Biosolids Soil Application: Agronomic and Environmental Implications 2013View this Special Issue
Soil Carbon Sequestration Resulting from Biosolids Application
Carbon (C) sequestration in soils through the increase of the soil organic carbon (SOC) pool has generated broad interest to mitigate the effects of climate change. Biosolids soil application may represent a persistent increase in the SOC pool. While a vast literature is available on the value of biosolids as a soil conditioner or nutrient source in agricultural systems, there is still limited knowledge on soil sequestration mechanisms of biosolids-borne C or the main factors influencing this capacity. The emerging challenges posed by global environmental changes and the stringent needs to enhance C storage call for more research on the potential of soil biosolids incorporation as a sustainable C storage practice. This review addresses the potential of C sequestration of agricultural soils and opencast mines amended with biosolids and its biological regulation.
Increasing concern about global climate change has led to growing interest in developing feasible methods to reduce the atmospheric levels of greenhouse gases (GHGs) . Among GHGs, atmospheric carbon dioxide (CO2) accounts for 60% of the global warming . The atmospheric concentration of CO2 increased from 280 parts per million (ppm) in the preindustrial era to the present 395 ppm . This increase is attributed to combustion of carbon based fuels, cement manufacturing, deforestation, burning of biomass, and land-use conversion, including soil tillage and animal husbandry. Soil C capture and storage is gaining global attention because of its role as a long-term C reservoir, low cost, and environmentally friendly means to minimize climate change.
Soil C pool is the largest terrestrial C pool, constituting approximately two-thirds of the total C in ecosystems . It is estimated at 2500 Pg to 1-m depth, with the biotic pool estimated at 560 Pg and characterized by fast turnover rates as compared to other natural compartments. The oceanic and geological pools are estimated at 39000 Pg and 5000–10000 Pg, respectively, whereas the atmospheric pool is estimated at 780 Pg . Therefore, total soil C pool is about 4, 1 times the biotic pool and 3 times the atmospheric pool.
Soil organic carbon (SOC) includes plant, animal, and microbial residues in all stages of decomposition. SOC represents a balance between inputs, mostly via primary productivity or organic amendments, and outputs via decomposition . Land application of organic amendments is a management practice that enhances SOC in the short term [7, 8]. In the last decades, the production of organic urban wastes such as biosolids has worldwide increased, and its accumulation, storage, and disposal pose growing environmental and socioeconomical problems. The safe disposal of biosolids has been a challenge for municipal wastewater treatment companies [9, 10]. In most countries, landfilling and land application have been the main disposal practices since they are the most economic outlet [11, 12]. However, sludge is a biodegradable material and releases CO2, CH4, and other gases when disposed in landfills . Biosolids are a valuable source of organic matter and plant nutrients, especially nitrogen (N) and phosphorus (P) . Recycling biosolids to agricultural land completes natural nutrient cycles. Besides, repeated land application of biosolids provides long-term benefits by increasing soil organic matter which, in turn, improves soil chemical and biological fertility [15–17]. Land application of biosolids may also result in a decrease in bulk density, increase in pore size, soil aeration, root penetrability, soil water holding capacity, and biological activity, all of which may be reflected in an increase in crop yields . One of the main disadvantages of land application of biosolids is the fact that it may contain human pathogens and trace elements, including arsenic, cadmium, zinc, copper, chromium, lead, mercury, nickel, and selenium [19–21]. The concentration of these compounds and concerns about nitrate leaching or losses to the atmosphere may limit biosolids land application [22, 23].
Soil C sequestration is defined as any persistent increase in SOC originated from removing CO2 from the atmosphere. Increases in soil carbon storage may be accomplished by the production of more biomass. In this way, there is a net transfer of atmospheric CO2 into the soil C pool through the humification of crop residues, resulting in net carbon sequestration . Powlson et al.  postulated that whether SOC increases produced by applying organic residues constitute C sequestration entirely depend on the alternative fate of this material. For example, biosolids soil application represents additional carbon retention in soil if the alternative disposal method is landfilling. On the contrary, if organic wastes are regularly land applied, increases in SOC resulting from biosolids application cannot be regarded as a waste management practice to mitigate climate change. Although many studies have examined the potential value of biosolids to increase soil productivity, relatively limited work has examined its effect on soil C sequestration [8, 26, 27].
2. Biosolids-Borne C Sequestration Capacity of Soils
2.1. Agricultural Soils
Soil C sequestration capacity reflects soil aptitude to retain and stabilize C. In the light of global change scenario, soil humification mechanisms have acquired renewed interest. Traditionally, the stability of organic compounds has been regarded as the main process controlling SOC retention, but recent analytical and experimental advances have demonstrated that molecular structure alone does not explain SOM stability . The amount of SOC accumulated does not only depend on the quantity and quality of the organic inputs, but on the physicochemical and biological influence of the environment as well [28, 29]. Various mechanisms of SOM stabilization have been proposed . Physical protection by incorporation into soil aggregates or by occlusion in micropores inaccessible to soil microorganisms or chemical protection through interaction with mineral surfaces is considered important mechanisms to reduce the bioavailability and accessibility of SOM for soil microorganisms or hydrolytic soil enzymes . Another mechanism of SOC stabilization is assumed to be biochemical protection. Biotic organic C is biologically transformed by the action of microbial populations (i.e., bacteria, fungi) and invertebrates, resulting in acquired chemical stability . Therefore, the residence time of organic compounds in soils is directly related to intrinsic or developed resistance to further microbiological degradation.
Biosolids are typically made up of 40–70% organic matter, with organic C content ranging from 20–50%, total nitrogen (N) ranging from 2–5%, and a C/N ratio of about 10–20 [32, 33]. Biosolids’ organic matter has usually undergone some degree of stabilization through anaerobic or aerobic digestion before being land applied. Long- and short- term observations have demonstrated that biosolids amended soils accumulate a significantly higher amount of organic C compared to mineral fertilized soils. Over a 34-year reclamation experiment, Tian et al.  reported that soil C sequestration capacity in agricultural soils under conventional tillage was significantly correlated with biosolids application rate. In the short term, Torri et al.  reported soil C accumulation in three pristine representative soils of the Pampas region, Argentina, amended with high biosolids rate. These soils had different particle size distribution, although the clay fraction had the same origin and mineralogical composition. During the 30 days following biosolids incorporation, decomposition mechanisms associated with an intense biological activity originated a rapid CO2-C release . After 150 days, the three pristine amended soils appeared to reach a new equilibrium, with C contents being significantly higher than the respective controls. Total C content did not change significantly between days 150 and 360 in the three studied soils, showing the potential of these soils to store biosolids-borne C (Figure 1).
Many mathematical models have been proposed to describe the decomposition process of land applied organic materials, ranging from one to multicompartment models [29, 36, 37]. In the study made by Torri et al. , a first-order exponential model provided the best fit to C mineralization data for the three soils (1): where %CB is the percent residual C from biosolids in soil; %CLB the initial percent of biosolids borne-C in the labile pool; %CRB the percent of biosolids borne-C in the resistant pool; is the first order rate constant (day− 1); is the time after biosolids application (days).
According to this model, organic C added through biosolids consisted of two fractions of different degree of biodegradability: a labile fraction (53–71%) that was quickly mineralized at a constant rate () and a recalcitrant fraction (28.5–45.4%), not available or resistant to soil microorganisms that remained in the soils one year after biosolids application . Organic compounds of the recalcitrant fraction are mainly stable cholestane-based sterols  which may have a turnover rate in the order of hundreds of years . The labile organic fraction has often been found to be largely dependent on the degree of biosolids stabilization .
In general, C mineralization rates of freshly added organic sources have been found to be more rapid in soils with low than with high clay content . An explanation to this could be that residual substrate and decomposition products become stabilized by sorption onto mineral clay particles, by incorporation into pores that are too small for bacteria or fungi to penetrate. Consequently, they are physically inaccessible to microbial turnover [42, 43]. Furthermore, organic matter may be protected against decomposition as a result of being inside large aggregates that become partially anaerobic because of slow O2 diffusion through the small intra-aggregate pores .
Despite the protection provided by clay particles, many studies reported that mineralization rates of biosolids-borne C were not related to soil texture . Strong et al.  indicated that clay protects the organic matter which had time to become entangled in the soil matrix, although this may not happen if a great volume of fresh material is added. Moreover, the turnover of organic matter in soils of different texture was better explained by other soil parameters, such as temperature, moisture, pH, redox condition, and nutrient availability [46–50]. In the study of Torri et al. , the water content of the three studied soils was periodically adjusted according to water holding capacity and did not limit microbial activity. In this case, soil pH was the dominant variable on soil decomposition of biosolids. Most studies reported that acidic pH delayed the decomposition of soil organic matter because of its profound influence on biomass, activity, and composition of the soil microbial community [51, 52]. The higher pH of the Natraquoll stimulated microbial activity, increasing carbon mineralization of incorporated biosolids, whereas slightly acidic soils retained more biosolids-borne C (Figure 1).
In turn, the effects of microbes on composition and recalcitrance of SOC have been shown to be as important as climatic and edaphic characteristics . Soil aggregates are held together by mucilages and by fungal hyphae, roots, and polysaccharides. Increased amounts of any of these agents would promote the formation of macroaggregates, which, after further decomposition, form the stable and more resistant core of microaggregates [54, 55].
X-ray fluorescence analysis of dried sludge indicated that oxides of Si, Al, and Fe were the three main inorganic constituents of biosolids [7, 56]. X-ray diffraction analysis of biosolids performed by a number of researchers also indicated the presence of quartz, feldspars, kaolinite, mica, and expandable clays [57, 58]. In Figure 2(a), the scanning electron microscopy with X-ray microanalysis (SEM-EDS) image of a biosolids sample showed the presence of both organic and inorganic phases . The inorganic phase included silica, Fe, Al, and calcium compounds (Figure 2(b)). Taking into account that soil organic matter carries negative charges, whereas Fe oxides have positive ones, under certain conditions both of them may be intimately associated . Biosolids-borne amorphous iron and aluminum oxides would promote SOM stabilization after biosolids application [60, 61]. Amorphous Fe and Al oxides are very reactive due to their small size and high surface area. These reactive surfaces are often presumed to account for sorption and stabilization of OM . More recent research has suggested that stabilization mechanisms include ternary C - Fe oxide - clay associations  and the formation of unidentified chemical bonds . Lines of evidences that the association of organic matter with secondary hydrous Fe and Al phases would prevent SOC degradation have been published [65, 66]. Taking into account that biosolids are rich in amorphous Fe/Al oxides [60, 67], long-term biosolids application could increase soil amorphous Fe/Al, leading to increased SOM stability.
Some authors indicated that “the capacity of terrestrial ecosystems to store carbon is finite and the current sequestration potential primarily reflects depletion due to past land use” . However, recalcitrant organic carbon and amorphous Fe/Al oxides are land applied through biosolids amendments. The presence of Fe/Al oxides has been shown to stabilize soil organic matter and, likely, biosolids borne organic matter . Moreover, Kögel-Knabner et al.  suggested that one possible reason for soil C immobilization in these soil amendments could be its adsorption or complexation by Fe and Al cations. These results may indicate that, with time, biosolids amended soils would be able to store more carbon than the one depleted due to past land use. Nevertheless, this hypothesis requires further investigation.
2.2. Opencast Mine Sites
In recent years, there has been growing evidence that biosolids may be used to restore mine spoils or tailings. Rehabilitation of rocky materials exposed by mining typically involves physical amelioration and organic matter incorporation. The use of biosolids in such operations represents an opportunity to couple biosolids application with soil C sequestration. In several cases, this practice has led to high soil C accumulation, edaphic improvement, and an effective vegetation cover establishment [70, 71]. Furthermore, organic matter inputs and revegetation lead to humus accumulation and pedogenesis, including soil profile development [70, 72–74]. As the system evolved, grasses progressively dominated and represented the most important source of SOC in biosolids amended soils . After a decade of biosolids incorporation, SOC reached concentrations comparable to those found in hydromorphic soils and about twice those of undisturbed mineral soils under primary forests .
Mined spoils in tropical regions present factors that can accelerate C flow, such as high temperatures, acidity, and low charges surfaces, and factors that may retard it, like clay texture, overburden materials, and anaerobic conditions due to waterlogging. Carbon accumulation in revegetated mining spoils suggests that retarding factors have prevailed under stripped soil situation. Common inorganic components present in mining spoils include aluminosilicates (allophone and imogolite) and Fe-(oxy) hydroxides (like ferrihydrite). Both of them have been reported to stabilize soil C [75, 76]. Since vegetation coverage is usually established on low-permeable rocky material in mining sites, roots are usually subjected to waterlogging, leading to SOC accumulation . Several hypotheses about deleterious effects on soil microbial activity by compounds formed under anaerobiosis, such as volatile fatty acids, H2S, and toxic concentrations of NH3, Al, Fe, and other elements, have been postulated .
Although mining spoils are not a suitable environment for plant development, the incorporation of biosolids has promoted plant colonization and unprecedented organic-C accumulation was reported in temperate and tropical regions [70, 79]. Depending on site management, Shrestha and Lal  estimated that C sequestration rates for reclaimed mine soils could be in the order of 0.1–3.1 and 0.7–4 Mg ha−1 y−1. Scaling up such figures, mining site restoration could account for ≈16 Tg CO2 per year .
3. Biological Regulation of C Storage in Biosolids Amended Soils
Soil organic C dynamic depends on microbial activity, community composition, and soil enzyme activity . While incorporation rates and quality are relevant factors controlling soil organic C inputs, land application of biosolids may change the activity and diversity of soil microbial communities [82, 83]. Consequently, the use of biosolids as a soil amendment may have variable effects on soil C retention.
3.1. Microbial Activity
Most of the existing information on soil microbial responses due to biosolids incorporation is related to the use of sewage sludge [84–86]. Contrasting responses—from stimulation to inhibition—have been reported. These results reflect the large variability of sludge chemical composition and the level of resolution of the biological studies (i.e., biochemical or biomolecular) [87–89].
In most soils, microbial activity and proliferation is typically C-limited whereas N limitation hardly occurs . Biosolids application modifies soil main regulating parameters, particularly the nutrient stoichiometry. Sludge incorporation into soils provides labile C that produces a large initial C-CO2 flush due to rapid labile organic matter decomposition and microbial growth. This respiratory response is known as the “C dominated phase” (Figure 3) and is invariably bell-shaped. The shape of the curve is generally related to N availability, the quality of biosolids’ organic matter, and the release of trace elements or organic pollutants through biosolids decomposition . On the contrary, soil application of composted or thermally dried sludge may reduce soil microorganisms decomposition rates due to the higher proportion of recalcitrant C added .
Before the onset of CO2 release, an increase in the lag time may be observed in sludge amended soils . The lag phase allows the adaptation required for bacterial cells to begin to exploit new environmental conditions  and has been suggested to be a sensitive microbial indicator of soil metal pollution . Sludges with high content of trace elements may result in a longer “lag phase,” as depicted in Figure 3. However, this may not be a universal microbial response .
There is still considerable controversy about the effects of biosolids applications on the native SOC pool . Some authors reported that the strong microbial activity induced by the application of biosolids with high contents of labile organic substances would mineralize native SOC . This effect was mainly noticed when biosolids were applied to soils containing high initial levels of SOC, a phenomenon known as priming effect . Conversely, the application of the same amount and type of biosolids in soils with low levels of initial SOC contributed, in general, to an increase in the short-term SOC pool. An explanation to this was the low density of microbial communities in soils with low organic matter content. Although positive and negative priming effects have been reported, the latter does not always result in reduced soil C storage capacity. In general, the amount of added organic amendment entirely compensates the priming-induced C loss . Soil microorganisms can be triggered into activity by the availability of water and nutrients such as those present in the root exudates , and therefore these factors are important covariates to be accounted for assessing the biological control of biosolids soil C storage. Theoretically, C storage is achievable when the metabolic energy required to decompose biosolids-borne organic substrates is larger than the energy obtained by catabolism within microbial cells.
Soil management practices may influence soil C storage after biosolids amendment. It has been widely reported that intensity of mineralization processes is much higher in soil surface layers than in deepest soil horizons . However, root exudates or decomposition of root litter in subsurface horizons may induce priming effects that may, in turn, enhance the decomposition of biosolids-borne organic C. Low molecular weight organic compounds present in root exudates support large microbial biomass in the rhizosphere and induce SOM mineralization [99, 100]. Therefore, the current information on the priming effects on native SOM cannot be extended to biosolid amended soils. The reason for this is that the overall effects will not only depend on soil’s characteristics and basal microbial activity, but on the nature of nutrient inputs as well. Therefore, the biosolid-borne C storage capacity of soils will depend on the site specific equilibrium between C inputs and outputs, regulated by mineralization processes. Nevertheless, it is undisputable that, on the long term, biosolids amended soils retain more C than soils under conventional agricultural regime in different tillage, fertilization, and rotational schemes . The same applies for marginal and degraded soils .
3.2. Soil Enzyme Activity
Soil enzyme activity is responsible for most of the soil functionality, as it promotes the decomposition of organic matter and release nutrients in forms available to plants and microorganisms. Soil enzymes are actively released by proliferating soil microorganisms, plant roots, and soil fauna or passively released by dead microorganisms and root cell sloughing. A large fraction of the enzymes released in the extra- or pericellular space are stabilized by stable soil organic and inorganic phases , which protect them from soil proteolytic activity . Biosolids amendments play a dual role on soil enzyme activity: biosolids may increase the stabilization of extracellular enzymes through their solid phase surface properties or they may provide substrates (i.e., proteins and peptides) for soils enzymes, leading to microbial proliferation and the increase of enzymatic activity. This aspect is important for the long term of biosolids-borne C storage in soils because the presence of active enzymes reduces energy barrier to the decomposition of complex organic substrates thus facilitating the biosolids matrix mineralization without new and metabolically expensive synthesis of extracellular enzymes . This may produce a long-term positive feedback effect on soil microbial activity after amendment (Figure 4).
In any case, the presence of soil stabilized “enzymatic background” makes soil’s decomposition capacity only partially related to the actual levels of microbial activity in biosolids amended soils. As it is currently impossible to estimate the ratio between intra- and extracellular enzyme activity, it is not possible to precisely determine the actual contribution of active microorganisms to biosolids degradation.
In the light of global change scenario, increasing soil organic matter stocks has been identified as a feasible way for soil C sequestration. Many experiments indicated that application of biosolids to land or opencast mines resulted in an increase in carbon reserves of soils from different regions and under different management practices. Biosolids are typically made up of 40–70% organic matter, consisting of two fractions of different degree of biodegradability: a labile fraction that is quickly mineralized by soil microorganisms and a recalcitrant fraction, not available or resistant to soil microorganisms, responsible for soil organic carbon accumulation. The amount and proportion of recalcitrant C in biosolids are important attributes to predict the biological control of C storage in soils. It seems to be a direct relationship between C recalcitrance and mineralization: the higher the C recalcitrance in biosolids amended soils, the higher the metabolic energy needed for biosolids mineralization by soil microorganims. Monitoring microbial communities and soil enzyme activity may be used as ecological indicators of biosolids C stabilization in soil.
Many studies reported that mineralization rates of biosolids-borne C may not depend on soil texture and that slightly acid soils retained more biosolids-borne carbon than soils with a higher pH. Furthermore, amorphous iron and aluminum oxides usually found in biosolids would play an important role in soil organic C accumulation. Therefore, the capacity of soils to sequester biosolids borne C may not be finite. It is important to remark that the benefits associated with the use of biosolids for soil carbon sequestration are in addition to other benefits, like the improvement of soil quality in terms of physical, chemical and biological fertility, although the presence of contaminants may impact soil microbial communities on the long term.
Conflict of Interests
The authors declare that there is no conflict of interests regarding the publication of this paper.
The research leading to this review has received funding from UBACYT 20620110200024, GEF UBA, and The Brazilian National Council for Scientific and Technological Development (CNPq).
WMO, Greenhouse Gas Bulletin, World Meteorological Organization, Geneva, Switzerland, 2009.
P. N. Pearson and M. R. Palmer, “Atmospheric carbon dioxide concentrations over the past 60 million years,” Nature, vol. 406, no. 6797, pp. 695–699, 2000.View at: Publisher Site | Google Scholar
M. Czaun, A. Goeppert, R. B. May et al., “Organoamines-grafted on nano-sized silica for carbon dioxide capture,” Journal of CO2 Utilization, vol. 1, pp. 1–7, 2013.View at: Publisher Site | Google Scholar
D. S. Schimel, B. H. Braswell, and E. A. Holland, “Climatic, edaphic, and biotic controls over storage and turnover of carbon in soils,” Global Biogeochemical Cycles, vol. 8, no. 3, pp. 279–293, 1994.View at: Google Scholar
R. Lal, “Managing soils and ecosystems for mitigating anthropogenic carbon emissions and advancing global food security,” BioScience, vol. 60, no. 9, pp. 708–721, 2010.View at: Publisher Site | Google Scholar
R. Amundson, “The carbon budget in soils,” Annual Review of Earth and Planetary Sciences, vol. 29, pp. 535–562, 2001.View at: Publisher Site | Google Scholar
S. Torri and R. Lavado, “Carbon sequestration through the use of biosolids in soils of the Pampas region, Argentina,” in Environmental Management: Systems, Sustainability and Current Issues, H. C. Dupont, Ed., pp. 221–336, Nova Science, Hauppauge, NY, USA, 2011.View at: Google Scholar
G. Tian, T. C. Granato, A. E. Cox, R. I. Pietz, C. R. Carlson Jr., and Z. Abedin, “Soil carbon sequestration resulting from long-term application of biosolids for land reclamation,” Journal of Environmental Quality, vol. 38, no. 1, pp. 61–74, 2009.View at: Publisher Site | Google Scholar
L. Giusti, “A review of waste management practices and their impact on human health,” Waste Management, vol. 29, no. 8, pp. 2227–2239, 2009.View at: Publisher Site | Google Scholar
N.-Y. Wang, C.-H. Shih, P.-T. Chiueh, and Y.-F. Huang, “Environmental effects of sewage sludge carbonization and other treatment alternatives,” Energies, vol. 6, no. 2, pp. 871–883, 2013.View at: Publisher Site | Google Scholar
J. Hong, M. Otaki, and O. Jolliet, “Environmental and economic life cycle assessment for sewage sludge treatment processes in Japan,” Waste Management, vol. 29, no. 2, pp. 696–703, 2009.View at: Publisher Site | Google Scholar
E. Ramlal, D. Yemshanov, G. Fox, and D. McKenney, “A bioeconomic model of afforestation in Southern Ontario: integration of fiber, carbon and municipal biosolids values,” Journal of Environmental Management, vol. 90, no. 5, pp. 1833–1843, 2009.View at: Publisher Site | Google Scholar
O. Ayalon, Y. Avnimelech, and M. Shechter, “Solid waste treatment as a high-priority and low-cost alternative for greenhouse gas mitigation,” Environmental Management, vol. 27, no. 5, pp. 697–704, 2001.View at: Publisher Site | Google Scholar
R. S. Corrêa, R. E. White, and A. J. Weatherley, “Biosolids effectiveness to yield ryegrass based on their nitrogen content,” Scientia Agricola, vol. 62, no. 3, pp. 274–280, 2005.View at: Google Scholar
C. G. Cogger, A. I. Bary, E. A. Myhre, and A. Fortuna, “Biosolids applications to tall fescue have long-term influence on soil nitrogen, carbon, and phosphorus,” Journal of Environmental Quality, vol. 42, pp. 516–522, 2013.View at: Publisher Site | Google Scholar
F. J. Larney and D. A. Angers, “The role of organic amendments in soil reclamation: a review,” Canadian Journal of Soil Science, vol. 92, no. 1, pp. 19–38, 2012.View at: Publisher Site | Google Scholar
P. E. Wiseman, S. D. Day, and J. R. Harris, “Organic amendment effects on soil carbon and microbial biomass in the root zone of three landscape tree species,” Arboriculture & Urban Forestry, vol. 38, no. 6, pp. 262–276, 2012.View at: Google Scholar
K. Barbarick, K. Doxtader, E. Redente, and R. Brobst, “Biosolids effects on microbial activity in shrubland and grassland soils,” Soil Science, vol. 169, no. 3, pp. 176–187, 2004.View at: Google Scholar
W. E. Cotching and J. R. Coad, “Metal element uptake in vegetables and wheat after biosolids application,” Journal of Solid Waste Technology and Management, vol. 37, no. 2, pp. 75–82, 2011.View at: Publisher Site | Google Scholar
M. J. Mcfarland, K. Kumarsamy, R. B. Brobst, A. Hais, and M. D. Schmitz, “Groundwater quality protection at biosolids land application sites,” Water Research, vol. 46, no. 18, pp. 5963–5969, 2012.View at: Publisher Site | Google Scholar
K. R. Islam, S. Ahsan, K. Barik, and E. L. Aksakal, “Biosolid impact on heavy metal accumulation and lability in soiln under alternate-year no-till corn—soybean rotation,” Water, Air, & Soil Pollution, vol. 224, pp. 1451–1461, 2013.View at: Publisher Site | Google Scholar
EU, “3rd Working Document of the EU Commission on Sludge Management,” ENV.E3/LM, Brussels, Belgium, 2000.View at: Google Scholar
G. Pu, M. Bell, G. Barry, and P. Want, “Estimating mineralisation of organic nitrogen from biosolids and other organic wastes applied to soils in subtropical Australia,” Soil Research, vol. 50, no. 2, pp. 91–104, 2012.View at: Publisher Site | Google Scholar
R. Lal, “Carbon management in agricultural soils,” Mitigation and Adaptation Strategies for Global Change, vol. 12, no. 2, pp. 303–322, 2007.View at: Publisher Site | Google Scholar
D. S. Powlson, A. P. Whitmore, and K. W. T. Goulding, “Soil carbon sequestration to mitigate climate change: a critical re-examination to identify the true and the false,” European Journal of Soil Science, vol. 62, no. 1, pp. 42–55, 2011.View at: Publisher Site | Google Scholar
C. Feller and M. Bernoux, “Historical advances in the study of global terrestrial soil organic carbon sequestration,” Waste Management, vol. 28, no. 4, pp. 734–740, 2008.View at: Publisher Site | Google Scholar
B. Marschner, S. Brodowski, A. Dreves et al., “How relevant is recalcitrance for the stabilization of organic matter in soils?” Journal of Plant Nutrition and Soil Science, vol. 171, no. 1, pp. 91–110, 2008.View at: Publisher Site | Google Scholar
M. W. I. Schmidt, M. S. Torn, S. Abiven et al., “Persistence of soil organic matter as an ecosystem property,” Nature, vol. 478, no. 7367, pp. 49–56, 2011.View at: Publisher Site | Google Scholar
M. Pansu, P. Bottner, L. Sarmiento, and K. Metselaar, “Comparison of five soil organic matter decomposition models using data from a 14C and 15N labeling field experiment,” Global Biogeochemical Cycles, vol. 18, no. 4, 2004.View at: Publisher Site | Google Scholar
P. Puget, C. Chenu, and J. Balesdent, “Dynamics of soil organic matter associated with particle-size fractions of water-stable aggregates,” European Journal of Soil Science, vol. 51, no. 4, pp. 595–605, 2000.View at: Publisher Site | Google Scholar
B. T. Christensen, “Physical fractionation of soil and structural and functional complexity in organic matter turnover,” European Journal of Soil Science, vol. 52, no. 3, pp. 345–353, 2001.View at: Publisher Site | Google Scholar
S. I. Torri, Distribution and availability of Cd, Cu, Pb y Zn in sewage sludge amended soils [M Sci. Dissertation], University of Buenos Aires, Faculty of Agronomy, Buenos Aires, Argentina, 2001.
E. Alonso, I. Aparicio, J. L. Santos, P. Villar, and A. Santos, “Sequential extraction of metals from mixed and digested sludge from aerobic WWTPs sited in the south of Spain,” Waste Management, vol. 29, no. 1, pp. 418–424, 2009.View at: Publisher Site | Google Scholar
S. Torri, R. Alvarez, and R. Lavado, “Mineralization of carbon from sewage sludge in three soils of the Argentine pampas,” Communications in Soil Science and Plant Analysis, vol. 34, no. 13-14, pp. 2035–2043, 2003.View at: Google Scholar
K. Lorenz, R. Lal, C. M. Preston, and K. G. J. Nierop, “Strengthening the soil organic carbon pool by increasing contributions from recalcitrant aliphatic bio(macro)molecules,” Geoderma, vol. 142, no. 1-2, pp. 1–10, 2007.View at: Publisher Site | Google Scholar
L. Thuriès, M. Pansu, C. Feller, P. Herrmann, and J.-C. Rémy, “Kinetics of added organic matter decomposition in a Mediterranean sandy soil,” Soil Biology & Biochemistry, vol. 33, no. 7-8, pp. 997–1010, 2001.View at: Publisher Site | Google Scholar
S. Manzoni, J. A. Trofymow, R. B. Jackson, and A. Porporato, “Stoichiometric controls on carbon, nitrogen, and phosphorus dynamics in decomposing litter,” Ecological Monographs, vol. 80, no. 1, pp. 89–106, 2010.View at: Publisher Site | Google Scholar
S. I. Torri and C. Alberti, “Characterization of organic compounds from biosolids of Buenos Aires city,” Journal of Soil Science and Plant Nutrition, vol. 12, no. 1, pp. 143–152, 2012.View at: Publisher Site | Google Scholar
R. E. Terry, D. W. Nelson, and L. E. Sommers, “Carbon cycling during sewage sludge decomposition in soils,” Soil Science Society of America Journal, vol. 43, no. 3, pp. 494–499, 1979.View at: Publisher Site | Google Scholar
R. S. Corrêa, R. E. White, and A. J. Weatherley, “Effects of sewage sludge stabilization on organic-N mineralization in two soils,” Soil Use and Management, vol. 28, no. 1, pp. 12–18, 2012.View at: Publisher Site | Google Scholar
R. Merckx, A. den Hartog, and J. A. van Veen, “Turnover of root-derived material and related microbial biomass formation in soils of different texture,” Soil Biology & Biochemistry, vol. 17, no. 4, pp. 565–569, 1985.View at: Google Scholar
B. T. Christensen, “Carbon in primary and secondary organomineral complexes,” in Advances in Soil Science Structure and Organic Matter Storage in Agricultural Soils, M. R. Carter and B. A. Stewart, Eds., pp. 97–165, CRC Lewis, Boca Raton, Fla, USA, 1996.View at: Google Scholar
F. J. Matus and R. C. Maire, “Interaction between soil organic matter, soil texture and the mineralization rates of carbon and nitrogen,” Agricultura Técnica, vol. 60, pp. 112–126, 2000.View at: Google Scholar
M. B. Jones, “Potential for carbon sequestration in temperate grassland soils,” in Grassland Carbon Sequestration: Management, Policy and Economics, M. Abberton, R. Conant, and C. Batello, Eds., Food and Agriculture Organization of the United Nations, Rome, Italy, 2010.View at: Google Scholar
D. T. Strong, P. G. Sale, and K. R. Helyar, “The influence of the soil matrix on nitrogen mineralisation and nitrification. IV. Texture,” Australian Journal of Soil Research, vol. 37, no. 2, pp. 329–344, 1999.View at: Google Scholar
I. Thomsen, P. Schjonning, B. Jensen, K. Kristensen, and B. T. Christensen, “Turnover of organic matter in differently textured soils. II. Microbial activity as influenced by soil water regimes,” Geoderma, vol. 89, no. 3-4, pp. 199–218, 1999.View at: Publisher Site | Google Scholar
S. Wan, R. J. Norby, J. Ledford, and J. F. Weltzin, “Responses of soil respiration to elevated CO2, air warming, and changing soil water availability in a model old-field grassland,” Global Change Biology, vol. 13, no. 11, pp. 2411–2424, 2007.View at: Publisher Site | Google Scholar
K. M. Batten, K. M. Scow, K. F. Davies, and S. P. Harrison, “Two invasive plants alter soil microbial community composition in serpentine grasslands,” Biological Invasions, vol. 8, no. 2, pp. 217–230, 2006.View at: Publisher Site | Google Scholar
Z.-F. Xu, R. Hu, P. Xiong, C. Wan, G. Cao, and Q. Liu, “Initial soil responses to experimental warming in two contrasting forest ecosystems, Eastern Tibetan Plateau, China: nutrient availabilities, microbial properties and enzyme activities,” Applied Soil Ecology, vol. 46, no. 2, pp. 291–299, 2010.View at: Publisher Site | Google Scholar
R. D. de Laune, C. N. Reddy, and W. H. Patrick Jr., “Organic matter decomposition in soil as influenced by pH and redox conditions,” Soil Biology & Biochemistry, vol. 13, no. 6, pp. 533–534, 1981.View at: Google Scholar
A. Saviozzi, G. Vanni, and R. Cardelli, “Carbon mineralization kinetics in soils under urban environment,” Applied Soil Ecology, vol. 73, pp. 64–69, 2014.View at: Publisher Site | Google Scholar
J. Rousk, P. C. Brookes, and E. Bååth, “Contrasting soil pH effects on fungal and bacterial growth suggest functional redundancy in carbon mineralization,” Applied and Environmental Microbiology, vol. 75, no. 6, pp. 1589–1596, 2009.View at: Publisher Site | Google Scholar
H. M. Throckmorton, J. A. Bird, L. Dane, M. K. Firestone, W. R. Horwath, and E. Cleland, “The source of microbial C has little impact on soil organic matter stabilisation in forest ecosystems,” Ecology Letters, vol. 15, no. 11, pp. 1257–1265, 2012.View at: Publisher Site | Google Scholar
J. Six, H. Bossuyt, S. Degryze, and K. Denef, “A history of research on the link between (micro)aggregates, soil biota, and soil organic matter dynamics,” Soil and Tillage Research, vol. 79, no. 1, pp. 7–31, 2004.View at: Publisher Site | Google Scholar
L. Vidal-Beaudet, C. Grosbelle, V. Forget-Caubel, and S. Charpentier, “Modelling long-term carbon dynamics in soils reconstituted with large quantities of organic matter,” European Journal of Soil Science, vol. 63, no. 6, pp. 787–797, 2012.View at: Publisher Site | Google Scholar
U. Thawornchaisit and K. Pakulanon, “Application of dried sewage sludge as phenol biosorbent,” Bioresource Technology, vol. 98, no. 1, pp. 140–144, 2007.View at: Publisher Site | Google Scholar
W. F. Jaynes and R. E. Zartman, “Origin of talc, iron phosphates, and other minerals in biosolids,” Soil Science Society of America Journal, vol. 69, no. 4, pp. 1047–1056, 2005.View at: Publisher Site | Google Scholar
K. J. Mun, N. W. Choi, and Y. S. Soh, “Feasibility study of lightweight aggregates using sewage sludge for non-structural concrete,” in RILEM International Symposium on Envronment-Conscious Materials and Systems, N. Kashino and Y. Ohama, Eds., pp. 155–162, RILEM, Bagneux, France, 2005.View at: Google Scholar
M. Kleber, R. Mikutta, M. S. Torn, and R. Jahn, “Poorly crystalline mineral phases protect organic matter in acid subsoil horizons,” European Journal of Soil Science, vol. 56, no. 6, pp. 717–725, 2005.View at: Publisher Site | Google Scholar
G. Tian, A. J. Franzluebbers, T. C. Granato, A. E. Cox, and C. O'connor, “Stability of soil organic matter under long-term biosolids application,” Applied Soil Ecology, vol. 64, pp. 223–227, 2013.View at: Publisher Site | Google Scholar
R. Mikutta, M. Kleber, M. S. Torn, and R. Jahn, “Stabilization of soil organic matter: association with minerals or chemical recalcitrance?” Biogeochemistry, vol. 77, no. 1, pp. 25–56, 2006.View at: Publisher Site | Google Scholar
K. Kaiser and G. Guggenberger, “The role of DOM sorption to mineral surfaces in the preservation of organic matter in soils,” Organic Geochemistry, vol. 31, no. 7-8, pp. 711–725, 2000.View at: Publisher Site | Google Scholar
R. Wagai and L. M. Mayer, “Sorptive stabilization of organic matter in soils by hydrous iron oxides,” Geochimica et Cosmochimica Acta, vol. 71, no. 1, pp. 25–35, 2007.View at: Publisher Site | Google Scholar
S. Spielvogel, J. Prietzel, and I. Kögel-Knabner, “Soil organic matter stabilization in acidic forest soils is preferential and soil type-specific,” European Journal of Soil Science, vol. 59, no. 4, pp. 674–692, 2008.View at: Publisher Site | Google Scholar
K. Kaiser, K. Eusterhues, C. Rumpel, G. Guggenberger, and I. Kögel-Knabner, “Stabilization of organic matter by soil minerals-investigations of density and particle-size fractions from two acid forest soils,” Journal of Plant Nutrition and Soil Science, vol. 165, no. 4, pp. 451–459, 2002.View at: Google Scholar
T. Chevallier, T. Woignier, J. Toucet, E. Blanchart, and P. Dieudonné, “Fractal structure in natural gels: effect on carbon sequestration in volcanic soils,” Journal of Sol-Gel Science and Technology, vol. 48, no. 1-2, pp. 231–238, 2008.View at: Publisher Site | Google Scholar
S. I. Torri and R. S. Lavado, “Dynamics of Cd, Cu and Pb added to soil through different kinds of sewage sludge,” Waste Management, vol. 28, no. 5, pp. 821–832, 2008.View at: Publisher Site | Google Scholar
B. Mackey, I. C. Prentice, W. Steffen et al., “Untangling the confusion around land carbon science and climate change mitigation policy,” Nature Climate Change, vol. 3, no. 6, pp. 552–557, 2013.View at: Publisher Site | Google Scholar
I. Kögel-Knabner, G. Guggenberger, M. Kleber et al., “Organo-mineral associations in temperate soils: integrating biology, mineralogy, and organic matter chemistry,” Journal of Plant Nutrition and Soil Science, vol. 171, no. 1, pp. 61–82, 2008.View at: Publisher Site | Google Scholar
L. C. R. Silva, R. S. Corrêa, T. A. Doane, E. I. P. Pereira, and W. R. Horwath, “Unprecedented carbon accumulation in mined soils: the synergistic effect of resource input and plant species invasion,” Ecological Applicatins, vol. 23, no. 6, pp. 1345–1356, 2013.View at: Publisher Site | Google Scholar
K. C. Haering, W. L. Daniels, and S. E. Feagly, “Reclaiming mined lands with biosolids, manures and papermill sludges,” in Re- Clamation of Drastically Disturbed Lands, R. Barnhisel, Ed., pp. 615–644, Soil Science Society of America, Madison, Wis, USA, 2000.View at: Google Scholar
P. R. Fresquez and W. C. Lindemann, “Soil and rhizosphere microorganisms in amended coal mine spoils,” Soil Science Society of America Journal, vol. 46, no. 4, pp. 751–755, 1982.View at: Google Scholar
H. F. Stroo and E. M. Jencks, “Effect of sewage sludge on microbial activity in an old, abandoned minesoil,” Journal of Environmental Quality, vol. 14, no. 3, pp. 301–304, 1985.View at: Google Scholar
G. Blaga, H. Banescu, L. Stefanescu et al., “Imbunatatirea ferilitatii protsolului antropic de la Capus (jud Cluj) prin utilizarea namolului orasenesc provenit de la statia de epurare a municipiului Cluj-Napoca,” Buletinul Institutului Agronomic Cluj-Napoca. Seria Agricultura si Horticultura, vol. 45, pp. 93–99, 1991.View at: Google Scholar
K. C. Haering, W. L. Daniels, and J. M. Galbraith, “Appalachian mine soil morphology and properties: effects of weathering and mining method,” Soil Science Society of America Journal, vol. 68, no. 4, pp. 1315–1325, 2004.View at: Google Scholar
J. A. Baldock and J. O. Skjemstad, “Role of the soil matrix and minerals in protecting natural organic materials against biological attack,” Organic Geochemistry, vol. 31, no. 7-8, pp. 697–710, 2000.View at: Publisher Site | Google Scholar
J. M. Oades, “The retention of organic matter in soils,” Biogeochemistry, vol. 5, no. 1, pp. 35–70, 1988.View at: Publisher Site | Google Scholar
K. L. Sahrawat, “Organic matter accumulation in submerged soils,” Advances in Agronomy, vol. 81, pp. 169–201, 2003.View at: Publisher Site | Google Scholar
G. Séré, C. Schwartz, S. Ouvrard, C. Sauvage, J.-C. Renat, and J. L. Morel, “Soil construction: a step for ecological reclamation of derelict lands,” Journal of Soils and Sediments, vol. 8, no. 2, pp. 130–136, 2008.View at: Publisher Site | Google Scholar
R. K. Shrestha and R. Lal, “Ecosystem carbon budgeting and soil carbon sequestration in reclaimed mine soil,” Environment International, vol. 32, no. 6, pp. 781–796, 2006.View at: Publisher Site | Google Scholar
P. Nannipieri, J. Ascher, M. T. Ceccherini, L. Landi, G. Pietramellara, and G. Renella, “Microbial diversity and soil functions,” European Journal of Soil Science, vol. 54, no. 4, pp. 655–670, 2003.View at: Publisher Site | Google Scholar
N. C. M. Gomes, L. Landi, K. Smalla, P. Nannipieri, P. C. Brookes, and G. Renella, “Effects of Cd- and Zn-enriched sewage sludge on soil bacterial and fungal communities,” Ecotoxicology and Environmental Safety, vol. 73, no. 6, pp. 1255–1263, 2010.View at: Publisher Site | Google Scholar
M. Ros, J. A. Pascual, C. Garcia, M. T. Hernandez, and H. Insam, “Hydrolase activities, microbial biomass and bacterial community in a soil after long-term amendment with different composts,” Soil Biology & Biochemistry, vol. 38, no. 12, pp. 3443–3452, 2006.View at: Publisher Site | Google Scholar
I. Jorge-Mardomingo, P. Soler-Rovira, M. T. Casermeiro, M. T. de la Cruz, and A. Polo, “Seasonal changes in microbial activity in a semiarid soil after application of a high dose of different organic amendments,” Geoderma, vol. 206, pp. 40–48, 2013.View at: Publisher Site | Google Scholar
J. Paz-Ferreiro, G. Gascó, B. Gutiérrez, and A. Méndez, “Soil biochemical activities and the geometric mean of enzyme activities after application of sewage sludge and sewage sludge biochar to soil,” Biology and Fertility of Soils, vol. 48, no. 5, pp. 511–517, 2012.View at: Publisher Site | Google Scholar
E. A. Guertal and B. D. Green, “Evaluation of organic fertilizer sources for south-eastern (USA) turfgrass maintenance,” Acta Agriculturae Scandinavica B, vol. 62, supplement 1, pp. 130–138, 2012.View at: Publisher Site | Google Scholar
G. Renella, A. M. Chaudri, C. M. Falloon, L. Landi, P. Nannipieri, and P. C. Brookes, “Effects of Cd, Zn, or both on soil microbial biomass and activity in a clay loam soil,” Biology and Fertility of Soils, vol. 43, no. 6, pp. 751–758, 2007.View at: Publisher Site | Google Scholar
N. C. M. Gomes, L. Landi, K. Smalla, P. Nannipieri, P. C. Brookes, and G. Renella, “Effects of Cd- and Zn-enriched sewage sludge on soil bacterial and fungal communities,” Ecotoxicology and Environmental Safety, vol. 73, no. 6, pp. 1255–1263, 2010.View at: Publisher Site | Google Scholar
X. Domene, W. Ramírez, S. Mattana, J. M. Alcañiz, and P. Andrés, “Ecological risk assessment of organic waste amendments using the species sensitivity distribution from a soil organisms test battery,” Environmental Pollution, vol. 155, no. 2, pp. 227–236, 2008.View at: Publisher Site | Google Scholar
L. Aldén, F. Demoling, and E. Bååth, “Rapid method of determining factors limiting bacterial growth in soil,” Applied and Environmental Microbiology, vol. 67, no. 4, pp. 1830–1838, 2001.View at: Publisher Site | Google Scholar
C. Palmborg and A. Nordgren, “Partitioning the variation of microbial measurements in forest soils into heavy metal and substrate quality dependent parts by use of near infrared spectroscopy and multivariate statistics,” Soil Biology & Biochemistry, vol. 28, no. 6, pp. 711–720, 1996.View at: Publisher Site | Google Scholar
M. T. Madigan, J. M. Martinko, and J. Parker, Eds., Brock Biology of Microorganisms, Prentice-Hall, Upper Saddle River, NJ, USA, 2000.
L. Haanstra and P. Doelman, “Glutamic acid decomposition as a sensitive measure of heavy metal pollution in soil,” Soil Biology & Biochemistry, vol. 16, no. 6, pp. 595–600, 1984.View at: Google Scholar
S. Dahlin, E. Witter, A. Mårtensson, A. Turner, and E. Bååth, “Where's the limit? Changes in the microbiological properties of agricultural soils at low levels of metal contamination,” Soil Biology & Biochemistry, vol. 29, no. 9-10, pp. 1405–1415, 1997.View at: Publisher Site | Google Scholar
S. K. Jones, R. M. Rees, D. Kosmas, B. C. Ball, and U. M. Skiba, “Carbon sequestration in a temperate grassland; management and climatic controls,” Soil Use and Management, vol. 22, no. 2, pp. 132–142, 2006.View at: Publisher Site | Google Scholar
J. M. Soriano-Disla, J. Navarro-Pedreño, and I. Gómez, “Contribution of a sewage sludge application to the short-term carbon sequestration across a wide range of agricultural soils,” Environmental Earth Sciences, vol. 61, no. 8, pp. 1613–1619, 2010.View at: Publisher Site | Google Scholar
J. W. Dalenberg and G. Jager, “Priming effect of some organic additions to 14C-labelled soil,” Soil Biology & Biochemistry, vol. 21, no. 3, pp. 443–448, 1989.View at: Google Scholar
G. Renella, L. Landi, F. Valori, and P. Nannipieri, “Microbial and hydrolase activity after release of low molecular weight organic compounds by a model root surface in a clayey and a sandy soil,” Applied Soil Ecology, vol. 36, no. 2-3, pp. 124–129, 2007.View at: Publisher Site | Google Scholar
S. Fontaine, S. Barot, P. Barré, N. Bdioui, B. Mary, and C. Rumpel, “Stability of organic carbon in deep soil layers controlled by fresh carbon supply,” Nature, vol. 450, no. 7167, pp. 277–280, 2007.View at: Publisher Site | Google Scholar
G. Renella, L. Landi, J. Ascher et al., “Long-term effects of aided phytostabilisation of trace elements on microbial biomass and activity, enzyme activities, and composition of microbial community in the Jales contaminated mine spoils,” Environmental Pollution, vol. 152, no. 3, pp. 702–712, 2008.View at: Publisher Site | Google Scholar
P. Rochette and E. G. Gregorich, “Dynamics of soil microbial biomass C, soluble organic C and CO2 evolution after three years of manure application,” Canadian Journal of Soil Science, vol. 78, no. 2, pp. 283–290, 1998.View at: Google Scholar
S. L. Brown, C. L. Henry, R. Chaney, H. Compton, and P. S. de Volder, “Using municipal biosolids in combination with other residuals to restore metal-contaminated mining areas,” Plant and Soil, vol. 249, no. 1, pp. 203–215, 2003.View at: Publisher Site | Google Scholar
R. G. Burns, “Enzyme activity in soil: location and a possible role in microbial ecology,” Soil Biology & Biochemistry, vol. 14, no. 5, pp. 423–427, 1982.View at: Google Scholar
G. Renella, L. Landi, and P. Nannipieri, “Hydrolase activities during and after the chloroform fumigation of soil as affected by protease activity,” Soil Biology & Biochemistry, vol. 34, no. 1, pp. 51–60, 2002.View at: Publisher Site | Google Scholar
J. P. Schimel and M. N. Weintraub, “The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model,” Soil Biology & Biochemistry, vol. 35, no. 4, pp. 549–563, 2003.View at: Publisher Site | Google Scholar