Sticking together «...wie Pech und Schwefel»

A thread on Twitter

Hand on heart, what comes to your mind when you're asked for sulfur-containing compunds that play a role in biology? The amino acids cysteine and methionine, for sure, and maybe the methyl-group donor SAM (S-ade­no­syl methionine), vitamin biotin, the non-canonical base 4-thiouracil in tRNAs, and the iron-sulfur clusters that are at the heart of many enzymatic reactions. But Sulfo­qui­novose, in which car­bohydrate and sulfonic acid stick together like in the German proverb «...wie Pech und Schwefel» (Pech, tar; Schwefel, sulfur) ?

We came across a long thread on Twitter about this not so well known but quantitatively – for the biosphere – important com­pound. The author, Alexander Loy (@LoyTeam), professor at the De­partment of Microbiology and Ecosystem Science University of Vienna, Austria, kindly granted us permission to re-blog his contribution on these pages. Here it goes...
 

by Alexander Loy
 

Sulfoquinovose. Source. Frontispiece: mod­i­fied from original by @LoyTeam. Source

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Hey geomicrobiology and microbiome tweeps!
 
Do you know that the sulfosugar #sulfoquinovose (SQ) is a ubiquitous microbial nutrient in the en­vironment and in a vegetarian diet? No? Here comes some SQ propa­ganda… a thread...

 
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First, for #sulfoquinovose newbies, I very much re­com­mend the wonderful review by Ethan God­dard-Borger @ethangbaus & Spencer Williams @sjwill99.
 
Ref.: Sulfoquinovose in the biosphere: occurrence, meta­bolism and functions.
 

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#sulfoquinovose is a sulfonated glucose and most often found as polar head group of sulfoquinovosyl diacyl­gly­cerol (SQDG), a ubiquitous sulfolipid in the photosyn­thetic membranes of all green land plants, algae, dino­flagellates, and cyanobacteria.
 
 

Spinach. Source

 
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SQDG is one of the most abundant organic sulfur com­pounds in the biosphere (production rate of
100,000,000,000 tons per year!) and can represent up to a third of the total li­pids in leafy green vegetables.
 
#spinach #lettuce #green­o­nion
 
 
 

(Popeye borrowed from Amazon.de)

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SQDG #sulfoquinovose are abundant sources of carbon and sulfur in the global nutrient cycles and substrates for the gut microbiota of animals/humans that like their greens.
 
Think of popeye's diet #spinach as the ultimate #sulfo­quinovose boost for your gut microbiota.

 
 
 

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So how is all the #sulfo­quinovose in the environment and our guts degraded?
 
Thanks to the work of team @DSchleheck
 
three bacterial pathways for #sulfo­quinovose degrada­tion (sulfoglycolytic pathways) are currently known.
 

 
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1. pathway: E. coli and some other Enterobacteriaceae have the sulfo-EMP (Embden-Meyerhof-Parnas) pathway for #sulfo­quinovose breakdown and growth.
 
Note that the sulfo-EMP pathway is an additional, analogous path­way to the classical EMP pathway.
 
Ref.: Sulphoglycolysis in Escherichia coli K-12 closes a gap in the biogeochemical sulphur cycle
 

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2. pathway: Pseudomonas putida and some other Pro­teobacteria have the sulfo-ED pathway for #sulfo­qui­novose breakdown and growth.
 
Ref.: Entner–Doudoroff pathway for sulfoquinovose degradation in Pseudomonas putida SQ1
 

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3. pathway: The newly discovered SFT pathway is present in some aerobic and anaerobic Firmi­cu­tes and named after its characteristic sulfofructose transaldolase (SFT)
 
Ref.: Environmental and intestinal phylum Firmicutes bacteria metabolize the plant sugar sulfo­quinovose via...

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All three #sulfo­qui­novose pathways encode a sulfoqui­novosidase (an alpha-glucosidase in the glycoside hy­drolase family 31 - GH31) that cleaves SQ from SQ-gly­cosides such as sulfoquinovosyl diacyl­gly­cerol (SQDG).
 
Ref.: YihQ is a sulfo­quinovosidase that cleaves sulfo­quinovosyl diacylglyceride sulfolipids
 
 
 
 
 

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Aerobic and anaerobic glycolytic #sulfo­qui­novose (C6) degradation produces a classical C3-compound for growth – either pyruvate or dihydroxyacetone phosphate (DHAP) – and a C3-sulfonate that is excreted – either sul­folactate or dihydroxypropanesulfonate (DHPS).
 
 
 

 
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The #sulfo­qui­novose degradation products sulfolactate and dihydroxypropanesulfonate (DHPS) can be utilized by other microorganisms as carbon and/or sulfur sources and energy sources via intracellular production of sulfite (S oxidation state +4) = electron donor or acceptor.
 
Ref.: Anaerobic Degradation of the Plant Sugar Sulfoquinovose Concomitant With H2S Production...
 
 

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Sulfonates as DHPS are nutrients and energy sources for sulfur oxidizers in the pelagic ocean.
 
Check out work by the teams of Mary Ann Moran & @BryndanDurham for more info!
 
Ref: Sulfur metabolites in the pelagic ocean, Sulfonate-based networks between eukaryotic phytoplankton and heterotrophic bacteria...
 

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Green-diet-derived #sulfo­qui­novose is an exclusive growth substrate and thus a potential prebiotic of some abundant bacterial commensals in the human gut. Yet, complete degradation of SQ by cross-feeding of #DHPS produces #H₂S ...
 
Our new preprint: Sulfoquinovose is a select nutrient of prominent bacteria and a source of hydrogen sulfide

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Eubacterium rectale and Bilophila wadsworthia coope­ratively catabolize #sulfo­qui­novose to acetate and H₂S as main products in human fecal microcosms and in co-culture
 
Interspecies transfer of DHPS links a green diet with H₂S production in the gut.
 
 
 

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Eubacterium rectale ferments #sulfo­qui­novose to DHPS via the SFT pathway, which is exclusive to E. rectale and few other intestinal Firmicutes species such as Feacali­bacterium prausnitzii.
 
 
 

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Across the fecal metatranscriptomes of many individuals #sulfo­qui­novose degradation was expressed prevalently and abundantly (top 33% of all microbial pathways).
 
 
 
 

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and mostly by Eubacterium rectale and Feacalibacterium prausnitzii.
 
 

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Bilophila utilizes DHPS as electron acceptor via a new oxygen-sensitive glycyl-radical enzyme that releases sulfite from DHPS for anaerobic respiration to #H2S via the DsrABC pathway. The DHPS sulfite-lyase cleaves DHPS into hydroxyacetone and sulfite
 
Ref.: Sulfoquinovose is a select nutrient of prominent bacteria...
 
 
 

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In parallel, the DHPS sulfite-lyase was also discovered by the team of Yan Zhang, with additional biochemical and structural data.
 
Excitingly, they also describe a DHPS-dehydratase in bacteria that ferment DHPS without #H2S production.
 
Ref.: Two radical-dependent mechanisms for anaerobic degradation of the...
 
 

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In Bilophila and other bacteria, the DHPS sulfite-lyase is paralogous to isothionate sulfite-lyase, a key enzyme in anaerobic taurine degradation that was also discovered by the teams of @DSchleheck.
 
Ref.: A glycyl radical enzyme enables hydrogen sulfide production...
 
and Yan Zhang: Radical-mediated C-S bond cleavage in C2 sulfonate degradation by anaerobic bacteria
 
 

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metatranscriptome analysis of DsrABC-sulfite reduction and DHPS/isethionate sulfite-lyase activities suggested Bilophila and other Desulfovibrionaceae use mostly taurine but also DHPS for H₂S production in the human gut.
 
 
 

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Thanks for reading!
 
Keep in mind that #sulfo­qui­novose metabolism is a core physiological attribute of the human gut that is likely mo­difiable by diet – think of Popeye spinach – and contribu­tes to host health.
 
 
 
 

modified from original by @LoyTeam. Source

24_ADDENDUM
H₂S is a Janus-faced molecule with detrimental...
– toxic: Oxidation of hydrogen sulfide and methane...
– mucusbreaker: Gut microbiota facilitates dietary...
and beneficial effects: Hydrogen sulfide: an agent...
on the intestinal environment.
 

Suggested further reading: Sulfur Cycling and the Intestinal Microbiome.