Soil Microorganisms as Precursors and Mediators of Soil Carbon Stabilization

Soil organic matter (SOM) results from a suite of microbial and geochemical processes that in combination convert carbon (C) of biological origin to stabilized, potentially long-lived materials. While it is well established that soil microorganisms are involved in the conversion of plant biomass into SOM, the conversion of microbial bodies themselves to stabilized soil organic materials is not well understood. Recent studies suggest that microbial products such as polysaccharides, amino acids, fatty acids, and a number of other biomolecules of microbial origin can remain in soils for long periods of time, and that microbial bodies play a much more important role as the precursors to SOM than previously considered. In this dissertation, I examine the flow of microbial carbon in two soil types as it is assimilated into the living microbial biomass under different climate regimes, how long it remains in the living microbial biomass, and ultimately the flow of this microbial C out of the living biomass as it is respired out as CO2 or is incorporated into SOM. The influence of soil type and climate were examined because both are key drivers of soil biogeochemical processes and strongly affect organic matter stabilization in soils. In Chapter 1, I report the results of a field study conducted to understand not only whether different microbial groups preferentially assimilate carbon from different microbial sources of C, but also whether climate and edaphic characteristics alter either the assimilation of necrotic microbial carbon and/or the length of residence of this carbon within the living biomass. This study followed the fate of 13C labeled dead microbial bodies for three years after they were injected into field soils located in a Temperate mixed-conifer forest and a Tropical wet forest. The 13C was subsequently assimilated into the standing microbial biomass and ultimately lost from the biomass over a 3 year period. In general, the saprophytic microbial groups preferentially assimilated carbon from their same groups or groups with similar molecular compositions; however, only the Gram-positive bacteria in the Tropical site and Gram-positive and Gram-negative bacteria in the Temperate site demonstrated an affinity for assimilating C from dead actinobacteria. At each harvest throughout the study, the Temperate soils retained more labeled 13C from the labeled necromass groups than the Tropical soils. The faster loss of labeled carbon from the living biomass in Tropical soils may have significant implications for the relative contributions of microbial biomass to the formation of SOM. As evidenced in Chapter 3, the retention time of C in living microbial biomass may be positively correlated to the sorption of microbial C to mineral surfaces in the heavy fraction (HF) of SOM. Since the HF is generally the longest-lived SOM pool, an increase in the proportion of microbial C sorbed to mineral surfaces in the HF due to longer residence times of C in the living biomass of Temperate soils may lead to a higher proportion of microbial C in the HF of Temperate soils which may then lead to longer residence times of microbial C in the SOM of Temperate soils. I also conducted a 1.5-year lab incubation designed to investigate the stability and fate of microbial cell materials by following the fate of added, labeled microbial cell C as it was assimilated into the living microbial biomass, respired out as CO2, and recovered in the SOM. Soil samples were collected from a Temperate mixed-conifer forest ecosystem and a Tropical wet forest ecosystem; a single common mixture of 13C labeled bodies was added to the soils, and the soils were incubated for 520 days under 3 different climate regimes (Mediterranean mixed conifer forest, Redwood forest, and Tropical forest). Results from the analyses of the stabilization of microbial C into operationally-defined organic matter fractions in two different soil ecosystems, and the fate of microbial C as it is assimilated into the living biomass, respired out as CO2, and stabilized in the SOM of a Tropical soil are presented in Chapters 2 and 3, respectively. The research presented in Chapter 2 addresses the interactions of climate and edaphic characteristics on the stabilization of microbial C into soil organic matter fractions in Temperate and Tropical soils. Both climate and soil type exerted significant influences on the total amount of 13C recovered in the incubated soils as well as the amount recovered in each of the three operationally-defined stabilized carbon pools: free light fraction (FLF), occluded light fraction (OLF), and heavy fraction (HF). The recovery of 13C was higher in the HF fraction than the OLF and FLF fractions in all but one soil-climate combination. The high recovery of 13C in the HF is consistent with the stabilization of microbial C through interactions with soil mineral surfaces. There was clear influence of climate on the 13C-OLF recoveries from Tropical soils as more 13C was stabilized under the Temperate climates (Mediterranean and Redwood) compared to the Tropical climate. In Chapter 3, the analyses were designed to ask whether longer residence times of carbon in the microbial biomass increased the association of microbial carbon with mineral surfaces in the heavy fraction of SOM. For this study, I monitored the fate of labeled dead carbon as it was added to Tropical soils under three climate regimes (Mediterranean, Redwood and Tropical), assimilated into the living saprophytic biomass, respired out as CO2, and recovered in the SOM. An increase in saprophytic fungi, actinobacteria, Gram-positive bacteria, Gram-negative bacteria, and unassigned lipid biomasses under the Mediterranean climate early in the incubation indicated that all four of these microbial communities temporarily responded favorably to the relatively cold, dry spring Mediterranean climate conditions. Interestingly, assimilation of the dead microbial carbon by actinobacteria was highest under the Tropical climate; this trend was primarily due to the atom% 13C excess of the actinobacterial cells, and not increases in actinobacterial biomass, indicating that while the presence of dead microbial carbon did not cause the actinobacterial communities to increase in size, the actinobacteria in this study did assimilate dead microbial carbon under the static warm, wet climate conditions. The results of Chapter 3 demonstrate that longer residence times of carbon in the microbial biomass may indeed increase the association of microbial carbon with mineral surfaces in the HF of SOM. Here, soils with the longest retention times of 13C in the living biomass and the lowest respiration rates stabilized the most labeled carbon in the HF, while soils with the lowest retention times of 13C in the living biomass and the highest respiration rates stabilized the least amount of labeled carbon in the HF. While the contribution of microbial bodies to soil organic matter have historically been overlooked, or have been considered to be negligible, the findings of this dissertation support recent research that shows that microbial bodies are central to organic matter stabilization and that soil type and climate influence the retention of microbial C in SOM. In Chapter 1, I found that Temperate mixed conifer soils retained higher amounts of microbial C in the living biomass than Tropical wet forest soils over a 3 year period. The research in Chapter 3 demonstrated that longer retention times of C in the living microbial biomass led to higher stabilization of microbial C in the the HF of SOM. Chapter 2 showed a higher retention of microbial C in the HF, as opposed to the FLF or OLF, is likely due to the stabilization of microbial C in the HF through interactions with mineral surfaces. Together, the chapters in this dissertation indicate that a higher proportion of microbial C in Temperate soils may be stabilized through association with soil mineral components than in Tropical soils; in Topical soils, C in the living biomass is lost at a faster rate, diminishing the amount of time that microbial C interacts with mineral surfaces, potentially lessening the proportion of microbial C sorbed to and stabilized on mineral surfaces.