Sulfoglycolysis

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Sulfoglycolysis is a catabolic process in primary metabolism in which sulfoquinovose (6-deoxy-6-sulfonato-glucose) is metabolized to produce energy and carbon-building blocks. [1] [2] Sulfoglycolysis pathways occur in a wide variety of organisms, and enable key steps in the degradation of sulfoquinovosyl diacylglycerol (SQDG), a sulfolipid found in plants and cyanobacteria into sulfite and sulfate. Sulfoglycolysis converts sulfoquinovose (C6H12O8S−) into various smaller metabolizable carbon fragments such as pyruvate and dihydroxyacetone phosphate that enter central metabolism. The free energy is used to form the high-energy molecules ATP (adenosine triphosphate) and NADH (reduced nicotinamide adenine dinucleotide). Unlike glycolysis, which allows metabolism of all carbons in glucose, sulfoglycolysis pathways convert only a fraction of the carbon content of sulfoquinovose into smaller metabolizable fragments; the remainder is excreted as C3-sulfonates 2,3-dihydroxypropanesulfonate (DHPS) or sulfolactate (SL); or C2-sulfonates isethionate or sulfoacetate.

Contents

Several sulfoglycolytic pathways are known:

Additionally, there are sulfoquinovose 'sulfolytic' pathways that allow degradation of sulfoquinovose through cleavage of the C-S bond. These include:

In all pathways, energy is formed by breakdown of the carbon-rich fragments in later stages through the 'pay-off' phase of glycolysis through substrate-level phosphorylation to produce ATP and NADH.

Growth of bacteria on sulfoquinovose and its glycosides

A range of bacteria can grow on sulfoquinovose or its glycosides as sole carbon source. E. coli can grow on sulfoquinovose, [3] methyl α-sulfoquinovoside and α-sulfoquinovosyl glycerol. [10] Growth on sulfoquinovosyl glycerol is both faster and leads to higher cell density than for growth on sulfoquinovose. [10] Pseudomonas aeruginosa strain SQ1, [11] Klebsiella sp. strain ABR11, [12] Klebsiella oxytoca TauN1, [11] Agrobacterium sp. strain ABR2, [12] and Bacillus aryabhattai [5] can grow on sulfoquinovose as sole carbon source. A strain of Flavobacterium was identified that could grow on methyl α-sulfoquinovoside. [13]

Production of sulfoquinovose and its mutarotation

Formation of sulfoquinovose from sulfoquinovosyl diacylglycerol (SQDG). SQDG-to-SQ.gif
Formation of sulfoquinovose from sulfoquinovosyl diacylglycerol (SQDG).

Sulfoquinovose is rarely found in its free form in nature; rather it occurs predominantly as a glycoside, SQDG. SQDG can be deacylated to form lyso-SQDG and sulfoquinovosylglycerol (SQGro). [14] [15] [16] Sulfoquinovose is obtained from SQ glycosides by the action of sulfoquinovosidases, which are glycoside hydrolases that can hydrolyse the glycosidic linkage in SQDG, or its deacylated form, sulfoquinovosyl glycerol (SQGro) [17] .

There are two main classes of sulfoquinovosidases. The first are classical glycoside hydrolases (which belong to CAZy family GH31), and is exemplified by the sulfoquinovosidase YihQ from Escherichia coli. Family GH31 sulfoquinovosidases cleave SQ glycosides with retention of configuration, initially forming α-sulfoquinovose. YihQ sulfoquinovosidase exhibits a preference for the naturally occurring 2’R-SQGro. [10] The second class of sulfoquinovosidases are NAD+-dependent enzymes (which belong to CAZy family GH188) that use an oxidoreductive mechanism to cleave both α- and β-glycosides of sulfoquinovose [18] .

Sulfoglycolysis encoding operons often contain gene sequences encoding aldose-1-epimerases that act as sulfoquinovose mutarotases, catalyzing the interconversion of the α and β anomers of sulfoquinovose. [19]

Sulfo-EMP pathway

The sulfoglycolytic Embden-Meyerhof-Parnas pathway. Sulfo-EMP.gif
The sulfoglycolytic Embden-Meyerhof-Parnas pathway.

The major steps in the sulfo-EMP pathway [3] are:

Expression of proteins within the sulfo-EMP operon of E. coli is regulated by a transcription factor termed CsqR (formerly YihW). [22] CsqR binds to DNA sites within the operon encoding the sulfo-EMP pathway, functioning as a repressor. SQ, SQGro and the transiently formed intermediate sulforhamnose (but not lactose, glucose or galactose) function as derepressors of CsqR. [20]

Sulfo-ED pathway

The sulfoglycolytic Entner-Douderoff pathway. Sulfo-ED.gif
The sulfoglycolytic Entner-Douderoff pathway.

The major steps in the sulfo-ED pathway [4] are:

Sulfo-SFT pathway

The sulfoglycolytic sulfofructose transaldolase pathway. SFT pathway.gif
The sulfoglycolytic sulfofructose transaldolase pathway.

The major steps in the sulfo-SFT pathway [5] are:

The transaldolase can also catalyze transfer of the C3-(glycerone)-moiety to erythrose-4-phosphate, giving sedoheptulose-7-phosphate.

Sulfo-TK pathway

The major steps in the Sulfo-TK pathway [23] are:

The sulfoacetaldehyde may be oxidized to sulfoacetate.

Degradation of DHPS and SL

The C3 sulfonates DHPS and SL are metabolized for their carbon content, as well as to mineralize their sulfur content. [2] Metabolism of DHPS typically involves conversion to SL. Metabolism of SL can occur in several ways including:

See also

Related Research Articles

<span class="mw-page-title-main">Glycolysis</span> Series of interconnected biochemical reactions

Glycolysis is the metabolic pathway that converts glucose into pyruvate, and in most organisms, occurs in the liquid part of cells, the cytosol. The free energy released in this process is used to form the high-energy molecules adenosine triphosphate (ATP) and reduced nicotinamide adenine dinucleotide (NADH). Glycolysis is a sequence of ten reactions catalyzed by enzymes.

<span class="mw-page-title-main">Phosphorylation</span> Chemical process of introducing a phosphate

In biochemistry, phosphorylation is the attachment of a phosphate group to a molecule or an ion. This process and its inverse, dephosphorylation, are common in biology. Protein phosphorylation often activates many enzymes.

Carbohydrate metabolism is the whole of the biochemical processes responsible for the metabolic formation, breakdown, and interconversion of carbohydrates in living organisms.

<span class="mw-page-title-main">Nicotinamide adenine dinucleotide phosphate</span> Chemical compound

Nicotinamide adenine dinucleotide phosphate, abbreviated NADP+ or, in older notation, TPN (triphosphopyridine nucleotide), is a cofactor used in anabolic reactions, such as the Calvin cycle and lipid and nucleic acid syntheses, which require NADPH as a reducing agent ('hydrogen source'). NADPH is the reduced form, whereas NADP+ is the oxidized form. NADP+ is used by all forms of cellular life.

<span class="mw-page-title-main">Aldolase A</span> Mammalian protein found in Homo sapiens

Aldolase A, also known as fructose-bisphosphate aldolase, is an enzyme that in humans is encoded by the ALDOA gene on chromosome 16.

Sulfoquinovosyl diacylglycerols, abbreviated SQDG, are a class of sulfur-containing but phosphorus-free lipids (sulfolipids) found in many photosynthetic organisms.

<span class="mw-page-title-main">Triosephosphate isomerase</span> Enzyme involved in glycolysis

Triose-phosphate isomerase is an enzyme that catalyzes the reversible interconversion of the triose phosphate isomers dihydroxyacetone phosphate and D-glyceraldehyde 3-phosphate.

<span class="mw-page-title-main">Transketolase</span> Enzyme involved in metabolic pathways

Transketolase is an enzyme that, in humans, is encoded by the TKT gene. It participates in both the pentose phosphate pathway in all organisms and the Calvin cycle of photosynthesis. Transketolase catalyzes two important reactions, which operate in opposite directions in these two pathways. In the first reaction of the non-oxidative pentose phosphate pathway, the cofactor thiamine diphosphate accepts a 2-carbon fragment from a 5-carbon ketose (D-xylulose-5-P), then transfers this fragment to a 5-carbon aldose (D-ribose-5-P) to form a 7-carbon ketose (sedoheptulose-7-P). The abstraction of two carbons from D-xylulose-5-P yields the 3-carbon aldose glyceraldehyde-3-P. In the Calvin cycle, transketolase catalyzes the reverse reaction, the conversion of sedoheptulose-7-P and glyceraldehyde-3-P to pentoses, the aldose D-ribose-5-P and the ketose D-xylulose-5-P.

<span class="mw-page-title-main">Glyceraldehyde 3-phosphate dehydrogenase</span> Enzyme of the glycolysis metabolic pathway

Glyceraldehyde 3-phosphate dehydrogenase is an enzyme of about 37kDa that catalyzes the sixth step of glycolysis and thus serves to break down glucose for energy and carbon molecules. In addition to this long established metabolic function, GAPDH has recently been implicated in several non-metabolic processes, including transcription activation, initiation of apoptosis, ER to Golgi vesicle shuttling, and fast axonal, or axoplasmic transport. In sperm, a testis-specific isoenzyme GAPDHS is expressed.

<span class="mw-page-title-main">Aldolase B</span> Mammalian protein found in Homo sapiens

Aldolase B also known as fructose-bisphosphate aldolase B or liver-type aldolase is one of three isoenzymes of the class I fructose 1,6-bisphosphate aldolase enzyme, and plays a key role in both glycolysis and gluconeogenesis. The generic fructose 1,6-bisphosphate aldolase enzyme catalyzes the reversible cleavage of fructose 1,6-bisphosphate (FBP) into glyceraldehyde 3-phosphate and dihydroxyacetone phosphate (DHAP) as well as the reversible cleavage of fructose 1-phosphate (F1P) into glyceraldehyde and dihydroxyacetone phosphate. In mammals, aldolase B is preferentially expressed in the liver, while aldolase A is expressed in muscle and erythrocytes and aldolase C is expressed in the brain. Slight differences in isozyme structure result in different activities for the two substrate molecules: FBP and fructose 1-phosphate. Aldolase B exhibits no preference and thus catalyzes both reactions, while aldolases A and C prefer FBP.

<span class="mw-page-title-main">Ribose 5-phosphate</span> Chemical compound

Ribose 5-phosphate (R5P) is both a product and an intermediate of the pentose phosphate pathway. The last step of the oxidative reactions in the pentose phosphate pathway is the production of ribulose 5-phosphate. Depending on the body's state, ribulose 5-phosphate can reversibly isomerize to ribose 5-phosphate. Ribulose 5-phosphate can alternatively undergo a series of isomerizations as well as transaldolations and transketolations that result in the production of other pentose phosphates as well as fructose 6-phosphate and glyceraldehyde 3-phosphate.

<span class="mw-page-title-main">Fructose-bisphosphate aldolase</span>

Fructose-bisphosphate aldolase, often just aldolase, is an enzyme catalyzing a reversible reaction that splits the aldol, fructose 1,6-bisphosphate, into the triose phosphates dihydroxyacetone phosphate (DHAP) and glyceraldehyde 3-phosphate (G3P). Aldolase can also produce DHAP from other (3S,4R)-ketose 1-phosphates such as fructose 1-phosphate and sedoheptulose 1,7-bisphosphate. Gluconeogenesis and the Calvin cycle, which are anabolic pathways, use the reverse reaction. Glycolysis, a catabolic pathway, uses the forward reaction. Aldolase is divided into two classes by mechanism.

<span class="mw-page-title-main">Sucrose phosphorylase</span>

Sucrose phosphorylase is an important enzyme in the metabolism of sucrose and regulation of other metabolic intermediates. Sucrose phosphorylase is in the class of hexosyltransferases. More specifically it has been placed in the retaining glycoside hydrolases family although it catalyzes a transglycosidation rather than hydrolysis. Sucrose phosphorylase catalyzes the conversion of sucrose to D-fructose and α-D-glucose-1-phosphate. It has been shown in multiple experiments that the enzyme catalyzes this conversion by a double displacement mechanism.

The enzyme phosphosulfolactate synthase catalyzes the reaction

UDP-sulfoquinovose synthase (EC 3.13.1.1) is an enzyme that catalyzes the chemical reaction

In enzymology, a 1-deoxy-d-xylulose-5-phosphate synthase (EC 2.2.1.7) is an enzyme in the non-mevalonate pathway that catalyzes the chemical reaction

In enzymology, a formaldehyde transketolase is an enzyme that catalyzes the chemical reaction

Fructolysis refers to the metabolism of fructose from dietary sources. Though the metabolism of glucose through glycolysis uses many of the same enzymes and intermediate structures as those in fructolysis, the two sugars have very different metabolic fates in human metabolism. Unlike glucose, which is directly metabolized widely in the body, fructose is almost entirely metabolized in the liver in humans, where it is directed toward replenishment of liver glycogen and triglyceride synthesis. Under one percent of ingested fructose is directly converted to plasma triglyceride. 29% - 54% of fructose is converted in liver to glucose, and about a quarter of fructose is converted to lactate. 15% - 18% is converted to glycogen. Glucose and lactate are then used normally as energy to fuel cells all over the body.

<span class="mw-page-title-main">Cysteic acid</span> Chemical compound

Cysteic acid also known as 3-sulfo-l-alanine is the organic compound with the formula HO3SCH2CH(NH2)CO2H. It is often referred to as cysteate, which near neutral pH takes the form −O3SCH2CH(NH3+)CO2−.

<span class="mw-page-title-main">Sulfoquinovose</span> Chemical compound

Sulfoquinovose, also known as 6-sulfoquinovose and 6-deoxy-6-sulfo-D-glucopyranose, is a monosaccharide sugar that is found as a building block in the sulfolipid sulfoquinovosyl diacylglycerol (SQDG). Sulfoquinovose is a sulfonic acid derivative of glucose, the sulfonic acid group is introduced into the sugar by the enzyme UDP-sulfoquinovose synthase (SQD1). Sulfoquinovose is degraded through a metabolic process termed sulfoglycolysis. The half-life for mutarotation of sulfoquinovose at pD 7.5 and 26C is 299 minutes.

References

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  18. ↑ Kaur, Arashdeep; Pickles, Isabelle B.; Sharma, Mahima; Madeido Soler, Niccolay; Scott, Nichollas E.; Pidot, Sacha J.; Goddard-Borger, Ethan D.; Davies, Gideon J.; Williams, Spencer J. (27 December 2023). "Widespread Family of NAD + -Dependent Sulfoquinovosidases at the Gateway to Sulfoquinovose Catabolism". Journal of the American Chemical Society. 145 (51): 28216–28223. doi: 10.1021/jacs.3c11126 . PMC   10755693 .
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