, accompanied by increasing alkaline phosphatase activity. This suggests a change of the metabolic focus from growth towards maintenance and the attempt to acquire organic P, which would be naturally contained in the sediment. P overplus uptake following a simulated P pulse further suggests that Sodalinema-dominated mats exhibit elaborated mechanisms to cope with severe P fluctuations to overcome unfavourable environmental conditions, and potentially modulate critical P fluxes in the aquatic cycle.https://doi.org/10.1038/s43705-023-00215-x
spellingShingle Laura Jentzsch
Hans-Peter Grossart
Sascha Plewe
Dirk Schulze-Makuch
Tobias Goldhammer
Response of cyanobacterial mats to ambient phosphate fluctuations: phosphorus cycling, polyphosphate accumulation and stoichiometric flexibility
ISME Communications
title Response of cyanobacterial mats to ambient phosphate fluctuations: phosphorus cycling, polyphosphate accumulation and stoichiometric flexibility
title_full Response of cyanobacterial mats to ambient phosphate fluctuations: phosphorus cycling, polyphosphate accumulation and stoichiometric flexibility
title_fullStr Response of cyanobacterial mats to ambient phosphate fluctuations: phosphorus cycling, polyphosphate accumulation and stoichiometric flexibility
title_full_unstemmed Response of cyanobacterial mats to ambient phosphate fluctuations: phosphorus cycling, polyphosphate accumulation and stoichiometric flexibility
title_short Response of cyanobacterial mats to ambient phosphate fluctuations: phosphorus cycling, polyphosphate accumulation and stoichiometric flexibility
title_sort response of cyanobacterial mats to ambient phosphate fluctuations phosphorus cycling polyphosphate accumulation and stoichiometric flexibility
url https://doi.org/10.1038/s43705-023-00215-x
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