Challenges in Enzymatic Route of Mannitol Production

b Leaf-cutter ants use plant matter to culture the obligate mutualistic basidiomycete Leucoagaricus gongylophorus. This fungus mediates ant nutrition on plant resources. Furthermore, other microbes living in the fungus garden might also contribute to plant digestion. The fungus garden comprises a young sector with recently incorporated leaf fragments and an old sector with partially digested plant matter. Here, we show that the young and old sectors of the grass-cutter Atta bisphaerica fungus garden operate as a biphasic solid-state mixed fermenting system. An initial plant digestion phase occurred in the young sector in the fungus garden periphery, with prevailing hemicellulose and starch degradation into arabinose, mannose, xylose, and glucose. These products support fast microbial growth but were mostly converted into four polyols. Three polyols, mannitol, arabitol, and inositol, were secreted by L. gongylophorus, and a fourth polyol, sorbitol, was likely secreted by another, unidentified, microbe. A second plant digestion phase occurred in the old sector, located in the fungus garden core, comprising stocks of microbial biomass growing slowly on monosaccharides and polyols. This biphasic operation was efficient in mediating symbiotic nutrition on plant matter: the microbes, accounting for 4% of the fungus garden biomass, converted plant matter biomass into monosaccharides and polyols, which were completely consumed by the resident ants and microbes. However, when consumption was inhibited through laboratory manipulation, most of the plant polysaccharides were degraded, products rapidly accumulated, and yields could be preferentially switched between polyols and monosaccharides. This feature might be useful in biotechnology. In the nests of leaf-cutter ants of the genera Atta and Acromyrmex, gardens of the obligate mutualistic basidiomycete fungus Leucoagaricus gongylophorus (1, 2) are cultivated on fresh vegetal materials (3-5). Although few leaf-cutter species prefer monocots, most leaf-cutter ants collect plant materials from both monocots and dicots (6). The ants collect and transport these plants to their nests and then fractionate and extensively clean the leaf fragments (7,8). Subsequently, the ants deposit a drop of fecal fluid onto the leaf fragment surface and inoculate the leaf fragment with L. gongylophorus hyphae. The plant-digesting enzymes in the fecal fluid facilitate fungal development (9). This fungus produces swollen hyphal tips, called gongylidia, that cluster together to form macroscopic structures known as staphylae, which are food sources for the ants (3-5). L. gongylophorus also secretes enzymes that act synergistically with ant enzymes to degrade plant matter, generating soluble compounds that are subsequently ingested by the ants (10-13). These enzymes attack plant polysaccharides, including starch, hemicellulose, pectin, and, to a lesser extent, cellulose (10,(14)(15)(16)(17)(18)(19)(20)(21)(22)(23). In addition, other microbes living in the fungus garden might mediate ant nutrition...

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“…1). Moreover, the major polyols produced from the fungus garden, mannitol and arabitol, are valuable products in the market (67,68).…”

Section: Discussionmentioning

confidence: 99%

Leaf-Cutter Ant Fungus Gardens Are Biphasic Mixed Microbial Bioreactors That Convert Plant Biomass to Polyols with Biotechnological Applications

Somera

Lima

Santos-Neto

et al. 2015

Appl Environ Microbiol

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“…Mannitol is a type of naturally occurring hexabasic alcohol that is widely used in the fields of food, medicine, chemical industry, and among others . Mannitol was traditionally produced from kelps, but this process was gradually eliminated because it consumed too much water and energy .…”

Section: Introductionmentioning

confidence: 99%

Microbial production of mannitol by Lactobacillus brevis 3‐A5 from concentrated extract of Jerusalem artichoke tubers

Cao

Yue

Liu

et al. 2017

Biotech and App Biochem

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In the present study, the conversion of the extract of Jerusalem artichoke tubers for mannitol production by Lactobacillus brevis 3-A5 was investigated. When the bacterium utilized enzymatic hydrolysates of Jerusalem artichoke extract as the main substrates in batch fermentation, the significant decrease in mannitol productivity was observed when the initial concentration of reducing sugar increased. Then, a strategy of continuous fed-batch fermentation was adopted for improving mannitol production with enzymatic hydrolysates of Jerusalem artichoke extract as main substrates. Although the concentration of mannitol could reach 199.86 g/L at the end of the fermentation, the productivity for the overall process of the fermentation was only 1.67 g/L/H. To improve the mannitol productivity with both higher yield and concentration, the simultaneous enzymatic saccharification and fermentation (SSF) was studied. In SSF, the mannitol production reached 176.50 g/L in 28 H with a productivity of 6.30 g/L/H and a yield of 0.68 g/g total sugar. Our study provides a cost-effective and eco-friendly method for mannitol production from a cheap biomass.

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“…Mannitol has also several applications in the food, pharmaceutical, medical, and chemical industries (Saha and Racine, 2011). Currently, most commercial production is achieved by the chemical hydrogenation of a mixture of glucose and fructose, leading to the formation of mannitol and sorbitol, which are then separated by selective crystallization (Saha and Racine, 2011;Bhatt et al, 2013). However, because of problems associated with chemical production, coupled with an increasing demand for natural products, the microbial production of mannitol has been the subject of significant interest in recent years (Saha and Racine, 2011).…”

Section: Introductionmentioning

confidence: 99%

Molecular and biochemical characterization of mannitol-1-phosphate dehydrogenase from the model brown alga Ectocarpus sp.

et al. 2015

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The sugar alcohol mannitol is important in the food, pharmaceutical, medical and chemical industries. It is one of the most commonly occurring polyols in nature, with the exception of Archaea and animals. It has a range of physiological roles, including as carbon storage, compatible solute, and osmolyte. Mannitol is present in large amounts in brown algae, where its synthesis involved two steps: a mannitol-1-phosphate dehydrogenase (M1PDH) catalyzes a reversible reaction between fructose-6-phosphate (F6P) and mannitol-1-phosphate (M1P) (EC 1.1.1.17), and a mannitol-1-phosphatase hydrolyzes M1P to mannitol (EC 3.1.3.22). Analysis of the model brown alga Ectocarpus sp. genome provided three candidate genes for M1PDH activities. We report here the sequence analysis of Ectocarpus M1PDHs (EsM1PDHs), and the biochemical characterization of the recombinant catalytic domain of EsM1PDH1 (EsM1PDH1cat). Ectocarpus M1PDHs are representatives of a new type of modular M1PDHs among the polyol-specific long-chain dehydrogenases/reductases (PSLDRs). The N-terminal domain of EsM1PDH1 was not necessary for enzymatic activity. Determination of kinetic parameters indicated that EsM1PDH1cat displayed higher catalytic efficiency for F6P reduction compared to M1P oxidation. Both activities were influenced by NaCl concentration and inhibited by the thioreactive compound pHMB. These observations were completed by measurement of endogenous M1PDH activity and of EsM1PDH gene expression during one diurnal cycle. No significant changes in enzyme activity were monitored between day and night, although transcription of two out of three genes was altered, suggesting different levels of regulation for this key metabolic pathway in brown algal physiology.

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Challenges in Enzymatic Route of Mannitol Production

Cited by 30 publications

References 62 publications

Leaf-Cutter Ant Fungus Gardens Are Biphasic Mixed Microbial Bioreactors That Convert Plant Biomass to Polyols with Biotechnological Applications

Leaf-Cutter Ant Fungus Gardens Are Biphasic Mixed Microbial Bioreactors That Convert Plant Biomass to Polyols with Biotechnological Applications

Microbial production of mannitol by Lactobacillus brevis 3‐A5 from concentrated extract of Jerusalem artichoke tubers

Molecular and biochemical characterization of mannitol-1-phosphate dehydrogenase from the model brown alga Ectocarpus sp.

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