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Denitrification from Nitrogen-Fixing Biologically Crusted Soils in a Cool

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Denitrification from Nitrogen-Fixing Biologically Crusted Soils in a Cool Barger et al. Ecological Processes 2013, 2:16 http://www.ecologicalprocesses.com/content/2/1/16 RESEARCH Open Access Denitrification from nitrogen-fixing biologically crusted soils in a cool desert environment, southeast Utah, USA Nichole N Barger1*, Sarah C Castle2 and Gavin N Dean1 Abstract Introduction: Nitrogen fixation by microorganisms within biological soil crust (“biocrust”) communities provides an important pathway for N inputs in cool desert environments where soil nutrients are low and symbiotic N-fixing plants may be rare. Estimates of N fixation in biocrusts often greatly exceed that of N accretion rates leading to uncertainty regarding N loss pathways. Methods: In this study we examined nitrogen fixation and denitrification rates in biocrust communities that differed in N fixation potential (low N fixation = light cyanobacterial biocrust, high N fixation = dark cyanolichen crust) at four temperature levels (10, 20, 30, 40°C) and four simulated rainfall levels (0.05, 0.2, 0.6, 1 cm rain events) under controlled laboratory conditions. Results: Acetylene reduction rates (AR, an index of N fixation activity) were over six-fold higher in dark crusts relative to light crusts. Dark biocrusts also exhibited eight-fold higher denitrification rates. There was no consistent effect of temperature on denitrification rates, but there was an interactive effect of water addition and crust type. In light crusts, denitrification rates increased with increasing water addition, whereas the highest denitrification rates in dark crusts were observed at the lowest level of water addition. Conclusions: These results suggest that there are no clear and consistent environmental controls on short-term denitrification rates in these biologically crusted soils. Taken together, estimates of denitrification from light and dark biocrusts constituted 3 and 4% of N fixation rates, respectively suggesting that losses as denitrification are not significant relative to N inputs via fixation. This estimate is based on a previously published conversion ratio of ethylene produced to N fixed that is low (0.295), resulting in high estimates of N fixation. If future N fixation studies in biologically crusted soils show that these ratios are closer to the theoretical 3:1 ratio, denitrification may constitute a more significant loss pathway relative to N fixed. Keywords: Biological soil crust, Colorado Plateau, Cool desert, Denitrification, Nitrogen fixation, Soil nitrogen cycling Introduction functions. One such function of primary importance in Biological soil crusts (“biocrusts”) are diverse communi- dryland ecosystems is the ability of microorganisms ties of cyanobacteria, algae, lichens, mosses, fungi, and within biocrusts to fix atmospheric nitrogen (N) other bacteria, which exist in open soil areas not favor- (Mayland and McIntosh 1966; Zaady et al. 1998; Evans able for the growth of higher autotrophs. They comprise and Belnap 1999; Hartley and Schlesinger 2002; Billings up to 70% of the living cover at many sites in arid and et al. 2003; Johnson et al. 2007). Nitrogen fixation by mi- semi-arid regions of the western United States (Belnap croorganisms within biocrust communities provides an et al. 2001), contributing to a broad range of ecological important pathway for N inputs in cool desert environ- ments that are characteristically low in nutrient avail- ability and have a paucity of symbiotic N-fixing plants. * Correspondence: [email protected] 1Department of Ecology and Evolutionary Biology, University of Colorado, What has been less clear is the fate of the N fixed by Campus Box 334, Boulder, CO 80309-0334, USA biocrust organisms and whether N fixed is retained Full list of author information is available at the end of the article © 2013 Barger et al.; licensee Springer. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Barger et al. Ecological Processes 2013, 2:16 Page 2 of 9 http://www.ecologicalprocesses.com/content/2/1/16 within the ecosystem. Estimates of N fixation in bio- Pilmanis 1998). At a Sonoran desert site, Virginia et al. crusts often greatly exceed that of N accretion rates (1982) reported a 58-fold increase in denitrification rates (Peterjohn and Schlesinger 1990), leading to uncertainty under Prosopis glandulosa, an N-fixing shrub, as com- regarding the fate of the fixed N by biologically crusted pared to plant interspaces. These patterns in denitrifica- soils and the potentially important N loss pathways. Soils tion suggest that high N availability associated with N in dryland ecosystems are characterized by pulse precipi- fixation is an important driver of this process. tation events resulting in wet and drying cycles. These Past studies of denitrification in biologically crusted pulsed dynamics in soils may result in N “leakage” by soils have yielded a wide range of denitrification rates. biological soil crust organisms to the surrounding soil Denitrification rates within surface soils (i.e., top 1 cm) + environment in such forms as NH4 and other soluble containing biocrusts were negligible relative to other N organic nitrogen compounds (Mayland and McIntosh loss pathways (Johnson et al. 2007; Strauss et al. 2012) 1966; Johnson et al. 2007). Nitrogen leakage from or increased with biocrust development (Brankatschk biocrusts may not only enhance soil nutrient availability et al. 2013). These studies, however, evaluated denitrifi- to support plant growth (Mayland and McIntosh 1966; cation from biologically crusted soils at a single Belnap and Harper 1995 but may also be lost from the temperature and soil moisture level, environmental con- system via gaseous N loss in transformations related to ditions that may strongly influence not only N fixation nitrification and denitrification processes (Zaady 2005; but also denitrification rates. Barger et al. 2005; Johnson et al. 2007; Strauss et al. Following this, our objective was to examine the influ- 2012; Brankatschk et al. 2013). ence of biocrust community on denitrification rates Denitrification is the biological process that occurs across a range of environmental conditions in the lab to − under reducing conditions where NO3 is used by de- better understand the potential for denitrification from nitrifying bacteria (primarily heterotrophic bacteria) in biocrust communities in dryland ecosystems. We hy- − the absence of O2 as an electron acceptor. NO3 is pothesized that denitrification rates would increase with converted to NO, N2O and N2 along a reduction path- increasing N fixation potential of the biocrust com- way. Factors regulating denitrification rates are low O2 munity and that environmental conditions such as − partial pressure, available NO3 to serve as an oxidant, temperature and soil moisture would further influence and organic C as an energy source for heterotrophic these rates. In this study, we examined nitrogen fixation bacteria (Williams et al. 1992). Previously, it was thought and denitrification rates in two biocrust communities that denitrification in dryland ecosystems should be low that differed in their N fixation potential (light cyano- because anaerobic conditions should rarely occur in arid bacterial biocrust and dark cyanolichen crust) at four environments. However, the presence of anaerobic temperature levels (10, 20, 30, 40°C) and four simulated microsites within dryland soils is not as rare as previ- rainfall levels (0.05, 0.2, 0.6, 1 cm rain events) under ously believed with oxygen levels reaching near zero in controlled laboratory conditions. the surface soils (Garcia-Pichel and Belnap 1996; Johnson et al. 2007). A large portion of the microbial Methods community resides in the top few millimeters of dryland Site description soils. Thus a pulse in microbial activity after a rain event In the spring of 2009, intact biocrust cores were col- may quickly reduce soil oxygen levels (Garcia-Pichel and lected to a 5 cm depth near the Island-in-the-Sky Dis- Belnap 1996; Johnson et al. 2007). trict of Canyonlands National Park, UT (38˚33'19.7" N, Estimates of denitrification are highly variable in desert 109˚44'38.8" 1,883 m.a.s.l.). Mean annual precipitation in ecosystems ranging from 0.4 to 9 kg N ha−1 year−1 in hot this area was 231 mm ranging from a low of 179 mm to North American deserts (e.g., Chihuahuan and Sonoran) a high of 327 mm in the 10 years prior to our study (Virginia et al. 1982; Peterjohn and Schlesinger 1991; (NADP site UT09). Throughout Canyonlands, well- Guilbault and Matthias 1998; Schade et al. 2002). In soils developed biocrust communities often occur on Rizno, from a cold desert site on the Colorado Plateau, denitrifi- dry-Rock outcrop soils, which are classified as loamy, cation was estimated as high as 19 kg N ha−1 year−1 (West mixed calcareous, mesic Lithic Ustic Torriorthents (Web and Skujins 1977). These highly variable estimates are Soil Survey, http://websoilsurvey.nrcs.usda.gov/app/Home likely driven by high spatial and temporal variability (e.g., Page.htm). High sand content and low organic C and N hot spots and hot moments) in denitrification rates. Both characterize these soils. biotic and abiotic processes drive patterns in resource dis- tribution in dryland ecosystems resulting in accumulation Sample collection of nutrients beneath shrub and tree canopies relative to Visual inspection of the presence of lichen species and interspace soils in what has been previously described as coloration in biocrusts is a strong indicator of biocrust “islands of fertility” (Noy-Meir 1985; Schlesinger and community structure and function across the cool desert Barger et al. Ecological Processes 2013, 2:16 Page 3 of 9 http://www.ecologicalprocesses.com/content/2/1/16 regions of the western U.S. (Barger et al. 2005; Belnap Acetylene reduction assay et al. 2008). In our study we used visual inspection of Incubation chambers were constructed of mason jars biocrust color in the field to evaluate the N fixation po- that were pre-drilled through the glass bottom and tential of the biocrust community.
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