Root Influence on Nitrogen Mineralization and Nitrification in Avena barbata Rhizosphere Soil

Micro–N pool dilution was used to quantify rates of gross N mineralization, consumption, and nitrification in bulk soil and in soil within 2 mm of root sections of Avena barbata (slender wild oats), an annual grass common to California oak woodland-savannas. Rates of gross N mineralization in rhizosphere soil (9.2 mg N kgd) were about ten times higher than in bulk soil (1.0 mg N kgd). Total bacterial numbers in soil adjacent to roots were slightly higher than in bulk soil; protozoa biomass was not measurably different. Changes in bacterial numbers or standing stocks of bacterial N could not account for rates of N mineralization. Nitrification potential values were similar in bulk and rhizosphere soil, yet gross rates of nitrification were highly dependent on location along the root. Gross nitrification rates in soil near the root tip were the same as those in bulk soil, while rapid uptake of NH4 by older sections of root (8–16 cm from the tip), appeared to limit nitrification rates. Only small differences in microbial community structure between bulk and rhizosphere soil were detected by terminal restriction fragment length polymorphism (TRFLP) analysis. While the small increases in bacterial numbers and changes in community composition may in-part explain the increased rates of N mineralization, other microbial-root interactions are likely involved in accelerating the flux of N from organic sources to the plant-available NH4 pool. The high rates of N mineralization observed in soil immediately adjacent to roots should facilitate plant access to N. Most of the stocks and fluxes determined in these studies exhibited distinct spatial patterns along the plant root that may have significantly impacted N-availability to the plant. IN TEMPERATE TERRESTRIAL ECOSYSTEMS, N is the nutrient most limiting to plant productivity (Vitousek and Howarth, 1991). Most temperate plants cannot directly access the large pool of N tied up in complex macromolecular soil organic matter, relying primarily on pools of inorganic N in soil solution (Jones et al., 2005). Microorganisms however, are less commonly N limited than plants because they have the enzymatic capacity to access and utilize macromolecular soil organic N (Paul andClark, 1996).Heterotrophic soil microbes are thought to be generally C limited (Paul and Clark, 1996). In mutualistic models of root–microbe interaction, roots supply soil microbes C while the microbes access soil organic N and make this N available to roots (Harte and Kinzig, 1993; Kinzig andHarte, 1998). The interactions of plant roots and microbes in the rhizosphere have been studied extensively because of their broad-ranging importance in nutrient availability, pathology, and soil C dynamics (Pinton et al., 2000). Plant roots exude large amounts (Minchin and Pate, 1973; Norton et al., 1990) and complex arrays of organic compounds into the nearby soil (Juma andMcGill, 1986; Paul and Clark, 1996; Kennedy, 1998). Primarily in response to elevated C availability, bacterial, fungal, and protozoal numbers are generally higher in rhizosphere soil than in bulk soil (Kennedy, 1998). Some types of microbial activity have also been found to be higher in rhizosphere than bulk soil (Hojberg and Sorensen, 1993; Sorensen, 1997; Naseby and Lynch, 1997; Yang and Crowley, 2000). The quality and quantity of root exudates vary temporally and spatially along the root (Klein et al., 1990; Newman, 1985; Jaeger et al., 1999; Bringhurst et al., 2001). We have mapped sugar and amino acid exudate patterns in soil adjacent to Avena barbata roots using engineered bacterial reporter gene systems (two different strains of Erwinia herbicola 299r) and found that sucrose/fructose availability was highest near the root tip and declined with distance from the tip (Jaeger et al., 1999). Increased numbers of microorganisms in rhizosphere soil can represent a potentially labile stock of organic N near plant roots. There are several ways that N contained in microbial biomass can become available to plants. If the supply of labile C is high near young roots and declines substantially in older root sections, then C-limited heterotrophs in a mature rhizosphere would mineralize NH4 during catabolism of N-rich cell components (Myrold, 1998). Such a spatial pattern of Cavailability along roots (high C availability near root tips and low C availability near mature roots) could in itself result in N mineralization. Alternatively, root-C enhancement of microbial numbers and activity may attract bacterivores, which on consumption of low C/N microbial biomass, release N as NH4 into the rhizosphere. Protozoa and other soil fauna excrete an estimated 30% of consumed bacterial N into the rhizosphere (Griffiths et al., 1992), where it is available for plant uptake (Elliott et al., 1984; Clarholm, 1985). Infection of rhizosphere bacteria by bacteriophage would also result in cell lysis and biomass N mineralization. Finally, rhizosphere soil is a zone of water potential fluctuation as a result of evapotranspiration during the day followed by re-equilibration with surrounding soil water during the night (Papendick and Campbell, 1975). Such relatively rapid fluctuations in soil water potential could also result in N mineralization from the rhizosphere microbial biomass as N-rich cellular materials are released during cell water potential equilibration with the surrounding Dep. of Environmental Science Policy and Management, Univ. of California, Berkeley, CA 94720; E. Schwartz, current address: Northern Arizona State Univ., Flagstaff, AZ. Received 7 Apr. 2005. *Corresponding author ([email protected]). Published in Soil Sci. Soc. Am. J. 70:1504–1511 (2006). Soil Biology & Biochemistry doi:10.2136/sssaj2005.0113 a Soil Science Society of America 677 S. Segoe Rd., Madison, WI 53711 USA Abbreviations: AM, arbuscular mycorrhizal; CFDE, chloroform fumigation-direct extraction; PCR, polymerase chain reaction; TRFLP, terminal restriction fragment length polymorphism. R e p ro d u c e d fr o m S o il S c ie n c e S o c ie ty o f A m e ri c a J o u rn a l. P u b lis h e d b y S o il S c ie n c e S o c ie ty o f A m e ri c a . A ll c o p y ri g h ts re s e rv e d . 1504 Published online August 3, 2006