Moving beyond mass loss: advancing understanding about the fate of decomposing leaf litter and pyrogenic organic matter in the mineral soil

2014 Summer.Leaf litter decomposition recycles the energy and nutrients fixed by plants during net primary productivity back to the soil and atmosphere from where they came. Traditionally, leaf litter decomposition studies have focused on litter mass loss rates, without consideration for where that mass ends up in the ecosystem. However, during litter decomposition by soil microbes a fraction of the litter mass lost is truly lost to the ecosystem as respired CO2, while another fraction remains in the ecosystem stored in the soil as soil organic matter (SOM). SOM is heterogeneous in composition, with various SOM pools remaining stored in the soil for time spans ranging from days to millennia depending on their biochemical and physical properties. Pyrogenic organic matter (py-OM) is the partially combusted plant residue left behind by fires, and has been found to contribute to long term SOM pools. SOM accounts for the largest terrestrial pool of carbon (C) in the global C cycle and stores nitrogen (N) and other nutrients for plant productivity. Therefore the formation of SOM during litter decomposition is critical to terrestrial C and N cycling and its feedback to global biogeochemical cycles. The focus of my dissertation is the study of leaf litter and py-OM decomposition, and quantitatively tracing how much decomposing litter and py-OM is used by soil microbes, how much is lost as CO2, and how much remains in the soil and contributes to SOM formation under different conditions. In order to best address my research questions, I first studied the methods of leaching of dissolved organic carbon (DOC) and 13C and 15N isotope labeling of plant material in the laboratory. Then, I conducted a laboratory incubation where I found that the amount of hot water extractable C and the lignocellulose index (Lignin/(lignin+cellulose)) can be used to predict DOM leaching, and the partitioning of C loss between DOC and CO2 from leaves and py-OM during decomposition. I also conducted two field studies using 13C and 15N labeled Andropogon gerardii leaf litter and py-OM to trace the fate of C and N losses during their decomposition in a fire affected tallgrass prairie, and understand the role of soil microarthropods in this process. I found that soil microarthropods increase the amount of leaf litter C that contributes to stabilized SOM formation during litter decomposition, by increasing litter inputs to the soil where they can be utilized by soil microbes. Finally, I found that frequent inputs of py-OM, rather than litter, due to annual burning of the tallgrass prairie alters the SOM formation process by removing relatively labile litter inputs to the soil and replacing it with py-OM that is unusable by soil microbes. Overall, my dissertation has focused on taking a mechanistic approach to understanding the process of litter and py-OM decomposition, and how their decomposition contributes to SOM formation and ecosystem CO2 fluxes. My results have helped to improve our understanding of terrestrial biogeochemistry, and the processes that control SOM formation during litter decomposition

Conceptualizing soil organic matter into particulate and mineral-associated forms to address global change in the 21st century.

Managing soil organic matter (SOM) stocks to address global change challenges requires well-substantiated knowledge of SOM behavior that can be clearly communicated between scientists, management practitioners, and policy makers. However, SOM is incredibly complex and requires separation into multiple components with contrasting behavior in order to study and predict its dynamics. Numerous diverse SOM separation schemes are currently used, making cross-study comparisons difficult and hindering broad-scale generalizations. Here, we recommend separating SOM into particulate (POM) and mineral-associated (MAOM) forms, two SOM components that are fundamentally different in terms of their formation, persistence, and functioning. We provide evidence of their highly contrasting physical and chemical properties, mean residence times in soil, and responses to land use change, plant litter inputs, warming, CO2 enrichment, and N fertilization. Conceptualizing SOM into POM versus MAOM is a feasible, well-supported, and useful framework that will allow scientists to move beyond studies of bulk SOM, but also use a consistent separation scheme across studies. Ultimately, we propose the POM versus MAOM framework as the best way forward to understand and predict broad-scale SOM dynamics in the context of global change challenges and provide necessary recommendations to managers and policy makers

The role of microarthropods in emerging models of soil organic matter

A new understanding of soil organic matter (SOM) formation and stabilization has emerged over the past decade, highlighting the importance of microbial activity, mineral association of organic matter and aggregate occlusion of organic matter to SOM persistence. To date, the contribution of microarthropods to litter decomposition and SOM formation processes has not received due consideration and theoretical and empirical models should be modified to include how these organisms impact SOM protection. Here, we highlight the biological, chemical and physical mechanisms by which microarthropods influence SOM formation both directly and indirectly. Although more data is needed to quantify the impacts of different microarthropods on SOM dynamics, we highlight areas where inclusion of microarthropods in emerging models of SOM formation could reduce model uncertainties

Microbial carbon limitation : the need for integrating microorganisms into our understanding of ecosystem carbon cycling

Numerous studies have demonstrated that fertilization with nutrients such as nitrogen, phosphorus, and potassium increases plant productivity in both natural and managed ecosystems, demonstrating that primary productivity is nutrient limited in most terrestrial ecosystems. In contrast, it has been demonstrated that heterotrophic microbial communities in soil are primarily limited by organic carbon or energy. While this concept of contrasting limitations, that is, microbial carbon and plant nutrient limitation, is based on strong evidence that we review in this paper, it is often ignored in discussions of ecosystem response to global environment changes. The plant-centric perspective has equated plant nutrient limitations with those of whole ecosystems, thereby ignoring the important role of the heterotrophs responsible for soil decomposition in driving ecosystem carbon storage. To truly integrate carbon and nutrient cycles in ecosystem science, we must account for the fact that while plant productivity may be nutrient limited, the secondary productivity by heterotrophic communities is inherently carbon limited. Ecosystem carbon cycling integrates the independent physiological responses of its individual components, as well as tightly coupled exchanges between autotrophs and heterotrophs. To the extent that the interacting autotrophic and heterotrophic processes are controlled by organisms that are limited by nutrient versus carbon accessibility, respectively, we propose that ecosystems by definition cannot be 'limited' by nutrients or carbon alone. Here, we outline how models aimed at predicting non-steady state ecosystem responses over time can benefit from dissecting ecosystems into the organismal components and their inherent limitations to better represent plant-microbe interactions in coupled carbon and nutrient models

Whole-soil warming decreases abundance and modifies the community structure of microorganisms in the subsoil but not in surface soil

The microbial community composition in subsoils remains understudied, and it is largely unknown whether subsoil microorganisms show a similar response to global warming as microorganisms at the soil surface do. Since microorganisms are the key drivers of soil organic carbon decomposition, this knowledge gap causes uncertainty in the predictions of future carbon cycling in the subsoil carbon pool (> 50 % of the soil organic carbon stocks are below 30 cm soil depth). In the Blodgett Forest field warming experiment (California, USA) we investigated how +4 ∘C warming in the whole-soil profile to 100 cm soil depth for 4.5 years has affected the abundance and community structure of microorganisms. We used proxies for bulk microbial biomass carbon (MBC) and functional microbial groups based on lipid biomarkers, such as phospholipid fatty acids (PLFAs) and branched glycerol dialkyl glycerol tetraethers (brGDGTs). With depth, the microbial biomass decreased and the community composition changed. Our results show that the concentration of PLFAs decreased with warming in the subsoil (below 30 cm) by 28 % but was not affected in the topsoil. Phospholipid fatty acid concentrations changed in concert with soil organic carbon. The microbial community response to warming was depth dependent. The relative abundance of Actinobacteria increased in warmed subsoil, and Gram+ bacteria in subsoils adapted their cell membrane structure to warming-induced stress, as indicated by the ratio of anteiso to iso branched PLFAs. Our results show for the first time that subsoil microorganisms can be more affected by warming compared to topsoil microorganisms. These microbial responses could be explained by the observed decrease in subsoil organic carbon concentrations in the warmed plots. A decrease in microbial abundance in warmed subsoils might reduce the magnitude of the respiration response over time. The shift in the subsoil microbial community towards more Actinobacteria might disproportionately enhance the degradation of previously stable subsoil carbon, as this group is able to metabolize complex carbon sources

Soil microbial CNP and respiration responses to organic matter and nutrient additions: evidence from a tropical soil incubation

Soil nutrient availability has a strong influence on the fate of soil carbon (C) during microbial decomposition, contributing to Earth's C balance. While nutrient availability itself can impact microbial physiology and C partitioning between biomass and respiration during soil organic matter decomposition, the availability of labile C inputs may mediate the response of microorganisms to nutrient additions. As soil organic matter is decomposed, microorganisms retain or release C, nitrogen (N) or phosphorus (P) to maintain a stoichiometric balance. Although the concept of a microbial stoichiometric homeostasis has previously been proposed, microbial biomass CNP ratios are not static, and this may have very relevant implications for microbial physiological activities. Here, we tested the hypothesis that N, P and potassium (K) nutrient additions impact C cycling in a tropical soil due to microbial stoichiometric constraints to growth and respiration, and that the availability of energy-rich labile organic matter in the soil (i.e. leaf litter) mediates the response to nutrient addition. We incubated tropical soil from French Guiana with a ¹³C labeled leaf litter addition and with mineral nutrient additions of +K, +N, +NK, +PK and +NPK for 30 days. We found that litter additions led to a ten-fold increase in microbial respiration and a doubling of microbial biomass C, along with greater microbial N and P content. We found some evidence that P additions increased soil CO² fluxes. Additionally, we found microbial biomass CP and NP ratios varied more widely than CN in response to nutrient and organic matter additions, with important implications for the role of microorganisms in C cycling. The addition of litter did not prime soil organic matter decomposition, except in combination with +NK fertilization, indicating possible P-mining of soil organic matter in this P-poor tropical soil. Together, these results point toward an ultimate labile organic substrate limitation of soil microorganisms in this tropical soil, but also indicate a complex interaction between C, N, P and K availability. This highlights the difference between microbial C cycling responses to N, P, or K additions in the tropics and explains why coupled C, N and P cycling modeling efforts cannot rely on strict microbial stoichiometric homeostasis as an underlying assumption

Soil properties explain tree growth and mortality, but not biomass, across phosphorus-depleted tropical forests

We observed strong positive relationships between soil properties and forest dynamics of growth and mortality across twelve primary lowland tropical forests in a phosphorus-poor region of the Guiana Shield. Average tree growth (diameter at breast height) increased from 0.81 to 2.1 mm yr-1 along a soil texture gradient from 0 to 67% clay, and increasing metal-oxide content. Soil organic carbon stocks in the top 30 cm ranged from 30 to 118 tons C ha-1, phosphorus content ranged from 7 to 600 mg kg-1 soil, and the relative abundance of arbuscular mycorrhizal fungi ranged from 0 to 50%, all positively correlating with soil clay, and iron and aluminum oxide and hydroxide content. In contrast, already low extractable phosphorus (Bray P) content decreased from 4.4 to <0.02 mg kg-1 in soil with increasing clay content. A greater prevalence of arbuscular mycorrhizal fungi in more clayey forests that had higher tree growth and mortality, but not biomass, indicates that despite the greater investment in nutrient uptake required, soils with higher clay content may actually serve to sustain high tree growth in tropical forests by avoiding phosphorus losses from the ecosystem. Our study demonstrates how variation in soil properties that retain carbon and nutrients can help to explain variation in tropical forest growth and mortality, but not biomass, by requiring niche specialization and contributing to biogeochemical diversification across this region

Automatic high-frequency measurements of full soil greenhouse gas fluxes in a tropical forest

Measuring in situ soil fluxes of carbon dioxide (CO2), methane (CH4), and nitrous oxide (N2O) continuously at high frequency requires appropriate technology. We tested the combination of a commercial automated soil CO2 flux chamber system (LI-8100A) with a CH4 and N2O analyzer (Picarro G2308) in a tropical rainforest for 4 months. A chamber closure time of 2 min was sufficient for a reliable estimation of CO2 and CH4 fluxes (100 % and 98.5 % of fluxes were above minimum detectable flux - MDF, respectively). This closure time was generally not suitable for a reliable estimation of the low N2O fluxes in this ecosystem but was sufficient for detecting rare major peak events. A closure time of 25 min was more appropriate for reliable estimation of most N2O fluxes (85.6 % of measured fluxes are above MDF ± 0.002 nmol m−2 s−1). Our study highlights the importance of adjusted closure time for each gas

Soil carbon loss in warmed subarctic grasslands is rapid and restricted to topsoil

Global warming may lead to carbon transfers from soils to the atmosphere, yet this positive feedback to the climate system remains highly uncertain, especially in subsoils (Ilyina and Friedlingstein, 2016; Shi et al., 2018). Using natural geothermal soil warming gradients of up to +6.4 degrees C in subarctic grasslands (Sigurdsson et al., 2016), we show that soil organic carbon (SOC) stocks decline strongly and linearly with warming (-2.8 t ha(-1) degrees C-1). Comparison of SOC stock changes following medium-term (5 and 10 years) and long-term (> 50 years) warming revealed that all SOC stock reduction occurred within the first 5 years of warming, after which continued warming no longer reduced SOC stocks. This rapid equilibration of SOC observed in Andosol suggests a critical role for ecosystem adaptations to warming and could imply short-lived soil carbon-climate feedbacks. Our data further revealed that the soil C loss occurred in all aggregate size fractions and that SOC stock reduction was only visible in topsoil (0-10 cm). SOC stocks in subsoil (10-30 cm), where plant roots were absent, showed apparent conservation after > 50 years of warming. The observed depth-dependent warming responses indicate that explicit vertical resolution is a prerequisite for global models to accurately project future SOC stocks for this soil type and should be investigated for soils with other mineralogies

AhR controls redox homeostasis and shapes the tumor microenvironment in BRCA1-associated breast cancer

Cancer cells have higher reactive oxygen species (ROS) than normal cells, due to genetic and metabolic alterations. An emerging scenario is that cancer cells increase ROS to activate protumorigenic signaling while activating antioxidant pathways to maintain redox homeostasis. Here we show that, in basal-like and BRCA1-related breast cancer (BC), ROS levels correlate with the expression and activity of the transcription factor aryl hydrocarbon receptor (AhR). Mechanistically, ROS triggers AhR nuclear accumulation and activation to promote the transcription of both antioxidant enzymes and the epidermal growth factor receptor (EGFR) ligand, amphiregulin (AREG). In a mouse model of BRCA1-related BC, cancer-associated AhR and AREG control tumor growth and production of chemokines to attract monocytes and activate proangiogenic function of macrophages in the tumor microenvironment. Interestingly, the expression of these chemokines as well as infiltration of monocyte-lineage cells (monocyte and macrophages) positively correlated with ROS levels in basal-like BC. These data support the existence of a coordinated link between cancer-intrinsic ROS regulation and the features of tumor microenvironment. Therapeutically, chemical inhibition of AhR activity sensitizes human BC models to Erlotinib, a selective EGFR tyrosine kinase inhibitor, suggesting a promising combinatorial anticancer effect of AhR and EGFR pathway inhibition. Thus, AhR represents an attractive target to inhibit redox homeostasis and modulate the tumor promoting microenvironment of basal-like and BRCA1-associated BC