Mannitol metabolism in brown algae involves a new phosphatase family

Agnès Groisillier; Zhanru Shao; Gurvan Michel; Sophie Goulitquer; Patricia Bonin; Stefan Krahulec; Bernd Nidetzky; Delin Duan; Catherine Boyen; Thierry Tonon

doi:10.1093/jxb/ert405

Mannitol metabolism in brown algae involves a new phosphatase family

Agnès Groisillier, Zhanru Shao, Gurvan Michel, Sophie Goulitquer, Patricia Bonin, Stefan Krahulec, Bernd Nidetzky, Delin Duan, Catherine Boyen, Thierry Tonon

CNAP

Research output: Contribution to journal › Article › peer-review

Abstract

Brown algae belong to a phylogenetic lineage distantly related to green plants and animals, and are found predominantly in the intertidal zone, a harsh and frequently changing environment. Because of their unique evolutionary history and of their habitat, brown algae feature several peculiarities in their metabolism. One of these is the mannitol cycle, which plays a central role in their physiology, as mannitol acts as carbon storage, osmoprotectant, and antioxidant. This polyol is derived directly from the photoassimilate fructose-6-phosphate via the action of a mannitol-1-phosphate dehydrogenase and a mannitol-1-phosphatase (M1Pase). Genome analysis of the brown algal model Ectocarpus siliculosus allowed identification of genes potentially involved in the mannitol cycle. Among these, two genes coding for haloacid dehalogenase (HAD)-like enzymes were suggested to correspond to M1Pase activity, and thus were named EsM1Pase1 and EsM1Pase2, respectively. To test this hypothesis, both genes were expressed in Escherichia coli. Recombinant EsM1Pase2 was shown to hydrolyse the phosphate group from mannitol-1-phosphate to produce mannitol but was not active on the hexose monophosphates tested. Gene expression analysis showed that transcription of both E. siliculosus genes was under the influence of the diurnal cycle. Sequence analysis and three-dimensional homology modelling indicated that EsM1Pases, and their orthologues in Prasinophytes, should be seen as founding members of a new family of phosphatase with original substrate specificity within the HAD superfamily of proteins. This is the first report describing the characterization of a gene encoding M1Pase activity in photosynthetic organisms.

Original language	English
Pages (from-to)	559-570
Number of pages	12
Journal	Journal of Experimental Botany
Volume	65
Issue number	2
Early online date	9 Dec 2013
DOIs	https://doi.org/10.1093/jxb/ert405
Publication status	Published - 1 Feb 2014

Keywords

Algal Proteins/chemistry
Amino Acid Sequence
Carbon/metabolism
Gene Expression Regulation, Plant
Light
Mannitol/metabolism
Models, Molecular
Molecular Sequence Data
Molecular Weight
Multigene Family
Phaeophyta/enzymology
Phosphoric Monoester Hydrolases/isolation & purification
Recombinant Proteins/metabolism
Sequence Alignment

Access to Document

10.1093/jxb/ert405

Cite this

@article{cb9901222f714c458d43f608a80850ff,

title = "Mannitol metabolism in brown algae involves a new phosphatase family",

abstract = "Brown algae belong to a phylogenetic lineage distantly related to green plants and animals, and are found predominantly in the intertidal zone, a harsh and frequently changing environment. Because of their unique evolutionary history and of their habitat, brown algae feature several peculiarities in their metabolism. One of these is the mannitol cycle, which plays a central role in their physiology, as mannitol acts as carbon storage, osmoprotectant, and antioxidant. This polyol is derived directly from the photoassimilate fructose-6-phosphate via the action of a mannitol-1-phosphate dehydrogenase and a mannitol-1-phosphatase (M1Pase). Genome analysis of the brown algal model Ectocarpus siliculosus allowed identification of genes potentially involved in the mannitol cycle. Among these, two genes coding for haloacid dehalogenase (HAD)-like enzymes were suggested to correspond to M1Pase activity, and thus were named EsM1Pase1 and EsM1Pase2, respectively. To test this hypothesis, both genes were expressed in Escherichia coli. Recombinant EsM1Pase2 was shown to hydrolyse the phosphate group from mannitol-1-phosphate to produce mannitol but was not active on the hexose monophosphates tested. Gene expression analysis showed that transcription of both E. siliculosus genes was under the influence of the diurnal cycle. Sequence analysis and three-dimensional homology modelling indicated that EsM1Pases, and their orthologues in Prasinophytes, should be seen as founding members of a new family of phosphatase with original substrate specificity within the HAD superfamily of proteins. This is the first report describing the characterization of a gene encoding M1Pase activity in photosynthetic organisms. ",

keywords = "Algal Proteins/chemistry, Amino Acid Sequence, Carbon/metabolism, Gene Expression Regulation, Plant, Light, Mannitol/metabolism, Models, Molecular, Molecular Sequence Data, Molecular Weight, Multigene Family, Phaeophyta/enzymology, Phosphoric Monoester Hydrolases/isolation & purification, Recombinant Proteins/metabolism, Sequence Alignment",

author = "Agn{\`e}s Groisillier and Zhanru Shao and Gurvan Michel and Sophie Goulitquer and Patricia Bonin and Stefan Krahulec and Bernd Nidetzky and Delin Duan and Catherine Boyen and Thierry Tonon",

year = "2014",

month = feb,

day = "1",

doi = "10.1093/jxb/ert405",

language = "English",

volume = "65",

pages = "559--570",

journal = "Journal of Experimental Botany",

issn = "0022-0957",

publisher = "Oxford University Press",

number = "2",

}

TY - JOUR

T1 - Mannitol metabolism in brown algae involves a new phosphatase family

AU - Groisillier, Agnès

AU - Shao, Zhanru

AU - Michel, Gurvan

AU - Goulitquer, Sophie

AU - Bonin, Patricia

AU - Krahulec, Stefan

AU - Nidetzky, Bernd

AU - Duan, Delin

AU - Boyen, Catherine

AU - Tonon, Thierry

PY - 2014/2/1

Y1 - 2014/2/1

N2 - Brown algae belong to a phylogenetic lineage distantly related to green plants and animals, and are found predominantly in the intertidal zone, a harsh and frequently changing environment. Because of their unique evolutionary history and of their habitat, brown algae feature several peculiarities in their metabolism. One of these is the mannitol cycle, which plays a central role in their physiology, as mannitol acts as carbon storage, osmoprotectant, and antioxidant. This polyol is derived directly from the photoassimilate fructose-6-phosphate via the action of a mannitol-1-phosphate dehydrogenase and a mannitol-1-phosphatase (M1Pase). Genome analysis of the brown algal model Ectocarpus siliculosus allowed identification of genes potentially involved in the mannitol cycle. Among these, two genes coding for haloacid dehalogenase (HAD)-like enzymes were suggested to correspond to M1Pase activity, and thus were named EsM1Pase1 and EsM1Pase2, respectively. To test this hypothesis, both genes were expressed in Escherichia coli. Recombinant EsM1Pase2 was shown to hydrolyse the phosphate group from mannitol-1-phosphate to produce mannitol but was not active on the hexose monophosphates tested. Gene expression analysis showed that transcription of both E. siliculosus genes was under the influence of the diurnal cycle. Sequence analysis and three-dimensional homology modelling indicated that EsM1Pases, and their orthologues in Prasinophytes, should be seen as founding members of a new family of phosphatase with original substrate specificity within the HAD superfamily of proteins. This is the first report describing the characterization of a gene encoding M1Pase activity in photosynthetic organisms.

AB - Brown algae belong to a phylogenetic lineage distantly related to green plants and animals, and are found predominantly in the intertidal zone, a harsh and frequently changing environment. Because of their unique evolutionary history and of their habitat, brown algae feature several peculiarities in their metabolism. One of these is the mannitol cycle, which plays a central role in their physiology, as mannitol acts as carbon storage, osmoprotectant, and antioxidant. This polyol is derived directly from the photoassimilate fructose-6-phosphate via the action of a mannitol-1-phosphate dehydrogenase and a mannitol-1-phosphatase (M1Pase). Genome analysis of the brown algal model Ectocarpus siliculosus allowed identification of genes potentially involved in the mannitol cycle. Among these, two genes coding for haloacid dehalogenase (HAD)-like enzymes were suggested to correspond to M1Pase activity, and thus were named EsM1Pase1 and EsM1Pase2, respectively. To test this hypothesis, both genes were expressed in Escherichia coli. Recombinant EsM1Pase2 was shown to hydrolyse the phosphate group from mannitol-1-phosphate to produce mannitol but was not active on the hexose monophosphates tested. Gene expression analysis showed that transcription of both E. siliculosus genes was under the influence of the diurnal cycle. Sequence analysis and three-dimensional homology modelling indicated that EsM1Pases, and their orthologues in Prasinophytes, should be seen as founding members of a new family of phosphatase with original substrate specificity within the HAD superfamily of proteins. This is the first report describing the characterization of a gene encoding M1Pase activity in photosynthetic organisms.

KW - Algal Proteins/chemistry

KW - Amino Acid Sequence

KW - Carbon/metabolism

KW - Gene Expression Regulation, Plant

KW - Light

KW - Mannitol/metabolism

KW - Models, Molecular

KW - Molecular Sequence Data

KW - Molecular Weight

KW - Multigene Family

KW - Phaeophyta/enzymology

KW - Phosphoric Monoester Hydrolases/isolation & purification

KW - Recombinant Proteins/metabolism

KW - Sequence Alignment

U2 - 10.1093/jxb/ert405

DO - 10.1093/jxb/ert405

M3 - Article

C2 - 24323504

SN - 0022-0957

VL - 65

SP - 559

EP - 570

JO - Journal of Experimental Botany

JF - Journal of Experimental Botany

IS - 2

ER -