Is humus humbug?

For more than a century the concept of humus as an important component of soils has been intensively studied and widely adopted by soil scientists, agronomists, ecologists, climatologists, biogeochemists and others. Outside our own interest of its effects on soil fertility, just one example of its broader significance relates to green-house gas emissions and global warming. Soil organic matter (SOM) contains more sequestered carbon than is present in the atmosphere and global vegetation combined, so turnover resulting in altered pool size is vitally important in efforts to understand and control this modern problem. Humus has historically been thought of as a range of dark-coloured, variably-sized but usually large and very stable molecules, synthesised by microorganisms in the course of plant and animal organic matter degradation. However research in the last 20 years, possible only with the development of modern techniques such as spectro-microscopy, is now challenging this well-established story, as revealed in a study ‘The contentious nature of soil organic matter’ published in the pre-eminent scientific journal Nature (2015) 50, 60-68.

Traditional humification models include a variety of features as follows: It is proposed that plant (eg branches and leaves) and animal residues are initially reduced to smaller fragments or particulates by fauna (eg cattle, worms and slaters), physical processes (eg moisture, temperature and oxidation) and enzymes secreted by soil microbes (exo-enzymes), but in these early stages they are still too large for microbial assimilation. Further exo-enzymes then continue this degradative process, ultimately producing much smaller molecules (molecular weight <600) that can then be taken up by soil microorganisms. In the course of microbial metabolism, large, complex and stable humic substances are produced which are subsequently released into the soil on microbial death. In this latter stage of the pathway, other absorbed organic molecules are used as a source of microbial energy supply, and the ultimate end product of this utilization is the oxidation product, carbon dioxide, released through the soil into the atmosphere. More labile chemical forms such as smaller carbohydrates and proteins are thought to be broken down faster and in preference to more stable macromolecules like cellulose and lignin, with the latter decomposition mainly occurring only after the labile forms have been exhausted. A build-up of humus in soils to typical levels of 5% was a desired attribute because it increased soil fertility through retention of water and nutrients, improved soil texture, and minimised toxic effects of pollutants such as heavy metals and industrial chemicals by complexation.

Given this concept has been used so successfully for such a long a time in so many scientific disciplines, how come it is now being challenged? Soils are an incredibly complex and changeable matrix of interacting minerals, organic matter, biota, water and air pockets. Until the 1990s the most productive way of studying the nature of these varied systems was to separate different components and then study these more tractable parts individually. The most effective way of separating SOM from the other components was to use strongly alkaline (pH13) extraction. This dissolved 30-50% of the organic matter, and when these solutions were re-acidified, the dark-coloured substances that were precipitated were called humic acids and those that remained in solution were called fulvic acids. The organic matter that was not dissolved under alkaline conditions was labelled the humin fraction, and collectively all of these were called humic substances, or humus. A number of techniques indicated the molecular weights of entities in humus varied from <1000 to millions. Radiocarbon dating also suggested that some of the larger alkaliextracted molecules could be many hundreds of years old, thus leading to the idea of part of any added organic matter to soils being converted by microbes to beneficially recalcitrant large molecules, while the smaller more labile molecules were used as energy supplies for microbial growth and metabolism.

Alkali-extraction became so well-entrenched as a pivotal step in study of SOM that it became a proxy, even though concerns about the representativeness of its products were raised very early on. At pH13, most oxygen-containing functional groups in SOM become ionised, making them more water soluble. But because less than half of all SOM is extracted, the soluble humic and fulvic acids can’t totally represent all SOM. Furthermore, other materials not really part of humus may be dissolved (eg cell wall parts from dead microbes – think of potent alkaline oven and drain cleaning solutions), and how these soluble extracts interact with the non-soluble humin parts in soils was not clarified. The harsh extraction conditions also gave a misleading and exaggerated impression of the reactivity of humic and fulvic acids compared to what they might be under more normal soil conditions of pH 3-8.

Review of the latest research reveals that secondary microbial synthesis (following degradation of litter materials sufficient to allow absorption) of large stable humus molecules has never been convincingly demonstrated. Radioisotope studies show that when the appropriate decomposers are present under suitable prevailing conditions of access, aeration, temperature and moisture, breakdown of celluloses and lignins can in fact be quite rapid. Dark humus colours are due to variable degradation of plant pigments. The apparently large molecular sizes of humus are actually aggregates of smaller molecules which can appear to be individual larger molecules, and radiocarbon dating suggesting century long stability reflects, not their stability but the times, that the atmospheric carbon was incorporated into organic molecules through plant photosynthesis.

The authors of the above study have suggested a Soil Continuum Model that provides a better understanding of what applies under actual soil conditions. Here, the breakdown of litter results in a full range of co-existing particulates and molecules, with gradual and one-way progress (ie no secondary synthesis) from large to small over time throughout the soil. As particles become smaller, the opportunities for them to become more water soluble increase due to the conversion of previously un-exposed ionisable groups within larger molecules and particles. The presence of these ionisable entities confers increased reactivity for interactions with mineral surfaces resulting in adsorption, and they also contribute to aggregate formation. Aggregates and mineral-adsorbed molecules are not fixed but may cycle between free and bound forms in competition with other cations and organic substances. When in free states they are more subject to further and continuing degradative processes. So the progress of SOM is always on an energetically downward spiral (exothermic) without the traditional humus postulate that it subsequently went through synthetic stages (anabolic reactions) requiring energy inputs to produce large and stable substances.

The long humus lifetimes are due to protection by minerals (primarily clays) and aggregate formation, not to intrinsic molecular chemical stability. This protection results from either complexation, or reduced degradative microbial action because of access limitations when SOM is located in particulate mineral crevices or tunnels, or through aggregate formation where interior particles are less available to microbes and exo-enzymes that are in the aqueous phase. The idea of enriching a soil by building a ‘stable humus pool’ is unrealisable as SOM is always rapidly degraded unless delayed through protection. Any positive plant responses to ‘humic substances’ in addition to conventional effects of SOM on soil fertility imply that the alkaline extraction process also removes other substances with plant hormone-like activity. This is a feature that will generate strong resistance to abandoning the traditional humus concept as a considerable agri-business sector rests on heavy marketing of these un-identified products as soil improvers and growth promoters. This should not be cause for continuing with the humus story but for research to identify any beneficial substances. In concluding, the authors propose that further insights into the properties of SOM will come from study of the time-dependent interactions with abiotic factors (eg clays, temperature, moisture, texture) and the microbial population in the three-dimensional architecture of whole soils in their natural aqueous environment, not from pH13 extracts and the supposed existence of large humic substances. The Soil Continuum Model represents a major upheaval to the long-established humus concept, but such major revisions are not all that unusual in the history of science when new experimental techniques periodically become available, allowing more realistic examination of worldly phenomena.

For those of us living in the Perth coastal region where our starting point for what we have as soil is almost pure beach sand without any clays, the new understanding of SOM has important implications for growing fruit trees. Regular addition of SOM is necessary to achieve good soil fertility, particularly for us where we start with almost none, but if not protected it’s rapidly consumed by soil microbes and will require more frequent applications. If sufficient clays are also added, this decay process can be slowed down significantly so the beneficial effects of SOM, namely cation exchange capacity, water retention, soil texture and microbiota population/diversity, can be maintained for longer periods. The first without the second means you’ll have more work to do more often and with less benefit.