Found: The little surprise in leafy greens

A pungent odour wafts through the classroom, eliciting giggles from all the kids: someone has farted and boy, can you tell.

Who had too many brussels sprouts for dinner?

That distinctive ‘fart’ odour is actually a chemical called hydrogen sulfide, or H2S – one of the more familiar forms of sulfur that we encounter in our everyday life. It’s the smell we associate with rotten eggs, pongy toilets, volcanic springs and pungent swamps: the stench of decay.

Professor Spencer Williams, from the University of Melbourne’s School of Chemistry and Bio21 Institute and Dr Ethan Goddard-Borger, from the Walter and Eliza Hall Institute, are keenly interested in sulfur.

In particular, they want to know how sulfur-containing molecules are broken down by bacteria in our gut and other organisms in our environment.

As part of an international collaboration that includes University of Melbourne PhD student Gaetano Speciale, they have discovered how the E. coli bacteria that live in our gut ‘feeds’ on green vegetables.

More precisely, they have discovered an enzyme that allows the bacteria to break down a sulfur-containing sugar called ‘sulfoquinovose’ (or ‘SQ’ for short) that is present in brussels sprouts, spinach and other leafy green vegetables.

The newly discovered enzyme, called ‘YihQ’, is the missing piece in a 50-year-old puzzle in our understanding of the immensely important biochemical sulfur cycle.

Sulfur on your veggies

Professor Williams first came across the sulfur cycle while growing up in the Western Australian town of Albany and helping his dad in the family nursery business.

His dad explained that the standard fertilisers - labelled N-P-K for nitrogen, phosphorus and potassium – were missing a key ingredient.

That missing element was sulfur.

Nowadays, most fertilisers contain sulfur and are thus labelled N-P-K-S (the S is for sulfur). They contain a mix of these four key nutrients in various proportions, depending on the plant.

Building a complete picture of how these nutrients move, or cycle, through organisms, soil, rocks, water and the atmosphere is critical to not just agriculture but also to human health.

Dr Goddard-Borger says that every time we eat leafy green vegetables we consume significant amounts of sulfoquinovose, which is used as a source of energy by our gut bacteria.

“We speculate that this will prove to be an important factor in maintaining healthy gut bacteria and good digestive health,” he says.

The world needs sulfur to build many of the proteins that life depends on. Two of the key building blocks of proteins, the amino acids cysteine and methionine, contain sulfur­.

As humans, we can get the sulfur our bodies need from eating protein-rich foods such as steak and pulses. But gut bacteria instead get sulfur from the SQ in leafy green vegetables.

In recent years we’ve been learning about the important role these bacterial communities play in our health and nutrition. Evidence is mounting that fibre and leafy green vegetables are essential in maintaining gut health and believe it or not, E. coli is one of the good guys.

the mystery of the ‘sulfur nutrient cycle’

So Mum was right, it is important to eat our greens. But this story is bigger than brussels sprouts: this humble enzyme solves a mystery that spans 50 years, and now opens a whole new chapter on our understanding of nutrient cycling on planet earth.

This little-known but super-abundant sugar SQ is the actual hero of our story.

Sugars are usually made up of carbon, hydrogen and oxygen atoms, but sulfoquinovose is remarkable in that it also contains sulfur. SQ is produced on a spectacular scale of some 10 billion tonnes per annum; an amount comparable to the annual production of iron ore by the global mining industry.

SQ combines with a fatty part called diacylglycerol to form a molecule called ‘SQDG’. This molecule is produced by essentially every organism on the planet that uses light to grow, and especially plants.

However, what this molecule actually does in plants remains something of a mystery. Although we know it is associated with the process of photosynthesis, that which uses light to turn water and carbon dioxide into sugar and the oxygen that we breathe.

SQDG, discovered in the 1950s, is therefore a critical part pf the biogeochemical cycle of sulfur, or more simply the ‘sulfur cycle’.

Fifteen years ago, researchers described the process of how SQDG was made inside plant cells, but it was only two years ago that we got the first hints of how this molecule was broken down.

In 2014 a German research group discovered that a group of genes in E. coli are involved in the breakdown of SQ. However there was still a missing link in the cycle – the enzyme that cuts the sugar SQ from the sugar-lipid SQDG. This is what the researchers call an ‘SQase’.

The discovery of the SQase ‘YihQ’ by Professor Williams and Dr Goddard-Borger completes the puzzle.

And not only that, this enzyme may open up a whole new chapter of discovery in how our world works. YihQ has a completely unique sequence, which serves as a ‘signature’ of sorts that defines SQases, and now that we know this signature we can use it to search for and identify other SQase enzymes:

“It turns out that these amino acid ‘signatures’ are unique, and we can in turn use computational methods to show that SQases are incredibly widespread across the tree of life, in plants, bacteria (particularly bacteria found in the gut), fungi, protozoa (unicellular eukaryotes) and metazoa (worms and molluscs),” says Professor Williams.

“This discovery, when combined with the recent work from Germany, now provides a complete description of the so-called ‘catabolic arm’ of the biochemical sulfur cycle of SQ, which degrades the sugar to make sulfur available to organisms in the environment.

“We think this information is likely to be of great interest to the agricultural industry, and may allow engineering of plants and environmental bacteria to maximize their use of sulfur to reduce their dependence on fertilisers.”

Banner Image: Freshly washed salad greens. Picture: Pixabay.