Analyzing sorbitol biosynthesis using a metabolic network flux model of a lichenized strain of the green microalga Diplosphaera chodatii

ABSTRACT Diplosphaera chodatii, a unicellular terrestrial microalga found either free-living or in association with lichenized fungi, protects itself from desiccation by synthesizing and accumulating low-molecular-weight carbohydrates such as sorbitol. The metabolism of this algal species and the in...

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Main Authors: Hadi Nazem-Bokaee, Erik F. Y. Hom, Sarah Mathews, Cécile Gueidan
Format: Article
Language:English
Published: American Society for Microbiology 2025-01-01
Series:Microbiology Spectrum
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Online Access:https://journals.asm.org/doi/10.1128/spectrum.03660-23
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author Hadi Nazem-Bokaee
Erik F. Y. Hom
Sarah Mathews
Cécile Gueidan
author_facet Hadi Nazem-Bokaee
Erik F. Y. Hom
Sarah Mathews
Cécile Gueidan
author_sort Hadi Nazem-Bokaee
collection DOAJ
description ABSTRACT Diplosphaera chodatii, a unicellular terrestrial microalga found either free-living or in association with lichenized fungi, protects itself from desiccation by synthesizing and accumulating low-molecular-weight carbohydrates such as sorbitol. The metabolism of this algal species and the interplay of sorbitol biosynthesis with its growth, light absorption, and carbon dioxide fixation are poorly understood. Here, we used a recently available genome assembly for D. chodatii to develop a metabolic flux model and analyze the alga’s metabolic capabilities, particularly, for sorbitol biosynthesis. The model contains 151 genes, 155 metabolites, and 194 unique metabolic reactions participating in 12 core metabolic pathways and five compartments. Both photoautotrophic and mixotrophic growths of D. chodatii were supported by the metabolic model. In the presence of glucose, mixotrophy led to higher biomass and sorbitol yields. Additionally, the model predicted increased starch biosynthesis at high light intensities during photoautotrophic growth, an indication that the “overflow hypothesis—stress-driven metabolic flux redistribution” could be applied to D. chodatii. Furthermore, the newly developed metabolic model of D. chodatii, iDco_core, captures both linear and cyclic electron flow schemes characterized in photosynthetic microorganisms and suggests a possible adaptation to fluctuating water availability during periods of desiccation. This work provides important new insights into the predicted metabolic capabilities of D. chodatii, including a potential biotechnological opportunity for industrial sorbitol biosynthesis.IMPORTANCELichenized green microalgae are vital components for the survival and growth of lichens in extreme environmental conditions. However, little is known about the metabolism and growth characteristics of these algae as individual microbes. This study aims to provide insights into some of the metabolic capabilities of Diplosphaera chodatii, a lichenized green microalgae, using a recently assembled and annotated genome of the alga. For that, a metabolic flux model was developed simulating the metabolism of this algal species and allowing for studying the algal growth, light absorption, and carbon dioxide fixation during both photoautotrophic and mixotrophic growth, in silico. An important capability of the new metabolic model of D. chodatii is capturing both linear and cyclic electron flow mechanisms characterized in several other microalgae. Moreover, the model predicts limits of the metabolic interplay between sorbitol biosynthesis and algal growth, which has potential applications in assisting the design of bio-based sorbitol production processes.
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spelling doaj-art-bb6fe378dd394c8195382cf9b73e80612025-01-07T14:05:18ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972025-01-0113110.1128/spectrum.03660-23Analyzing sorbitol biosynthesis using a metabolic network flux model of a lichenized strain of the green microalga Diplosphaera chodatiiHadi Nazem-Bokaee0Erik F. Y. Hom1Sarah Mathews2Cécile Gueidan3Australian National Herbarium, National Research Collections Australia, NCMI, CSIRO, Canberra, AustraliaDepartment of Biology and Center for Biodiversity and Conservation Research, The University of Mississippi, University, Mississippi, USAAustralian National Herbarium, National Research Collections Australia, NCMI, CSIRO, Canberra, AustraliaAustralian National Herbarium, National Research Collections Australia, NCMI, CSIRO, Canberra, AustraliaABSTRACT Diplosphaera chodatii, a unicellular terrestrial microalga found either free-living or in association with lichenized fungi, protects itself from desiccation by synthesizing and accumulating low-molecular-weight carbohydrates such as sorbitol. The metabolism of this algal species and the interplay of sorbitol biosynthesis with its growth, light absorption, and carbon dioxide fixation are poorly understood. Here, we used a recently available genome assembly for D. chodatii to develop a metabolic flux model and analyze the alga’s metabolic capabilities, particularly, for sorbitol biosynthesis. The model contains 151 genes, 155 metabolites, and 194 unique metabolic reactions participating in 12 core metabolic pathways and five compartments. Both photoautotrophic and mixotrophic growths of D. chodatii were supported by the metabolic model. In the presence of glucose, mixotrophy led to higher biomass and sorbitol yields. Additionally, the model predicted increased starch biosynthesis at high light intensities during photoautotrophic growth, an indication that the “overflow hypothesis—stress-driven metabolic flux redistribution” could be applied to D. chodatii. Furthermore, the newly developed metabolic model of D. chodatii, iDco_core, captures both linear and cyclic electron flow schemes characterized in photosynthetic microorganisms and suggests a possible adaptation to fluctuating water availability during periods of desiccation. This work provides important new insights into the predicted metabolic capabilities of D. chodatii, including a potential biotechnological opportunity for industrial sorbitol biosynthesis.IMPORTANCELichenized green microalgae are vital components for the survival and growth of lichens in extreme environmental conditions. However, little is known about the metabolism and growth characteristics of these algae as individual microbes. This study aims to provide insights into some of the metabolic capabilities of Diplosphaera chodatii, a lichenized green microalgae, using a recently assembled and annotated genome of the alga. For that, a metabolic flux model was developed simulating the metabolism of this algal species and allowing for studying the algal growth, light absorption, and carbon dioxide fixation during both photoautotrophic and mixotrophic growth, in silico. An important capability of the new metabolic model of D. chodatii is capturing both linear and cyclic electron flow mechanisms characterized in several other microalgae. Moreover, the model predicts limits of the metabolic interplay between sorbitol biosynthesis and algal growth, which has potential applications in assisting the design of bio-based sorbitol production processes.https://journals.asm.org/doi/10.1128/spectrum.03660-23microalgaesystems biologymetabolic network modelingsorbitolsymbiosis
spellingShingle Hadi Nazem-Bokaee
Erik F. Y. Hom
Sarah Mathews
Cécile Gueidan
Analyzing sorbitol biosynthesis using a metabolic network flux model of a lichenized strain of the green microalga Diplosphaera chodatii
Microbiology Spectrum
microalgae
systems biology
metabolic network modeling
sorbitol
symbiosis
title Analyzing sorbitol biosynthesis using a metabolic network flux model of a lichenized strain of the green microalga Diplosphaera chodatii
title_full Analyzing sorbitol biosynthesis using a metabolic network flux model of a lichenized strain of the green microalga Diplosphaera chodatii
title_fullStr Analyzing sorbitol biosynthesis using a metabolic network flux model of a lichenized strain of the green microalga Diplosphaera chodatii
title_full_unstemmed Analyzing sorbitol biosynthesis using a metabolic network flux model of a lichenized strain of the green microalga Diplosphaera chodatii
title_short Analyzing sorbitol biosynthesis using a metabolic network flux model of a lichenized strain of the green microalga Diplosphaera chodatii
title_sort analyzing sorbitol biosynthesis using a metabolic network flux model of a lichenized strain of the green microalga diplosphaera chodatii
topic microalgae
systems biology
metabolic network modeling
sorbitol
symbiosis
url https://journals.asm.org/doi/10.1128/spectrum.03660-23
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