The Microbial Pathway to Soil Organic Matter Formation
In recent years there has been growing interest in the potential of soils to sequester carbon [C] from the atmosphere and there has been an increased number of studies investigating the dynamics and nature of soil organic matter [SOM]. Even without highlighting the obvious benefits of carbon sequestration for the climate, there are many ecosystem and agronomic benefits to building SOM which can improve both production and profitability – clearly a major win-win. Many new ideas and new paradigms are emerging and perhaps challenging some of the previous ideas about SOM. One such example is the decomposition and stabilisation of complex vs simple plant residues as they integrate into the soil. That is, the structural plant materials such as lignin and cellulose vs plant metabolic products; such as root exudates, sugars and amino acids. Essentially what this boils down to is a debate on recalcitrant, or complex substrates vs labile, or simple substrates.
Slow Decay: The Previous Paradigm
Previous thinking on how best to build soil organic matter placed greater importance on the more structural plant compounds – the thinking being that these complex C substrates would undergo a slow decay and take a long time to breakdown1–3. The slower the breakdown, the longer the residence time of that C in the soil; and hence bring longer lasting benefits to soil functionality. Consequently, the practical application of this thinking placed greater emphasis on practices such as stubble retention and the preservation of cereal and grass residues over legume litters. This of course comes back to the C:N ratio of these residues with monocot residues containing a high, while legume residues containing a low, C:N ratio. This difference in C:N ratio means that legume residues decay much faster and so it was thought that the benefits of their residues were also short lived. Along the same lines, root exudates were equally discounted as they were too labile and thought to rapidly respire off as carbon dioxide [CO2]1. However, as we will move on and highlight, SOM that is derived from high quality substrates [legume litter and root exudates] is a very different quality and ultimately – is more stable – than SOM derived from structurally complex litters. That said, I must stress, of course I am not advocating the cessation of stubble cover and high residue farming practices – this is an absolutely essential practice particularly in dry climates where moisture is the greatest limitation to overcome.
But the problem with high C:N, structural plant litters is that due to their very complex nature, microbes cannot assimilate the C within these litters very easily, so these litters require a lot of microbial energy to break them down first. A process of pre-digestion, prior to microbial assimilation is necessary. The only way microbes can consume such recalcitrant C compounds is by producing and excreting various enzymes to chemically attack and break down these complex litters. Via this enzymatic digestion, microbes can then subsequently absorb the smaller, more labile break down products. This ultimately means that microbes have to expend or waste metabolic energy to produce these costly extracellular enzymes, and that energy wasted, leads to lower growth rates or lower production of microbial biomass. In other words, the amount of microbial biomass produced per unit of C is lower from these complex litters and consequently, they have a lower carbon use efficiency4 [CUE].
Efficient Assimilation: The Emerging Paradigm
So the obvious question emerges – what if we simply fed microbes more labile and lower C:N ratio substrates in the first place? Then microbes would not have to waste metabolic energy via the production of external enzymes and they could grow more microbial biomass more efficiently. Herein lies the emerging idea of the microbial pathway to SOM formation – if microbes feed on C substrates with a higher CUE – such as labile root exudates and low C:N ratio litters – they can more efficiently grow microbial biomass4,5. I stress the importance of the most efficient way to grow this biomass because recent studies have found that dead microbial biomass [called necromass] makes up more than 50% of soil organic carbon6–8. This microbial contribution is much more than we previously thought; it was assumed that most soil carbon was made up of plant materials in various states of decay. These C inputs – a continuum of decomposing plant remains – which due to their structural complexity, have not yet been assimilated by living microbial biomass, are referred to as particulate organic matter9 [POM]. The key point being, they have not yet been integrated into or through a microbial body. So indeed, SOM is a mixture of both plant derived and microbial derived C inputs10. This new evidence brings to light how important it is to focus on feeding soil microorganisms but specifically to feed them in the most efficient way11. Moving forward, it is suggested that “next‐generation field management requires promoting microbial biomass formation and necromass preservation to maintain healthy soils, ecosystems, and climate7”.
Beyond Sequestration: Stabilisation
As much as there is significant discussion and focus on soil carbon sequestration, I must emphasise a critical message. There is no sequestration without stabilisation. It’s all very well to sequester C into the soil [be that plant or microbially derived], but then it has to stay there! If not, we are simply engaging in the elegant dance that is the global C cycle – a breath in, an exhale. But how to stabilise sequestered C inputs? There are important chemical and physical processes which both uniquely stabilise C into various SOM pools12. Chemical stabilisation occurs when C compounds bind tightly to soil mineral surfaces forming what is called mineral associated organic matter [MAOM]9. The emerging evidence highlights that microbial necromass and high quality plant litters [low C:N ratio] are both more likely to form this highly stable fraction of SOM9,13. MAOM is very slow cycling or has a long residence time in the soil, estimated to have a lifetime of 10-1000 years14.
On the other hand, the physical processes that stabilise C inputs are perhaps more familiar – this happens through physical entrapment into soil micro and macro aggregates. Although the soils inherent chemical and physical condition have an initial influence, aggregate synthesis is primarily driven through biological processes – a complex interaction between roots, root exudates, microorganisms, microbial metabolites and soil macrofauna15. These processes intermingle to glue soil particles together into aggregates of various shapes and sizes and by default, also generate pore space and interconnected pores which optimise gaseous and water exchange16. Of all these biological interactions, it appears that mycorrhizal fungi play a particularly important role via their extensive hyphal branching and synthesis of glomalin – a particularly sticky and stable microbial glue17. It is within soil aggregates where all kinds of SOM can be physically stabilised18 – however this is a particularly important mechanism for stabilisation of POM, which does not have those strong chemical association with mineral surfaces. POM is much more likely to be stabilised via this physical entrapment into aggregates where oxygen is occluded and hence the C is protected. Aggregate existence is not eternal however, they have a limited lifespan and are in a perpetual state of turnover – constantly being formed and broken down and this constant turnover is what makes POM less stable than minerally stabilised C. Consequently, POM is faster cycling and so has a lifespan of approximately 1-50 years14.
Quality and Context Matter
We have outlined how the quality of the litter or C substrate that enters the soil, ultimately influences the quality and the lifespan of the SOM it forms. Low quality or high C:N ratio litters do not so easily pass through microbial bodies and hence, predominantly form POM. POM is stabilised primarily within aggregates but consequently, is vulnerable to oxidative loss during aggregate turnover12. Root exudates and high quality or low C:N ratio litters however, are rapidly digested by the soil microbiota and once these C compounds are ingested and become microbial bodies [and hence part of the microbial pathway], they are more likely to form the more stable fractions of soil carbon when microbial necromass adheres to soil mineral surfaces19. The obvious context that then surrounds this discussion is the different sequestration potential of clay vs sandy soils. Because medium and fine textured soils have more mineral surfaces, they have much greater potential to form MAOM. Sandy and lighter soils with less mineral surfaces cannot form as much of this stable MAOM and are more likely to accumulate POM14. This is not to detract from the potential of POM – it might well form a lower quality and less stable fraction of SOM, but in lighter soils, it is a more dominant fraction and this only emphasises the importance of minimising soil disturbance and maintaining aggregate stability in such sandy soils. Perhaps it could be concluded that stubble cover is king in lighter soils and dry climates while living cover is king in temperate regions and medium textured soils.
Keeping the soil covered with stubble residue is still a valid and appropriate soil health practice and the benefits to soil protection and moisture conservation cannot be understated. However, the emerging evidence suggests that both legume litters and living roots with their associated exudates induce more efficient microbial biomass and necromass production. Consequently, adopting the ‘constant living roots’ soil health principle should be a priority for all farmers whenever possible. This soil health principle will particularly help to optimise the microbial pathway to SOM formation. Sequestration is impossible without stabilisation however, and chemical and physical stabilisation of necromass and plant derived substrates is also key. Consequently, also embracing the minimising soil disturbance principle can bring additional gains to the beneficial effects of living roots, exudates and subsequent microbial interactions and stabilisation of C inputs.
- Leveraging a New Understanding of how Belowground Food Webs Stabilize Soil Organic Matter to Promote Ecological Intensification of Agriculture. In: Soil Carbon Storage. (2018). doi:10.1016/b978-0-12-812766-7.00004-4
- Soil organic matter turnover is governed by accessibility not recalcitrance. (2012). doi:10.1111/j.1365-2486.2012.02665.x
- How relevant is recalcitrance for the stabilization of organic matter in soils? (2008). doi:10.1002/jpln.200700049
- Managing Agroecosystems for Soil Microbial Carbon Use Efficiency: Ecological Unknowns, Potential Outcomes, and a Path Forward. (2019). doi:10.3389/FMICB.2019.01146
- Evidence for the primacy of living root inputs, not root or shoot litter, in forming soil organic carbon. (2019). doi:10.1111/nph.15361
- SOM genesis: Microbial biomass as a significant source. (2012). doi:10.1007/s10533-011-9658-z
- Quantitative assessment of microbial necromass contribution to soil organic matter. (2019). doi:10.1111/gcb.14781
- Divergent accumulation of microbial necromass and plant lignin components in grassland soils. (2018). doi:10.1038/s41467-018-05891-1
- Conceptualizing soil organic matter into particulate and mineral-associated forms to address global change in the 21st century. (2019). doi:10.1111/gcb.14859
- Microbial and plant-derived compounds both contribute to persistent soil organic carbon in temperate soils. (2018). doi:10.1007/s10533-018-0475-5
- The importance of anabolism in microbial control over soil carbon storage. (2017). doi:10.1038/nmicrobiol.2017.105<
- Mechanisms of carbon sequestration in soil aggregates. (2004). doi:10.1080/07352680490886842
- Soil organic matter is stabilized by organo-mineral associations through two key processes: The role of the carbon to nitrogen ratio. (2020). doi:10.1016/j.geoderma.2019.113974
- Soil carbon storage informed by particulate and mineral-associated organic matter. (2019). doi:10.1038/s41561-019-0484-6
- Soil Aggregate Stability: A Review. (1999). doi:10.1300/J064v14n02_08
- Soil structure as an indicator of soil functions: A review.(2018). doi:10.1016/j.geoderma.2017.11.009
- Soil aggregation and carbon sequestration are tightly correlated with the abundance of arbuscular mycorrhizal fungi: Results from long-term field experiments. (2009). doi:10.1111/j.1461-0248.2009.01303.x
- Sub-micron level investigation reveals the inaccessibility of stabilized carbon in soil microaggregates. (2018). doi:10.1038/s41598-018-34981-9
- Nitrogen-rich microbial products provide new organo-mineral associations for the stabilization of soil organic matter. (2018). doi:10.1111/gcb.14009