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J. Jason L. Cantera . Fiona L. Jordan . Lisa Y. Stein. Effects of irrigation sources on ammonia-oxidizing bacterial communities in a managed turf-covered aridisol.
Biol Fertil Soils (2006) 43: 247–255 DOI 10.1007/s00374-006-0101-x

ORIGINA L PA PER

J. Jason L. Cantera . Fiona L. Jordan . Lisa Y. Stein

Effects of irrigation sources on ammonia-oxidizing bacterial communities in a managed turf-covered aridisol

Received: 5 June 2005 / Revised: 28 February 2006 / Accepted: 15 March 2006 / Published online: 20 April 2006 # Springer-Verlag 2006

Abstract Ammonia-oxidizing bacteria (AOB) perform the rate-limiting step of nitrification, a key process in the global nitrogen cycle. In this study, chemical factors controlling AOB activity, diversity, and composition in a turfgrass-covered aridisol irrigated with groundwater, Colorado River water, or reclaimed wastewater were examined. Activity of AOB contributed an average of 96% of potential nitrification activity in four soils examined, and this activity correlated positively with ammonium concentration and negatively with salinity of the irrigation water. AOB abundance, as determined by quantitative polymerase chain reaction, also correlated positively with ammonium concentration in the irrigation water but negatively with soil salinity. Characterization of AOB communities by denaturing gradient gel electrophoresis showed the presence in every soil of AOB taxa, most commonly found in high-ammonia environments. The soil with the fewest years of management had the least diverse AOB population, compared to the other three soils, and much lower specific nitrification activity. This soil was irrigated with highly saline Colorado River water, which likely exerted acute negative effects on the activity of AOB. In summary, this study revealed that, although AOB activity and growth responded positively to ammonium availability in irrigation water, the salinity of the water and soil had strong negative effects on these aspects of the AOB community. Present address: F. L. Jordan Environmental Research Laboratory, Department of Soil, Water and Environmental Sciences, University of Arizona, 2601 E. Airport Rd., Tucson, AZ 85706, USA J. J. L. Cantera . F. L. Jordan . L. Y. Stein (*) Department of Environmental Sciences, University of California, Geology 2207, Riverside, CA 92521, USA e-mail: [email protected] Tel.: +1-951-8272704 Fax: +1-951-8273993

Keywords Ammonia-oxidizing bacteria . Salinity . Turfgrass . Aridisol . Reclaimed wastewater

Introduction One consequence of rapid urbanization in the desert Southwest USA is the spread of turfgrass cover on aridisols—a soil order characterized as dry, sandy, low in nutrients, and therefore traditionally underutilized for agriculture. At present, turfgrass environments (e.g., golf courses) are among the most rapidly increasing managed ecosystems in this region (Qian and Follett 2002). Golf courses within the same geographical range often have similar turf cover and soil composition, but each course receives a different management regime. Differences in irrigation source may significantly influence the structure and function of the soil microbial community, which in turn may alter nutrient cycling in turfgrass ecosystems. For instance, in the Southern California desert where water is a limiting resource, irrigating turf soils with reclaimed wastewater is becoming an inexpensive option to irrigation with groundwater. However, irrigation with reclaimed wastewater may have adverse side effects as these waters often contain high levels of solutes, such as salts, organic carbon and metals, and could provide an undesirable inoculum of microorganisms (Pettygrove et al. 1985). Until recently, irrigation of arid agricultural regions within the Coachella and Imperial valleys of southern California with Colorado River water via the All-American Canal was considered a relatively inexpensive option to using groundwater. However, several years of drought have dramatically increased the cost and political pressure for conserved use of canal water. Furthermore, canal water is often extremely saline (∼800 ppm salts) due to high rates of evapotranspiration as the water travels in open channels through the desert (Pillsbury 1981). Irrigation with such saline water can adversely affect plant growth, soil chemistry, and microbial activity over time (Pillsbury 1981; Rietz and Haynes 2003; Ashraf 2004).

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In-depth analysis of microbial activity in turf-covered aridisols receiving different sources of irrigation water will aid in understanding the potential effects of salinity and management practices on soil health. A particularly important microbial group, affected by both N-fertilization and irrigation, is the autotrophic ammonia-oxidizing bacteria (AOB) (Phillips et al. 2000a; Oved et al. 2001; Webster et al. 2002). This group of microorganisms, which oxidizes ammonia to nitrite, effectively competes with plants for ammonia, and acidifies the environment during active nitrification (Prosser 1989). Comparative 16S rRNA gene sequence analysis of AOB in several ecosystems has shown the apparent dominance of Nitrosospira spp. in terrestrial environments, whereas the majority of the characterized Nitrosomonas spp. inhabit high-ammonia environments, such as wastewater, sewage, manure/compost, soils irrigated with wastewater effluent, some marine environments, and some acidic soils (Kowalchuk and Stephen 2001; Oved et al. 2001; Carnol et al. 2002; Koops et al. 2003). These studies and others have shown that activity, abundance, and diversity of AOB are highly influenced by chemical and environmental factors such as ammonium (NH þ 4 ) levels, O2, pH, organic matter, salt concentrations, temperature, and application of organic vs inorganic fertilizers (Princic et al. 1998; Stephen et al. 1998; Kowalchuk et al. 2000a; Bollmann and Laanbroek 2002; Avrahami and Conrad 2003; Avrahami et al. 2003; Okano et al. 2004; Grommen et al. 2005). In the present study, we used molecular approaches targeting 16S rRNA genes, along with activity and chemical measurements, to examine the impact of different irrigation sources on the activity, abundance, and population structure of AOB in a heavily fertilized, turfgrasscovered aridisol located in the Coachella Valley, Southern California. We hypothesized that activity and abundance of AOB communities would be positively affected by NH þ 4 concentration, as documented in studies of other highly managed soils, such as grassland (Kowalchuk et al. 2000a, 2000b; Webster et al. 2002), humisol (Briones et al. 2003), meadow (Avrahami and Conrad 2003), and arable soils (Bruns et al. 1999; Hermansson and Lindgren 2001; Okano et al. 2004). In addition, because aridisols generally accumulate high levels of salts due to high rates of evapotranspiration in hot summer months, we hypothesized negative correlations of AOB activities and abundances with high ion concentrations in the soil and/or irrigation waters.

Materials and methods Study area, sample collection, and analytical procedures Soil and irrigation water samples were taken from four golf courses (denoted as HP, IR, PV, and SR) located within a 10-km region of the Coachella Valley, Southern California in September 2003. All golf course soils were characterized

as Myoma fine sandsown with Bermuda grass (Cynodondactylon) in the spring and ryegrass (Loliumperenne L.) in the fall. Fertilizer-N was applied to each golf course through the irrigation systems at approximated rates of 40, 15, 15, and 5 g m−2 year−1 for HP, IR, PV, and SR,  respectively. Fertilizer mixtures contained NH þ 4 ; NO3 ;  þ and urea for HP, PV, and SR, and NH 4 and NO3 for IR. The oldest course (SR) had been operational since 1979, while the youngest course (HP) was constructed in 1997. Each course received irrigation water year round from a different primary source: IR and SR received tertiarytreated, reclaimed, wastewater from different locations, PV received groundwater, and HP received Colorado River water. Three 500-g samples from rough (turf-covered) soils and three 250-g samples from sand traps (imported washed sand with 3% or less total silt plus clay) were collected at each golf course using a 2.5 cm (i.d.)×10 cm soil auger. Each set of soil or sand sample was pooled and homogenized by sieving (0.05). This was most likely because Colorado River water irrigating the youngest course, HP, had much higher ion content than any other irrigation source. The EC of the 6-year-old HP rough soil was already close to 1.5 times that of the 18-year-old PV rough soil, indicating the beginnings of salt accumulation at HP.

Results and discussion Soil and irrigation water properties

Potential nitrification activity and abundance of ammonia-oxidizing bacteria

Chemical properties of soils, sands, and irrigation waters were compared across four different golf courses to determine how duration of management (golf course age) and type of irrigation water influenced the same parent aridisol. Samples were taken from single sites at each golf course, such that spatial heterogeneities in chemical, physical, or biological factors within individual golf courses were not accounted for. Golf course sand traps, consisting of non-turf covered imported sands that also received fertilizer-amended irrigation water, were used to distinguish effects of plant cover and developed rhizospheres on microbial populations. Total organic carbon (TOC), ion concentrations, and salinity were significantly higher (two–ten times, with few exceptions), and soil pH was significantly lower in rough soils relative to sand traps (ANOVA, P