Overexpression of PSR1 in Chlamydomonas reinhardtii induces luxury phosphorus uptake

Remediation using micro-algae offers an attractive solution to environmental phosphate (PO43-) pollution. However, for maximum efficiency, pre-conditioning of algae to induce ‘luxury phosphorus (P) uptake’ is needed. To replicate this process, we targeted the global regulator PSR1 (Myb transcription...

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Main Authors: Stephen P. Slocombe, Tatiana Zúñiga-Burgos, Lili Chu, Payam Mehrshahi, Matthew P. Davey, Alison G. Smith, Miller Alonso Camargo-Valero, Alison Baker
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-07-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1208168/full
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author Stephen P. Slocombe
Tatiana Zúñiga-Burgos
Tatiana Zúñiga-Burgos
Lili Chu
Payam Mehrshahi
Matthew P. Davey
Alison G. Smith
Miller Alonso Camargo-Valero
Miller Alonso Camargo-Valero
Alison Baker
author_facet Stephen P. Slocombe
Tatiana Zúñiga-Burgos
Tatiana Zúñiga-Burgos
Lili Chu
Payam Mehrshahi
Matthew P. Davey
Alison G. Smith
Miller Alonso Camargo-Valero
Miller Alonso Camargo-Valero
Alison Baker
author_sort Stephen P. Slocombe
collection DOAJ
description Remediation using micro-algae offers an attractive solution to environmental phosphate (PO43-) pollution. However, for maximum efficiency, pre-conditioning of algae to induce ‘luxury phosphorus (P) uptake’ is needed. To replicate this process, we targeted the global regulator PSR1 (Myb transcription factor: Phosphate Starvation Response 1) for over-expression in algae. Manipulating a single gene (PSR1) drove uptake of both PO43- and a Mg2+ counter-ion leading to increased PolyP granule size, raising P levels 4-fold to 8% dry cell weight, and accelerated removal of PO43- from the medium. Examination of the gene expression profile showed that the P-starvation response was mimicked under P-replete conditions, switching on luxury uptake. Hyper-accumulation of P depended on a feed-forward mechanism, where a small set of ‘Class I’ P-transporter genes were activated despite abundant external PO43- levels. The transporters drove a reduction in external PO43- levels, permitting more genes to be expressed (Class II), leading to more P-uptake. Our data pointed toward a PSR1-independent mechanism for detection of external PO43- which suppressed Class II genes. This model provided a plausible mechanism for P-overplus where prior P-starvation elevates PSR1 and on P-resupply causes luxury P-uptake. This is because the Class I genes, which include P-transporter genes, are not suppressed by the excess PO43-. Taken together, these discoveries facilitate a bio-circular approach of recycling nutrients from wastewater back to agriculture.
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spelling doaj.art-f773281e1b1543bbb29928bb489413622023-07-27T16:44:53ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-07-011410.3389/fpls.2023.12081681208168Overexpression of PSR1 in Chlamydomonas reinhardtii induces luxury phosphorus uptakeStephen P. Slocombe0Tatiana Zúñiga-Burgos1Tatiana Zúñiga-Burgos2Lili Chu3Payam Mehrshahi4Matthew P. Davey5Alison G. Smith6Miller Alonso Camargo-Valero7Miller Alonso Camargo-Valero8Alison Baker9School of Molecular and Cellular Biology, Centre for Plant Sciences and Astbury Centre for Structural Molecular Biology, Faculty of Biological Sciences, University of Leeds, Leeds, United KingdomSchool of Molecular and Cellular Biology, Centre for Plant Sciences and Astbury Centre for Structural Molecular Biology, Faculty of Biological Sciences, University of Leeds, Leeds, United KingdomBioResource Systems Research Group, School of Civil Engineering, University of Leeds, Leeds, United KingdomSchool of Molecular and Cellular Biology, Centre for Plant Sciences and Astbury Centre for Structural Molecular Biology, Faculty of Biological Sciences, University of Leeds, Leeds, United KingdomDepartment of Plant Sciences, Cambridge University, Cambridge, United KingdomDepartment of Plant Sciences, Cambridge University, Cambridge, United KingdomDepartment of Plant Sciences, Cambridge University, Cambridge, United KingdomBioResource Systems Research Group, School of Civil Engineering, University of Leeds, Leeds, United KingdomDepartamento de Ingeniería Química, Universidad Nacional de Colombia, Manizales, ColombiaSchool of Molecular and Cellular Biology, Centre for Plant Sciences and Astbury Centre for Structural Molecular Biology, Faculty of Biological Sciences, University of Leeds, Leeds, United KingdomRemediation using micro-algae offers an attractive solution to environmental phosphate (PO43-) pollution. However, for maximum efficiency, pre-conditioning of algae to induce ‘luxury phosphorus (P) uptake’ is needed. To replicate this process, we targeted the global regulator PSR1 (Myb transcription factor: Phosphate Starvation Response 1) for over-expression in algae. Manipulating a single gene (PSR1) drove uptake of both PO43- and a Mg2+ counter-ion leading to increased PolyP granule size, raising P levels 4-fold to 8% dry cell weight, and accelerated removal of PO43- from the medium. Examination of the gene expression profile showed that the P-starvation response was mimicked under P-replete conditions, switching on luxury uptake. Hyper-accumulation of P depended on a feed-forward mechanism, where a small set of ‘Class I’ P-transporter genes were activated despite abundant external PO43- levels. The transporters drove a reduction in external PO43- levels, permitting more genes to be expressed (Class II), leading to more P-uptake. Our data pointed toward a PSR1-independent mechanism for detection of external PO43- which suppressed Class II genes. This model provided a plausible mechanism for P-overplus where prior P-starvation elevates PSR1 and on P-resupply causes luxury P-uptake. This is because the Class I genes, which include P-transporter genes, are not suppressed by the excess PO43-. Taken together, these discoveries facilitate a bio-circular approach of recycling nutrients from wastewater back to agriculture.https://www.frontiersin.org/articles/10.3389/fpls.2023.1208168/fullbiomassmicro-algaepolyphosphatetranscription factorwastewater remediation
spellingShingle Stephen P. Slocombe
Tatiana Zúñiga-Burgos
Tatiana Zúñiga-Burgos
Lili Chu
Payam Mehrshahi
Matthew P. Davey
Alison G. Smith
Miller Alonso Camargo-Valero
Miller Alonso Camargo-Valero
Alison Baker
Overexpression of PSR1 in Chlamydomonas reinhardtii induces luxury phosphorus uptake
Frontiers in Plant Science
biomass
micro-algae
polyphosphate
transcription factor
wastewater remediation
title Overexpression of PSR1 in Chlamydomonas reinhardtii induces luxury phosphorus uptake
title_full Overexpression of PSR1 in Chlamydomonas reinhardtii induces luxury phosphorus uptake
title_fullStr Overexpression of PSR1 in Chlamydomonas reinhardtii induces luxury phosphorus uptake
title_full_unstemmed Overexpression of PSR1 in Chlamydomonas reinhardtii induces luxury phosphorus uptake
title_short Overexpression of PSR1 in Chlamydomonas reinhardtii induces luxury phosphorus uptake
title_sort overexpression of psr1 in chlamydomonas reinhardtii induces luxury phosphorus uptake
topic biomass
micro-algae
polyphosphate
transcription factor
wastewater remediation
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1208168/full
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