Joshua P. Schimel

NITROGEN MINERALIZATION: CHALLENGES OF A CHANGING PARADIGM

Until recently, the common view of the terrestrial nitrogen cycle had been driven by two core assumptions—plants use only inorganic N and they compete poorly against soil microbes for N. Thus, plants were thought to use N that microbes “left over,” allowing the N cycle to be divided cleanly into two pieces—the microbial decomposition side and the plant uptake and use side. These were linked by the process of net mineralization. Over the last decade, research has changed these views. N cycling is now seen as being driven by the depolymerization of N-containing polymers by microbial (including mycorrhizal) extracellular enzymes. This releases organic N-containing monomers that may be used by either plants or microbes. However, a complete new conceptual model of the soil N cycle needs to incorporate recent research on plant–microbe competition and microsite processes to explain the dynamics of N across the wide range of N availability found in terrestrial ecosystems. We discuss the evolution of thinking abou...

Variations in microbial community composition through two soil depth profiles

Soil profiles are often many meters deep, but with the majority of studies in soil microbiology focusing exclusively on the soil surface, we know very little about the nature of the microbial communities inhabiting the deeper soil horizons. We used phospholipid fatty acid (PLFA) analysis to examine the vertical distribution of specific microbial groups and to identify the patterns of microbial abundance and communitylevel diversity within the soil profile. Samples were collected from the soil surface down to 2 m in depth from two unsaturated Mollisol profiles located near Santa Barbara, CA, USA. While the densities of microorganisms were generally one to two orders of magnitude lower in the deeper horizons of both profiles than at the soil surface, approximately 35% of the total quantity of microbial biomass found in the top 2 m of soil is found below a depth of 25 cm. Principal components analysis of the PLFA signatures indicates that the composition of the soil microbial communities changes significantly with soil depth. The differentiation of microbial communities within the two profiles coincides with an overall decline in microbial diversity. The number of individual PLFAs detected in soil samples decreased by about a third from the soil surface down to 2 m. The ratios of cyclopropyl/monoenoic precursors and total saturated/total monounsaturated fatty acids increased with soil depth, suggesting that the microbes inhabiting the deeper soil horizons are more carbon limited than surface-dwelling microbes. Using PLFAs as biomarkers, we show that Gram-positive bacteria and actinomycetes tended to increase in proportional abundance with increasing soil depth, while the abundances of Gram-negative bacteria, fungi, and protozoa were highest at the soil surface and substantially lower in the subsurface. The vertical distribution of these specific microbial groups can largely be attributed to the decline in carbon availability with soil depth. q 2003 Elsevier Science Ltd. All rights reserved.

The implications of exoenzyme activity on microbial carbon and nitrogen limitation in soil: a theoretical model

Traditional models of soil organic matter (SOM) decomposition are all based on first order kinetics in which the decomposition rate of a particular C pool is proportional to the size of the pool and a simple decomposition constant (dC/dt=kC). In fact, SOM decomposition is catalyzed by extracellular enzymes that are produced by microorganisms. We built a simple theoretical model to explore the behavior of the decomposition–microbial growth system when the fundamental kinetic assumption is changed from first order kinetics to exoenzymes catalyzed decomposition (dC/dt=KC×Enzymes). An analysis of the enzyme kinetics showed that there must be some mechanism to produce a non-linear response of decomposition rates to enzyme concentration—the most likely is competition for enzyme binding on solid substrates as predicted by Langmuir adsorption isotherm theory. This non-linearity also induces C limitation, regardless of the potential supply of C. The linked C and N version of the model showed that actual polymer breakdown and microbial use of the released monomers can be disconnected, and that it requires relatively little N to maintain the maximal rate of decomposition, regardless of the microbial biomass’ ability to use the breakdown products. In this model, adding a pulse of C to an N limited system increases respiration, while adding N actually decreases respiration (as C is redirected from waste respiration to microbial growth). For many years, researchers have argued that the lack of a respiratory response by soil microbes to added N indicates that they are not N limited. This model suggests that conclusion may be wrong. While total C flow may be limited by the functioning of the exoenzyme system, actual microbial growth may be N limited.

Effects of drying–rewetting frequency on soil carbon and nitrogen transformations

Soil drying and rewetting impose a significant stress on the soil microbial community. While wetting events are common in most environments, the short and long-term effects of soil rewetting on microbial processes have not been well studied. Furthermore, it is not clear if stress history is important to consider when modeling microbial controls on ecosystem dynamics. In this experiment, we manipulated the frequency of soil rewetting events during 2 months to determine how stress history influences the response of soil microbial communities to rewetting events. Two soils were collected from the Sedgwick Ranch Natural Reserve in Santa Ynez, CA, one from an annual grassland, the other from underneath an oak canopy. Soils were incubated in the lab and went through either 0, 1, 2, 4, 6, 9, or 15 drying–rewetting cycles over 2 months. Soil moisture content was adjusted so that the average moisture content over the course of the incubation was the same for all samples, compensating for the number of drying–rewetting cycles. Soils were analyzed for respiration rate, substrate utilization efficiency, nitrification potential, microbial biomass, and NH4+ and NO3− concentrations. Total CO2 loss during incubation significantly increased with number of rewetting events for oak soils but not for grass soils, where a large number of rewetting events decreased total CO2 loss. Exposure to frequent drying–rewetting events decreased the amount of CO2 released upon rewetting and dramatically increased the activity of autotrophic nitrifier populations. For up to 6 weeks after the last drying–rewetting cycle, respiration rates in soils exposed to a history of drying–rewetting events were substantially lower than their non-stressed controls. In all cases, the effects of the rewetting stress were greater in oak than in grass soils. The results indicate that drying–rewetting events can induce significant changes in microbial C and N dynamics and these effects can last for more than a month after the last stress. The frequency of drying–rewetting stress events has important ecosystem-level ramifications and should be incorporated into models of soil microbial dynamics.

A Proposed Mechanism for the Pulse in Carbon Dioxide Production Commonly Observed Following the Rapid Rewetting of a Dry Soil

There is uncertainty about the mechanisms responsible for producing the rewetting CO2 pulse. One proThe rapid rewetting of a dry soil often yields a pulse in soil CO2 posed mechanism is that the pulse of CO2 is largely a production that persists for 2 to 6 d. This phenomenon is a common occurrence in surface soils, yet the mechanism responsible for producresult of the mineralization of nonbiomass soil organic ing the CO2 pulse has not been positively identified. We studied the matter (SOM) rendered accessible to microbial attack effects of a single drying and rewetting event on soil C pools, to by the rewetting event. According to this hypothesis, identify which specific C substrates are mineralized to produce the the drying and rewetting process disrupts aggregate observed pulse in respiration rates. We labeled two soils with structure, releasing organic matter from physical protec14C-glucose and measured the enrichment and pool sizes of the retion within aggregates and producing a pulse in microleased CO2, extractable biomass C, and extractable soil organic matter bial activity as this material is mineralized (Adu and (SOM-C) throughout a drying and rewetting cycle. After rewetting, Oades, 1978; Appel, 1998; Denef et al., 2001; Sorensen, respiration rates were 475 to 370% higher than the rates measured 1974; Utomo and Dexter, 1982). Alternatively, others before the dry down. The enrichment of the released CO2 was 1 to have proposed that microbial C, not SOM-C, is the major 2 times higher than the enrichment of the extractable biomass C pools and 10 to 20 times higher than the enrichment of the extractable substrate mineralized to produce the rewetting CO2 organic C, suggesting that the CO2 pulse was generated entirely from pulse (Bottner, 1985; Kieft et al., 1987). The rapid inthe mineralization of microbial biomass C. However, there was no crease in soil water potential associated with the rewetevidence of substantial microbial cell lysis on rewetting. We hypotheting of a dry soil causes microbes to experience osmotic size that the pulse of CO2 is generated by the rapid mineralization of shock. In general, microbial cells either lyse completely highly enriched intracellular compounds as a response by the microbial or adjust to the water potential shock by releasing intrabiomass to the rapid increase in soil water potentials. The drying and cellular osmoregulatory solutes (Halverson et al., 2000; rewetting process also releases physically protected SOM, increasing Harris, 1981). The compounds released into the soil the amount of extractable SOM-C by up to 200%. The additional environment are taken up by surviving microbes and SOM-C rendered soluble by the rewetting event did not contribute mineralized, producing the respiration pulse. Some substantially to the rewetting CO2 pulse. Overall, the rapid rewetting of a dry soil can influence soil C cycling in the short-term, by increasing studies have combined these two proposed mechanisms, the microbial mineralization of cytoplasmic solutes, and in the longersuggesting that both biomass C and nonbiomass SOM-C term, by decreasing the total amount of SOM physically protected contribute to the rewetting CO2 pulse (Scheu and Parkwithin microaggregates. inson, 1994; Van Gestel et al., 1993a; Van Gestel et al., 1991; Van Veen et al., 1985). The identification of the specific mechanisms responN studies have shown that the rapid rewetsible for producing the rewetting CO2 pulse is important ting of a dry soil can cause a large pulse in soil C if we want to understand the implications of climate mineralization rates (Birch, 1958; Clein and Schimel, change on soil C dynamics. In the future, many regions 1994; Franzluebbers et al., 2000; Jager and Bruins, 1975; of the globe may experience higher mean annual temSoulides and Allison, 1961). After a soil rewetting, CO2 peratures and greater intra-annual variability in the timproduction rates are often elevated by as much as 500% ing of precipitation events (Barrow and Hulme, 1996; compared with samples kept continuously moist, with Houghton et al., 1996; Waggoner, 1989). Under these the CO2 pulse generally persisting for a 2to 6-d period scenarios, we would expect many surface soils to experifollowing the rewetting event. Since many surface soils ence more frequent drying and rewetting events. If nonexperience large seasonal fluctuations in moisture conbiomass SOM-C is the primary source of the rewetting tent, these short-term pulses in CO2 production after CO2 pulse, an increase in the frequency of soil drying rewetting are likely to be a common occurrence in many and rewetting will increase the amount of soil C accessisoils. In arid, semi-arid, or Mediterranean environble to microbial attack, potentially decreasing the total ments, where rainfall events are infrequent and soils are amount of C sequestered in a particular soil over time. often dry, the rewetting CO2 pulse may constitute a However, if microbial biomass is the source of the rewetsignificant proportion of the total annual CO2 flux from ting CO2 pulse, an increase in the frequency of dryingsurface soils. rewetting events may increase the level of physiological stress for soil microbes, potentially reducing C mineralN. Fierer and J. P. Schimel, Dep. of Ecology, Evolution, and Marine ization and increasing C sequestration rates over time. Biology, Univ. of California, Santa Barbara, CA 93106. Received 1 We conducted an experiment with two soils from a July 2002. *Corresponding author (fierer@lifesci.ucsb.edu). Abbreviations: SOM, soil organic matter. Published in Soil Sci. Soc. Am. J. 67:798–805 (2003).

Influence of Drying–Rewetting Frequency on Soil Bacterial Community Structure

Soil drying and rewetting represents a common physiological stress for the microbial communities residing in surface soils. A drying–rewetting cycle may induce lysis in a significant proportion of the microbial biomass and, for a number of reasons, may directly or indirectly influence microbial community composition. Few studies have explicitly examined the role of drying–rewetting frequency in shaping soil microbial community structure. In this experiment, we manipulated soil water stress in the laboratory by exposing two different soil types to 0, 1, 2, 4, 6, 9, or 15 drying–rewetting cycles over a 2-month period. The two soils used for the experiment were both collected from the Sedgwick Ranch Natural Reserve in Santa Ynez, CA, one from an annual grassland, the other from underneath an oak canopy. The average soil moisture content over the course of the incubation was the same for all samples, compensating for the number of drying–rewetting cycles. At the end of the 2-month incubation we extracted DNA from soil samples and characterized the soil bacterial communities using the terminal restriction fragment length polymorphism (T-RFLP) method. We found that drying–rewetting regimes can influence bacterial community composition in oak but not in grass soils. The two soils have inherently different bacterial communities; only the bacteria residing in the oak soil, which are less frequently exposed to moisture stress in their natural environment, were significantly affected by drying–rewetting cycles. The community indices of taxonomic diversity and richness were relatively insensitive to drying–rewetting frequency. We hypothesize that drying–rewetting induced shifts in bacterial community composition may partly explain the changes in C mineralization rates that are commonly observed following exposure to numerous drying–rewetting cycles. Microbial community composition may influence soil processes, particularly in soils exposed to a significant level of environmental stress.

LITTER QUALITY AND THE TEMPERATURE SENSITIVITY OF DECOMPOSITION

The temperature sensitivity of litter decomposition will influence the rates of ecosystem carbon sequestration in a warmer world. A number of studies have shown that the temperature sensitivity of litter decomposition can vary depending on litter type and extent of decomposition. However, the underlying causes of this variation are not well understood. According to fundamental principles of enzyme kinetics, the temperature sen- sitivity of microbial decomposition should be inversely related to litter carbon quality. We tested the accuracy of this hypothesis by adding ground plant shoot and root material to soils incubated under controlled conditions and measuring the temperature sensitivities of decomposition at three time points throughout a 53-d incubation. As the overall quality of the litter organic C declined, litter decomposition became more sensitive to temperature. This was true regardless of whether differences in C quality were due to inherent differences in litter chemistry or due to differences in the extent of decomposition. The same pattern was observed when specific C compounds of varying quality were added to soil, suggesting that substrate C quality has a significant and predictable influence on the temperature sensitivity of microbial decomposition.

Microbial response to freeze-thaw cycles in tundra and taiga soils

Abstract Four tundra and taiga soils were experimentally subjected to three freeze-thaw cycles (5 days each at −5°C and +5°C). After each thaw, there was an initial pulse (

Microbial control over carbon cycling in soil

A major thrust of terrestrial microbial ecology is focused on understanding when and how the composition of the microbial community affects the functioning of biogeochemical processes at the ecosystem scale (meters-to-kilometers and days-to-years). While research has demonstrated these linkages for physiologically and phylogenetically “narrow” processes such as trace gas emissions and nitrification, there is less conclusive evidence that microbial community composition influences the “broad” processes of decomposition and organic matter (OM) turnover in soil. In this paper, we consider how soil microbial community structure influences C cycling. We consider the phylogenetic level at which microbes form meaningful guilds, based on overall life history strategies, and suggest that these are associated with deep evolutionary divergences, while much of the species-level diversity probably reflects functional redundancy. We then consider under what conditions it is possible for differences among microbes to affect process dynamics, and argue that while microbial community structure may be important in the rate of OM breakdown in the rhizosphere and in detritus, it is likely not important in the mineral soil. In mineral soil, physical access to occluded or sorbed substrates is the rate-limiting process. Microbial community influences on OM turnover in mineral soils are based on how organisms allocate the C they take up – not only do the fates of the molecules differ, but they can affect the soil system differently as well. For example, extracellular enzymes and extracellular polysaccharides can be key controls on soil structure and function. How microbes allocate C may also be particularly important for understanding the long-term fate of C in soil – is it sequestered or not?

Short-term partitioning of ammonium and nitrate between plants and microbes in an annual grassland

We measured short-term (24 h) partitioning of 15NH4+ and 15NO3− into plants and microbes in a California annual grassland. Experiments were done in early spring at the peak of plant growth (February), and in late spring (April) when plant senescence had begun. Soil moisture decreased from 31 to 9% during this period. We injected either 15NH4+, 15NO3−, 15NH4+NO3− or NH415NO3− (≈ 2μg Ng−1 soil for each N-species) into the top 10cm of soil in cylinders which had been driven into the soil. After 24 h the soil and plants in the cylinders were harvested and we measured total N and 15N in inorganic forms, the microbial biomass (chloroform fumigation technique) and harvested plant material. Ammonium was the dominant source of N to both plants and microbes. In February, uptake rates of NH4+ were 81 and 426 mg N m−2 day−1 for plants and microbes, respectively, while in April the rates were 110 and 639 mg N m−2 day−1. Rates of NO3− uptake were 41 and 81 mgNm−2day−1 in February and 83 and 146mgNm−2 day−1 in April for plants and microbes, respectively. Thus, microbes took up substantially more NH4+ and NO3− than plants. On both sampling dates, NH4+ concentrations in the top 10cm of soil ranges from 600 to 800mg N m−2, andNO3− concentrations were <50 mg N m−2 High rates of microbial NO3−3 uptake may have resulted from the occurrence of microsites that were depleted in NH4+. Even though plants competed better for NO3− than for NH4+, microbial uptake was a major factor controlling NO3− availability to plants. The high rates of NH4+ and NO3− uptake by plants and microbes clearly demonstrate that the soil N pool bears little relationship to actual N availability.