Living on air: uncovering bacterial mysteries for agriculture and climate

By Thea Williams August 27th, 2015

Scientists have solved one of the mysteries of certain soil bacteria that allows them to persist without an apparent source of sustenance. It might lead to solutions for improving agricultural production while reducing greenhouse gas emissions.
Two tractors preparing paddocks for cropping

Agriculture is the main human source of the greenhouse gas nitrous oxide. Image: Stuart Rankin/Flickr, CC BY-NC 2.0

This greenhouse gas is almost 300 times more powerful than CO2 – and in Australia, agriculture is responsible for producing more than 85 per cent of it.[i]

It’s nitrous oxide, N2O.

Forget the familiar images of belching industry or traffic smog; the N2O released from fertiliser used in cropping and pasture, along with industrial quantities of urine from dairy and cattle, has become one of the major sources of greenhouse gas emissions from human activity.

The other side of the story for agriculture is that nitrogen fertiliser delivers great benefits for crop growth and yield.

Ever since medieval England discovered the advantages of introducing legumes in their crop rotation, farmers have been playing with nitrogen in their production systems. What the farmers at that time had stumbled on was that bacteria associated with the legumes they introduced were able to ‘fix’ nitrogen – that is, convert it into ammonia, which is the form of nitrogen that can be used by other crops.

So these nitrogen fixing bacteria are particularly useful for production.

But then there are other bacteria in soil that undo that process – converting the ammonia into the greenhouse gas N2O, through a process called nitrification.

Graphic showing nitrogen cycling from soils to atmospher via plants, industry and agriculture

The Nitrogen Cycle

Modern fertilisers and the nitrogen conundrum

In the early 1900s German chemist Fritz Haber developed a way of synthesising ammonia from nitrogen and hydrogen – and helped develop modern fertiliser. He won the Nobel Prize for chemistry in 1918 for his efforts.[ii]

While ammonia-based fertiliser was revolutionary, it does have its problems. Much of the ammonia is oxidised to nitrate and nitrous oxide through the process of nitrification and denitrification. Not only is this wasteful, but it’s also environmentally unsustainable – nitrate leaches through soils into waterways and nitrous oxide is emitted into the atmosphere. Large-scale grazing of animals has added to the nitrogen conundrum. New Zealand has a particular appreciation of the dangers of too much nitrification, a country where the number of cows grew from just more than 2 million in 1973/74 to 4.7 million in 2012/13.[iii]

The question for agriculture – whether it’s cropping using ammonia-based fertilisers or grazing and dairy farming with ammonia from animal urine – is how to fix the nitrogen in the soil and avoid nitrification.

Anyone interested in the cause and effect of greenhouse gas emissions may do well to understand that it is the microorganisms in soil that control the mix of gases in the atmosphere – nitrous oxide, methane and trace gases such as hydrogen among them.

So for farmers looking to solve their nitrification problems, and for those concerned about greenhouse gas emissions, answers might well lie in the bacteria in the soil.

That’s where the microbiologists come in.

Taking a closer look at the lifestyles of bacteria

Two men standing in a lab

Professor Gregory Cook (left) and Dr Chris Greening. Image: Alan Dove.

One of those microbiologists is Dr Chris Greening, postdoctoral fellow at CSIRO Land and Water, who works under the supervision of Dr Matthew Taylor. His interest centres on greenhouse gas cycling and the role that hydrogen consumption plays in the survival of soil bacteria. This fascination traces back to doctoral research he conducted under Professor Greg Cook at the University of Otago.

He has recently published, with other authors including Professor Cook, three articles in the prestigious journal Proceedings of the National Academy of Sciences (PNAS), and will soon publish another in the journal of the International Society for Microbial Ecology (ISME).

It has long been a mystery, how some dormant bacteria manage to survive and dominate in soils where all fuel sources appear to exhausted, especially those responsible for converting the ammonia that’s useful for agriculture into the greenhouse gas N2O.

In breakthrough work, Dr Greening and Professor Cook found that they manage to persist by scavenging hydrogen in the air, metabolising the energy from hydrogen using a special enzyme called a hydrogenase. “Though hydrogen is only present in tiny amounts in the atmosphere, it is always present and therefore serves as a highly dependable backup fuel,” Dr Greening says.

To prove their point, Dr Greening and Professor Cook studied Pyrinomonas methylaliphatogenes, a bacteria isolated from a volcanic crater near Lake Taupo – inhospitable even for most microorganisms because of its lack of nutrients. They studied the genetic and biochemical capabilities of the organism and found that, even in that nutrient-starved environment, the bacteria could survive. How? With hydrogen.

This work was significant because it helped explain the paradox of how a group of slow-growing bacteria, the Acidobacteria, have somehow become the second most-populous bacteria in global soils.[iv] “They’re not very good at growing, but they can survive just about whatever Earth has to throw at them”, Dr Greening says.

Two black squares with different sized green oval shapes inside

Bacterial cells growing on carbon (left) are visibly larger than cells persisting on hydrogen (right). This is because atmospheric hydrogen provides the bare minimum energy for survival. Image: Michael Berney.

The findings have been welcomed by the microbiology community. “This work is exciting because it expands on our understanding of how microbes, and which species of them, can persist when confronted with energy starvation in the environment,” says Dr Damien Finn, a soil microbiologist at University of Queensland.

“Exploring the lifestyles of energy-starved microbes has thus far received little attention, and yet it represents the dominant state of organisms that drive globally important biogeochemical processes. A greater understanding of microbes under these conditions will lead us to a greater understanding of how our planet functions.”

The implications for agriculture

In their upcoming ISME article, they’ve extended their research from looking at single organisms to the ecosystem as a whole. In the process, they’ve shown that hydrogen consumption is much more than a niche process. In fact, many of the bacteria in global soils encode hydrogenases, including those bacteria responsible for nitrification in agricultural soils.

“What we’ve realized is that the bacteria that are mainly responsible for nitrification – that’s converting ammonia in soil into the undesirable nitrous-oxide – are more flexible than previously thought and survive longer in starvation conditions. Because once they’ve exhausted their preferred energy source, ammonium, they may be able feed off hydrogen to survive in a dormant state,” says Dr Greening.

“This is bad for farmers who don’t want such bacteria in their soils.’’

In Australia and New Zealand, a nitrification inhibitor called DCD is commonly used. It prevents bacteria from oxidising ammonia. In doing so, it aims to mitigate greenhouse gas emissions from intensive agricultural systems in Australia.

But these nitrification inhibitors only work transiently. A collaborator and co-author of Dr Greening’s, Dr Sergio Morales (University of Otago), has shown they only pause growth of nitrifying bacteria.[v] They don’t kill them. So these bacteria must be more flexible than we previously realized.

“Hydrogen may be the key to this: Hydrogen is the fuel those bacteria can survive from. If farmers still keep adding this DCD fertiliser, the bacteria will come back again and again.’’

The question then becomes: Having identified the key enzyme at work which helps these unwanted bacteria survive, can scientists develop a product that would improve the effect of nitrification inhibitors?

“Hydrogenases might be a potential next-generation target. If you co-administer a hydrogenase inhibitor with a nitrification inhibitor like DCD, those bacteria that are really wasteful for nitrogen and produce greenhouse gas emissions might be preferentially killed off,’’ says Dr Greening.

But he admits that, as hydrogen metabolism is so widespread, administering such an inhibitor might also kill useful microorganisms in the soil. “There’s a fine balance to achieve: to enhance the sustainability of agriculture, we want to keep as much ammonia as possible in the soil without disrupting the ecosystem as a whole.”

Dr Greening and his co-workers are now investigating the consequences of inhibiting these survival processes on agricultural soils.

“We’ve known for a long time that bacteria control the hydrogen cycle, but we didn’t understand why they would bother consuming such tiny concentrations of hydrogen in the air. But now we do: it’s no good for growth, but it’s a great lifeline for survival.’’

And what makes these micro-organisms so hardy – the enzyme that enables them to process hydrogen – may just prove to be their Achilles heel.


 

Notes

[i] The N2O Network – Information for policy makers: Why focus on N2O from agriculture?

[ii] Chemical Heritage Foundation: Fritz Haber

[iii] New Zealand Dairy Statistics 2012/13 [PDF]

[iv] Persistence of the dominant soil phylum Acidobacteria by trace gas scavenging in the Proceedings of the National Academy of Sciences, approved July 15, 2015. Authors: Chris Greening, Carlo R. Carere, Rowena Rushton-Green, Liam K. Harold, Kiel Hards, Matthew C. Taylor, Sergio E. Morales, Matthew B. Stott and Gregory M. Cook.

[v] Impact of urine and the application of the nitrification inhibitor DCD on microbial communities in dairy-grazed pasture soils in ScienceDirect, September 2013. Authors: Sergio E. Morales, Neha Jha and Surinder Saggar.

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