Focus 15 July 2013

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Microbial impact on climate change The largest driver of global warming is carbon dioxide. Nevertheless, this issue of Focus addresses the formation of two other, often ignored greenhouse gases and their impact on our changing climate. Two microbiologists share their ideas on mitigating the amounts of methane and nitrous oxide in our atmosphere. Other scientists add to the topic with some interesting and closely related views on climate research.

From the editors A FEMS Focus on climate change has long been expected. While climate change is believed to be the result of anthropogenic activities, we should not forget that microorganisms contribute to it, performing their major role in element cycling in the biosphere. With this issue, we want to shed light on the subject from a microbiologist’s perspective, by highlighting the impact of methane and nitrous oxide on raising atmospheric temperature. In this context, these gases also hold their own solutions. Tjitske Visscher & Stefano Donadio, editors

Nitrogen fertilisers in agriculture add to atmospheric nitrous oxide levels.

What are you studying? Caroline Plugge (CP): My research focuses on the interactions that are important in the production of methane. It is a major component of the natural gas we use as a fuel, but it is also a greenhouse gas. We use our knowledge on methane to try and deploy the gas better. People may not expect this, but we actually make methane out of biowaste and then use it as the high-caloric biofuel it is. In addition, we recently started a new research project on finding strategies to mitigate current emissions of methane from ruminant livestock, in our case dairy cows. David Richardson (DR): We look at the way bacteria work when they lack oxygen and how this influences the environment. Anaerobic metabolism in sediments, soils and oceans has a huge impact on geochemical cycles. One of my

Dr. Caroline Plugge is an assistant professor at the Laboratory of Microbiology, Wageningen University and Research Centre, The Netherlands. Together with her students, she studies the cooperation between anaerobic organisms in degrading complex organic compounds.

Prof. David Richardson is a professor in microbial biochemistry and deputy vicechancellor of the University of East Anglia in Norwich, United Kingdom. His group works on the biochemistry of bacteria in the nitrogen, iron and carbon biogeochemical cycles.

personal topics is the biochemistry of denitrification in agricultural areas, which impacts global warming. Global warming arises, in part, through the intensive use of nitrogen fertilisers for the last hundred years. During one stage of this process, the greenhouse gas nitrous oxide is formed.


Nitrous oxide in the environment

How could your work on microbes contribute in countering or decreasing climate change?

When bacteria and certain fungi are deprived of oxygen, they turn to nitrate respiration. One of the products generated in this process is nitrous oxide, commonly known as laughing gas. Nitrous oxide accounts for only 0.3% of all greenhouse gases emitted, but its impact on global warming in CO2-equivalents is as much as 10%. The reason: it is as much as 300 times more potent than CO2 itself. Each year since the introduction of nitrogen fertilisers 100 years ago, the concentration of nitrous oxide in the atmosphere increases by 2.5%. When deprived of oxygen, some bacteria

CP on methane: In bioreactors, archaea produce methane from bioresources under controlled conditions. We can then use methane as a high-caloric biofuel to generate electricity. In that form, the energy is usable anytime and anywhere. It can both serve as a substitute for fossil fuels and help to solve our waste problem. We call it upcycling instead of recycling of biowaste. DR on nitrous oxide: The influence of microorganisms on climate change is substantial. They contribute to it. But of course, microbes can’t think. It is man who is producing greenhouse gases, albeit sometimes indirectly via microorganisms. Our agricultural fertilisers are part of the biggest geo-engineering process in the world. You can possibly reverse their influence on global warming when you understand how microbes in the soil work. It is a sort of scientific intelligence, if you like.

Methane in the environment Methane is a greenhouse gas produced by archaea. These microorganisms are present in many anoxic environments: in natural ones such as lake sediments, but also in human-induced environments, such as rice fields and waste deposits. Ruminant cattle make up the largest group of anthropogenically driven methane producers. Methane is able to catch the Earth’s heat 24 times better than is carbon dioxide and methane accounts for about 14-17% of global warming in so-called CO2 equivalents. Methane is generated by the anoxic degra-

dation of organic carbon from, for example, plant material. The process involves several basic steps in different microorganisms. After hydrolysis of large polymers, fermentation results in short chained fatty acids. Then, acetate, hydrogen and carbon dioxide are formed. These are the three major components for methanogenesis, which can only be performed by the methanogenic archaea. After that, methane oxidizing bacteria can degrade methane, but need oxygen to do it. Methanogenesis in a rice field.

CP on methane: I think that indeed, they are. The principle of controlled methane-generation is actually already applied on farms in Germany. During the last ten years, 5,000 bioreactors have been installed, making methane out of biowaste such as corn and animal manure. And then there is the methane that ruminants emit by mouth. There is worldwide consensus that methane emission from cows should be decreased significantly by 2020 and we are now also trying to find out how that could be achieved. DR on nitrous oxide: It is the job of scientists to advise politics in solving major problems. I am, though, not directly involved in politics. Mitigating atmospheric methane levels Several disciplines and industries can provide solutions for bringing down the amount of methane in the atmosphere. Much methane is emitted by wetlands, among them rice fields. In those environments, methane degradation is carried out by methane oxidizing bacteria, but these organisms evidently need oxygen, which is not available in anoxic soils. Temporary drainage would provide oxygen to those bacteria. Collecting methane from all kinds of sources and using it directly as a fuel, could be an effective and direct method. Decreasing the levels of methane produced by archaea in cow stomachs could contribute significantly. Solutions may lie in alternative food and possibly even animal breeding.




fatty acids




carbon dioxide

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Production of nitrous oxide in soil below grassland.

An electromicroscopic image of the methane producing archaeum Methanosaeta concilii. Picture: WUR.

But we are part of an international training network called the Nitrous Oxide Research Alliance. It brings together different parties from all over Europe. With our knowledge, we think that farmers could be taken along in a new way of looking at their land. Individual farms and larger companies already have to think of their carbon footprints. They could possibly meet this challenge easier when they focus on the decrease of nitrous oxide that they emit. In my opinion, you should combine natural and social sciences in this issue. It is partly about influencing human behaviour. Is your possible solution expensive? CP on methane: Not necessarily, primarily as the infrastructure for spreading natural gas is already available. In the end, it could even generate money, because we would need fewer fossil fuels. It is hard to say exactly how much energy from fossil fuel can be saved, but the amount is certainly significant. DR on nitrous oxide: Evidently, it would require some expense, but it is mostly about changing practice. Certain fertilisers have been used for many, many years and are very efficient, I am sure. But that doesn’t mean that crops would necessarily be disadvantaged by the use of alternatives. Governments should probably make it attractive for farmers to incur those expenses, maybe even by setting legal targets.

Are your results interesting for international politics?


and fungi switch to the process of denitrification. They convert nitrate in four steps, to nitrite, nitric oxide, the greenhouse gas nitrous oxide and finally dinitrogen. As nitric oxide is a potent cytotoxin, reducing it to nitrous oxide is essential to the organism. In some cases, however, that remains the final step, leaving behind a greenhouse gas in the environment. It is estimated that two third of all nitrous oxide in our atmosphere is formed by denitrifying microorganisms.







nitric oxide nitrous oxide

How many degrees of global warming will we, in the end, have to accept? CP on methane: I think that I am a climate sceptic. We can speculate on the effect of human activities or make all sorts of calculations. But the climate specialists do not agree on this matter either. The geological time scale has to be taken into account as well. DR on nitrous oxide: When you ask this question of different scientists, some would say that keeping global warming at two degrees is the best we can do. Others would find this insufficient and would plead to keep it below two degrees. Personally, I think that holding back to two degrees is pragmatic, but still challenging in itself.

N2 dinitrogen

Mitigating atmospheric nitrous oxide levels The main reasons for an unfinished denitrification process are to be found in the activity of the reductive enzyme N2OR. First of all, fungi and certain bacteria simply lack the genes to produce N2OR. For those with these genes, stimulating completion of the process could mitigate the nitrous oxide release from our soils. That is why some important measurements, suggested by Richardson and his colleagues, are based on that concept. Low soil pH reduces the activity of N2OR. Liming for pH regulation can solve this. Copper ions make up an essential part of the active compounds in N2OR, so copper deficiency in the soil is restrictive. Management of soil organic matter can ensure the availability of copper. At a nitrate level higher than 10 mg/g soil, nitrate is preferred above nitrous oxide as an electron acceptor. Therefore, controlled fertilisation with nitrate is important.

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Microbes in climate models Dr. Paul Bodelier is a microbiologist at the Netherlands Institute of Ecology (NIOO-KNAW). He is working on the functional diversity of microorganisms in natural and semi-natural wetlands, for example rice fields and flood plains. “We microbiologists have good evidence that the properties of microbial species have to be considered in climate models”.

Bodelier: “There is a strong relationship between the N-cycle and methane cycling in soils and sediments, which is affected by methane-consuming microbes present. Therefore, in some areas, nitrogen fertilisation can lead to raised methane emissions, while in other environments they are reduced. The reason is a difference in the reaction of bacterial species oxidising methane. For methane-producing microbes, we showed that from soils that are physically identical, but inhabited by communities composed of different species, up 400 times different methane emissions could be observed. Biogeochemists think that biogeochemical reactions, such as the production or consumption of methane, are controlled mainly by physical, abiotic parameters. However, I strongly suggest that the characteristics of, and relations between microbial species should be considered in climate models. This will be especially important when predicting the effects of disturbance. Responses of microbes after disturbances can not be predicted from physical parameters.” Rice fields contribute significantly to methane production.

Global change on the higher level Prof. dr. Michael Wagner studies the physiology of microbes in their environments. Specifically, he works on nitrification, the oxidation of ammonium into nitrate and nitrite, which is a process in aerobic microorganisms. Wagner works at the Division of Microbial Ecology at the University of Vienna. “Microbes have a large impact on more aspects of global change than temperature alone.” Wagner: “Most people are primarily interested in the effects of microorganisms on global warming, but there is actually a large impact on the even higher level of global change. There are many long-term alterations by microbes to their ecosystems. As there is a huge amount of nitrogen present in the worldwide nitrogen cycle, it has side effects on our climates through the activities of microbes. Think, for example, of eutrophication, the accumulation of nitrogen in an ecosystem. It can influence certain parts of the oceanic water columns and cause algal blooms in the upper part. Eutrophication can also, due to other microbial processes, be responsible for the existence of anoxic zones in intermediate parts of the water column. This may in extreme cases cause the death of all organisms that need oxygen.”

Find out more about the topics in this Focus David Richardson: Caroline Plugge: Paul Bodelier: Göran Ågren: Michael Wagner: The UN Framework Convention on Climate Change: The Nitrous Oxide Research Alliance:

The view of an ecologist Prof. Göran Ågren studies the consequences of currently increasing temperature on the reproduction of microbes and on the amount of greenhouse gasses in the atmosphere. He is connected to the Department of Ecology at the Swedish University of Agricultural Sciences. “But I am an ecologist, so I look at the ecosystem rather than at individual species or processes within the organisms.” Ågren: “It is known that due to global warming, bacteria and fungi reproduce more rapidly. At the same time, they use a larger share of the available carbon for their own respiration, thus bringing more carbon dioxide into the air and stimulating atmospheric warming even more. That is how microbes are believed to contribute to climate change, but this is only true for the short term. Under temperate conditions, there is a shortage of easily accessible matter in the soil after about five years. The microorganisms just don’t have enough food for their reproduction and they stick to maintaining themselves. The microbial community stops growing. When microbes then start dying, the amount of active organisms declines. This will, in turn, reduce soil respiration and therefore greenhouse gas emissions to pre-warming levels. I believe that we have to become more aware of

the exact response of microbes to higher temperatures if we want to predict how the soil will respond to it as a whole. At this moment, we don’t know enough and responses strongly depend on the type of ecosystem.” The FEMS Focus is published by: FEMS Central Office Keverling Buismanweg 4 2628 CL Delft The Netherlands Tel: +31-15-269 3920 Fax: +31-15-269 3921 E-mail: FEMS is a registered charity (no. 1072117) and also a company limited by guarantee (no. 3565643). © 2013 Federation of European Microbiological Societies Final Editor: Jim Prosser Design: Zak Princic Production:

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