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
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...
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.
#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.
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
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.
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.
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
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
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...
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
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).
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...
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...
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
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.
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.
Across the fecal metatranscriptomes of many individuals #sulfoquinovose degradation was expressed prevalently and abundantly (top 33% of all microbial pathways).
and mostly by Eubacterium rectale and Feacalibacterium prausnitzii.
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...
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...
In Bilophila and other bacteria, the DHPS sulfite-lyase is paralogous to isethionate 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
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.
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.
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.