Organic matter in permafrost soils: storage, turnover and possible effects of global warming
Permafrost soils cover about 22 million km2 in circumarctic polar areas, and 65% of the land area of the Russian Federation is underlain by permanently frozen soils. Estimates on the organic carbon storage in permafrost soils range from about 1.000 to 1.700 gigatons. With that permafrost soils are currently the largest terrestrial sink for non-fossil carbon, and small changes in the stock of organic carbon in permafrost soils will have profound impact on the atmosphere’s CO2 (and CH4) concentration and with that very likely on the Earth’s climate.
Whether these soils will become a major source of greenhouse gases in the future depends on the accessibility of organic compounds to the decomposer community under the given environmental conditions. In permafrost soils, primarily low (frozen) temperatures and high moisture is most decisive in limiting biodegradation of organic matter. Permafrost thaw will change these conditions with increasing temperature and oxygen availability likely favor conditions for microbial decay of organic matter. With this respect it is important to know whether other processes than freezing and anaerobiosis will lead to the stabilization of organic matter in permafrost soils. From temperate soils we know that the formation of mineral-organic associations by sorption of dissolved organic matter to reactive soil minerals like iron oxyhydroxydes or coprecipitation of dissolved organic matter with metal cations is a very efficient process in the stabilization of organic matter in soils. Nothing is known whether such process is relevant also in permafrost soils, and whether this may help to reduce to organic carbon losses from permafrost soils at permafrost thaw.
The goal of our work was to assess the organic matter resource in Siberian permafrost soils under the aspect of climate change with respect to the following questions:
- What is the variability of organic carbon stocks in Siberian permafrost soils at landscape scale and within the soil profile?
- What is the chemical composition of organic matter in permafrost soils and how is soil organic matter transformed?
- Is organic matter stabilized in permafrost soils also by other processes than freezing and anaerobiosis and is this relevant with respect to mitigation of the consequences of permafrost thaw?
Materials and Methods
For our studies we have chosen two transects. One transect covers tundra sites with continuous permafrost from east (Cherskiy), central (Ary-Mas, Logata), and western (Tazovskiy) Siberian north. The other transects stretches in the central part of Siberia from the north under tundra vegetation (Ary-Mas, Logata) to the forest tundra (Igarka) and taiga (Tura, Baikit) further south. The sites at Igarka and Baikit are characterized by discontinuous permafrost. While the northern permafrost soils developed mostly on aeolian sediments, the soils at Tura and Baikit formed in igneous rocks (trapp basalts). In total we dug about 80 soil profiles, analyzed them for organic carbon and nitrogen contents and stocks and measured for most of the soils other general soil parameters like soil texture. On selected soil profiles, we performed some in-depth analysis of the composition and the function of the soil organic matter and the microbial community. This includes
- density fractionation of soil and organic matter to separate different functional pools,
- chemolytic analysis of the most prominent organic matter constituents lignin and polysaccharades to identify decomposition pathways of soil organic matter,
- general characterization of the organic carbon using 13C nuclear magnetic resonance spectroscopy as a complementary method to identify decomposition pathways,
- quantification of bacterial, archaeal and fungal SSU rRNA genes by quantitative PCR to assess microbial community composition,
- priming experiments in order to assess the possible role of easy available carbon and/or nitrogen source on organic matter decomposition,
- large scale incubation experiments to delineate controlling factors on organic matter decomposition.
Results and Discussion
The organic carbon storage showed a high spatial variability of <10-50 kg m-2 in the soils under study. Largest stocks were observed in continuous permafrost soils developed on sedimentary parent material. Cryoturbation and cryohomogenization processes led to a large contribution of subsoil horizons (incl. the permafrost layer) to the total soil organic carbon stocks. At Igarka, comparison of permafrost soils with non-permafrost soils showed much smaller organic carbon stocks in the latter. Soils at Tazowskiy, which are characterized by very thick active layer or lacking permafrost, revealed the smallest soil organic carbon stocks. This indicates that in the northern soils developed from sedimentary materials permafrost thaw leads to prominent organic matter losses. The situation is a bit different in the soils at Tura and Baikit, which developed from igneous rocks. There, differences in organic carbon stocks between permafrost soils and soils with deep active layer or no permafrost were small, and in some cases non-permafrost soils contained even more organic carbon than permafrost soils. Hence, permafrost thaw in the large central Siberian regions may have completely different consequences than in the Siberian north. The density separation revealed that on average 56% of the organic matter in the investigated permafrost soils can be fractionated into the heavy fraction and thus occurs in form of mineral-organic associations. This may impose a possible protection mechanism against organic matter decomposition, which will be discussed later.
Even though environmental conditions are not favorable for organic matter decomposition in permafrost soils, different proxies revealed an increasing decomposition of organic matter with increasing soil depth. This is already indicated by the increasing carbon-to-nitrogen ratio along with increasing δ13C ratios with soil depth. Also 13C nuclear magnetic resonance spectroscopy shows a decrease of O-alkyl carbon along with an increase in alkyl carbon and aryl carbon with increasing soil depth, being indicative of a pronounced organic matter decomposition and enrichment of more refractory organic matter constituents. The chemolytic data revealed some interesting differences in the decomposition pattern of lignin and lignocellulose. In contrast to temperate soils, particularly the permafrost soils with high permafrost table and large storage of organic matter are characterized by a restrained lignin decomposition, as is indicated by constant acid-to-aldehyde ratio of the vanillyl units and rather increasing proportion of lignin-derived organic matter with soil depth. In soils with thicker active layer, more aerobic soil conditions, and smaller organic carbon stocks, lignin decomposition is much more proceeded. The restrained lignin decomposition indicates a major mechanism of organic matter sequestration in permafrost soils, which is similar as in bogs. Also similarly to bogs, changing environmental conditions and better aeration with permafrost thaw fosters primarily losses of lignin with soil organic matter decomposition.
In the laboratory, the soils were subjected to a range of incubation experiments. Using a 15N dilution assay to quantify the gross protein depolymerization indicated that the topsoil materials of the permafrost soils were not nitrogen limited. In contrast, the subsoil and particularly the cryoturbated pockets revealed a strong reduction of the protein depolymerization. This suggests a nitrogen deficiency as a control of the organic matter turnover in the subsoil. Priming experiments with monomeric and polymeric easily available carbon and nitrogen sources confirmed this result. In the cryoturbated pockets the addition of an amino acid or a protein strongly increased soil organic carbon mineralization, thus emphasizing the impact of low nitrogen availability on organic matter stabilization. In contrast, the mineral subsoil responded also positively to the addition of glucose or cellulose. This so-called positive priming suggests that the decomposition of organic matter in the subsoil is also carbon limited. Hence, if a changing soil environment will lead to a larger release of easily-available organic substances in the subsoil, i.e., by rhizodeposition, this may also result in losses of indigenous soil organic matter in permafrost soils.
As said above, the majority of soil organic matter in permafrosts soils is involved in mineral-organic associations, thus possessing a potential stabilization mechanism. In 120 soil samples from 24 soil profiles, mineralization of whole soil and of mineral-associated organic matter was monitored for 180 days to assess the temperature dependency and the protection of minerals for organic carbon decomposition. The incubation revealed a large active pool in the topsoil and in the permafrost horizons, while decomposition was restrained in the cryoturbated pockets. The application of linear mixed effects models revealed that the basic drivers for the bioavailability of permafrost soil organic carbon decomposition are nutrient availability, mineral protection and microbial community response.
Temperature was the principle driver of the organic matter mineralization throughout the whole incubation, however, the temperature effect strongly decreased with soil depth. As the organic matter quality decreased with soil depth (see above), this contradicts the carbon-quality-temperature hypothesis stating that the turnover of low quality organic matter is more sensitive to temperature increase than easier available organic matter. This observation can be explained by an active protection mechanism. Enzymes for decomposition can be excluded by physicochemical protection with the mineral soil matrix, causing substrate limitation to decomposers. This is process is almost independent of temperature and can attenuate the inherent kinetic properties of organic molecules. And in fact, linear mixed effects models indicated a partially strong negative effect of clay-sized minerals and pyrophosphate-soluble iron on organic carbon mineralization, thus confirming the stabilizing effect of organic matter by association with poorly crystalline iron oxides and clay minerals or by coprecipitation with multivalent cations (aluminium, iron).
Under future scenarios, besides higher soil temperature a better oxygen availability, higher nutrient availability and larger input of rhizodeposition at larger soil depth will stimulate organic matter decomposition, thus decreasing the soil organic carbon storage. At the other hand, warmer temperature will increase plant net primary production and thus organic matter input in soil, and dryer and more oxic conditions in the soils likely will increase the protection of soil organic matter by an increasing formation of reactive soil minerals, which both will lead to larger organic carbon stocks. Different permafrost systems may respond differently on these two contrasting processes. At the nowadays largely anaerobic permafrost soils in the north Siberian lowlands, the effects of a better oxygen availability on organic matter decomposition, particularly of lignin, as well as nutrient and carbon priming will outcompete the effects of an increasing organic matter stabilization by neoformation of reactive soil minerals at permafrost thawing. In the permafrost soils of the central Siberian trapp basalts, the situation is different. There, the soils do not contain as much organic carbon as the permafrost soils in the north due to the limitation of soil depth by the parent rocky material and the almost lacking cryoturbation processes. These permafrost soils are also better aerated and rooted. Hence, the negative consequences permafrost of thaw on organic carbon stocks at will not prevail, but rather the positive ones such as higher plant residue input and effective stabilization of organic matter by formation of mineral-organic associations due to high production of particularly iron oxyhydroxides by weathering from the iron-rich primary minerals. The soils in the large areas of the Siberian mountain ranges, which are partly underlain by permafrost, may thus be even carbon sinks in the future.