Abstract
Aim
There is interest in determining how cheatgrass (Bromus tectorum L.) modifies N cycling in sagebrush (Artemisia tridentata Nutt.) soils of the western USA.
Methods
To gain insight into the roles of fungi and bacteria in N cycling of cheatgrass-invaded and uninvaded sagebrush soils, the fungal protein synthesis inhibitor, cycloheximide (CHX), and the bacteriocidal compound, bronopol (BRO) were combined with a 15NH4 + isotope pool dilution approach.
Results
CHX reduced gross N mineralization to the same rate in both sagebrush and cheatgrass soils indicating a role for fungi in N mineralization in both soil types. In cheatgrass soils BRO completely inhibited gross N mineralization, whereas, in sagebrush soils a BRO-resistant gross N mineralization rate was detected that was slower than CHX sensitive gross N mineralization, suggesting that the microbial drivers of gross N mineralization were different in sagebrush and cheatgrass soils. Net N mineralization was stimulated to a higher rate in sagebrush than in cheatgrass soils by CHX, implying that a CHX inhibited N sink was larger in the former than the latter soils. Initial gross NH4 + consumption rates were reduced significantly by both CHX and BRO in both soil types, yet, consumption rates recovered significantly between 24 and 48 h in CHX-treated sagebrush soils. The recovery of NH4 + consumption in sagebrush soils corresponded with an increase in the rate of net nitrification.
Conclusions
These results suggest that cheatgrass invasion of sagebrush soils of the northern Great Basin reduces the capacity of the fungal N consumption sink, enhances the capacity of a CHX resistant N sink and alters the contributions of bacteria and fungi to gross N mineralization.
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References
Adair EC, Burke IC (2010) Plant phenology and life span influence soil pool dynamics: Bromus tectorum invasion of perennial C3-C4 grass communities. Plant Soil 335:255–269. doi:10.1007/s11104-010-0413-3
Bailey VL, Peacock AD, Smith JL, Bolton H Jr (2002) Relationships between soil microbial biomass determined by chloroform fumigation-extraction, substrate-induced respiration, and phospholipid fatty acid analysis. Soil Biol Biochem 34:1385–1389
Bailey VL, Smith JL, Bolton H (2003) Novel antibiotics as inhibitors for the selective respiratory inhibition method of measuring fungal:bacterial ratios in soil. Biol Fertil Soils 38:154–160. doi:10.1007/s00374-003-0620-7
Bardgett RD, Mawdsley JL, Edwards S, Hobbs PJ, Rodwell JS, Davies WJ (1999) Plant species and nitrogen effects on soil biological properties of temperate upland grasslands. Funct Ecol 13:650–660
Bates JD, Svejcar T, Miller RF, Angell RA (2006) The effects of precipitation timing on sagebrush steppe vegetation. J Arid Environ 64:670–697
Belnap J, Stark JM, Rau BM, Allen EB, Phillips S (2016) Soil moisture and biogeochemical factors influence the distribution of annual Bormus species. In: Germino MJ, Chambers JC, Brown CJ (eds) Exotic brome-grasses in arid and semiarid ecosystems of the western US. Springer, Switzerland
Ben Sassi M, Dollinger J, Renault P, Tlili A, Berard A (2012) The FungiResp method: an application of the MicroResp (TM) method to assess fungi in microbial communities as soil biological indicators. Ecol Indic 23:482–490. doi:10.1016/j.ecolind.2012.05.002
Bengtsson G (1992) Interactions between fungi, bacteria and beech leaves in a stream microcosm. Oecologia 89:542–549
Bolton H Jr, Smith JL, Wildung RE (1990) Nitrogen mineralization potentials of shrub-steppe soils with different disturbance histories. Soil Sci Soc Am J 54:887–891
Booth MS, Stark JM, Caldwell MM (2003) Inorganic N turnover and availability in annual- and perennial-dominated soils in a northern Utah shrub-steppe ecosystem. Biogeochemistry 66:311–330
Boyle SA, Yarwood RR, Bottomley PJ, Myrold DD (2008) Bacterial and fungal contributions to soil nitrogen cycling under Douglas fir and red alder at two sites in Oregon. Soil Biol Biochem 40:443–451
Bruulsema TW, Duxbury JM (1996) Simultaneous measurement of soil microbial nitrogen, carbon, and carbon isotope ratio. Soil Sci Soc Am J 60:1787–1791
Bulgarelli D, Rott M, Schlaeppi K, van Ver Loren Themaat E, Ahmadinejad N, Assenza F, Huettel B, Reinhardt R, Schmelzer E, Peplies J, Gloeckner FO, Amann R, Eickhorst T, Schulze-Lefert P (2012) Revealing structure and assembly cues for Arabidopsis root-inhabiting bacterial microbiota. Nature 488:91–95
Callaway RM, Cipollini D, Barto K, Thelen GC, Hallett SG, Prati D, Stinson K, Klironomos J (2008) Novel weapons: invasive plant suppresses fungal mutualists in America but not in its native Europe. Ecology 89:1043–1055
Chen J, Stark JM (2000) Plant species effects and carbon and nitrogen cycling in a sagebrush-crested wheatgrass soil. Soil Biol Biochem 32:47–57
D'Antonio CM, Vitousek PM (1992) Biological invasions by exotic grasses, the grass/fire cycle, and global change. Annu Rev Ecol Syst 23:63–87
Evans RD, Rimer R, Sperry L, Belnap J (2001) Exotic plant invasion alters nitrogen dynamics in an arid grassland. Ecol Appl 11:1301–1310
Germino MJ, Belnap J, Stark JM, Allen EB, Rau B (2016) Ecosystem impact of exotic annual invaders in the genus Bromus. In: Germino MJ, Chambers JC, Brown CS (eds) Exotic brome-grasses in arid and semiarid ecosystems of the western US. Springer, Switzerland
Grayston SJ, Wang SQ, Campbell CD, Edwards AC (1998) Selective influence of plant species on microbial diversity in the rhizosphere. Soil Biol Biochem 30:369–378
Hart S, Stark JM, Davidson EA, Firestone MK (1994) Nitrogen mineralization, immobilization, and nitrification. In: Weaver RW et al (eds) Methods of soil analysis part 2 microbiological and biochemical properties. Soil Science Society of America, Inc., Madison
Hawkes CV, Belnap J, D'Antonio C, Firestone MK (2006) Arbuscular mycorrhizal assemblages in native plant roots change in the presence of invasive exotic grasses. Plant & Soil 281:369–380
Hooker TD, Stark JM, Norton U, Leffler AJ, Peek M, Ryel R (2008) Distribution of ecosystem C and N within contrasting vegetation types in a semiarid rangeland in the Great Basin, USA. Biogeochemistry 90:291–308
Horwath WR, Paul EA (1994) Microbial biomass. In: Weaver RW, Angle S, Bottomley PJ, Bezdicek DF, Smith S, Tabatabai A, Wollum A (eds) Methods of soil analysis part 2: biochemical and microbiological properties. Soil Science Society of America, Madison
Huenneke LF, Hamburg SP, Koide R, Mooney HA, Vitousek PM (1990) Effects of soil resources on plant invasion and community structure in Californian serpentine grassland. Ecology 71:478–491
James JJ, Davies KW, Sheley RL, Ananderud ZT (2008) Linking nitrogen partitioning and species abundance to invasion resistance in the Great Basin. Oecologia 156:637–648
Jordan NR, Larson DL, Huerd SC (2008) Soil modification by invasive plants: effects on native and invasive species of mixed-grass prairies. Biol Invasions 10:177–190
Kirkham D, Bartholomew WV (1954) Equations for following nutrient transformations in soil, utilizing tracer data. Soil Sci Soc Am Proc 18:33–34
Knapp PA (1996) Cheatgrass (Bromus tectorum L) dominance in the Great Basin desert. Glob Environ Chang 6:37–52
Kourtev PS, Ehrenfeld JG, Haggblom M (2002) Exotic plant species alter the microbial community structure and function in the soil. Ecology 83:3152–3166
Kuske CR, Ticknor LO, Miller ME, Dunbar JM, Davis JA, Barns SM, Belnap J (2002) Comparison of soil bacterial communities in rhizospheres of three plant species and the interspaces in an arid grassland. Appl Environ Microbiol 68:1854–1863
Lin Q, Brookes PC (1999) Comparison of substrate induced respiration, selective inhibition and biovolume measurements of microbial biomass and its community structure in unamended, ryegrass-amended, fumigated and pesticide-treated soils. Soil Biol Biochem 31:1999–2014. doi:10.1016/S0038-0717(99)00122-4
Martin G, Guggiari M, Bravo D, Zopfi J, Cailleau G, Aragno M, Job D, Verrecchia E, Junier P (2012) Fungi, bacteria and soil pH: the oxalate-carbonate pathway as a model for metabolic interaction. Environ Microbiol 14:2960–2970. doi:10.1111/j.1462-2920.2012.02862.x
Meidute S, Demoling F, Baath E (2008) Antagonistic and synergistic effects of fungal and bacterial growth in soil after adding different carbon and nitrogen sources. Soil Biol Biochem 40:2334–2343. doi:10.1016/j.soilbio.2008.05.011
Miranda KM, Espey MG, Wink DA (2001) A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide-Biol Ch 5:62–71. doi:10.1006/niox.2000.0319
Norton JB, Monaco TA, Norton JM, Johnson DA, Jones TA (2004) Soil morphology and organic matter dynamics under cheatgrass and sagebrush-steppe plant communities. J Arid Environ 57:445–466
Norton JB, Monaco TA, Norton U (2007) Mediterranean annual grasses in western North America: kids in a candy store. Plant & Soil 298:1–5
Olsson PA, Chalet M, Baath E, Finlay RD, Soderstrom B (1996) Ectomycorrhizal mycelia reduce bacterial activity in a sandy soil. FEMS Microbiol Ecol 21:77–86. doi:10.1111/j.1574-6941.1996.tb00335.x
Romani AM, Fischer H, Mille-Lindblom C, Tranvik LJ (2006) Interactions of bacteria and fungi on decomposing litter: differential extracellular enzyme activities. Ecology 87:2559–2569. doi:10.1890/0012-9658(2006)87[2559:Iobafo]2.0.Co;2
Rousk J, Demoling LA, Bahr A, Baath E (2008) Examining the fungal and bacterial niche overlap using selective inhibitors in soil. FEMS Microbiol Ecol 63:350–358. doi:10.1111/j.1574-6941.2008.00440.x
Rousk J, Demoling L, Baath E (2009) Contrasting short-term antibiotic effects on respiration and bacterial growth compromises the validity of the selective respiratory inhibition technique to distinguish fungi and bacteria. Microb Ecol 58:75–85
Rousk J, Brookes PC, Baath E (2010) Investigating the mechanisms for the opposing pH relationships of fungal and bacterial growth in soil. Soil Biol Biochem 42:926–934. doi:10.1016/j.soilbio.2010.02.009
Saetre P, Stark JM (2005) Microbial dynamics and carbon and nitrogen cycling following re-wetting of soils beneath two semi-arid plant species. Oecologia 142:247–260
Smart DR, Stark JM, Diego V (1999) Resource limitations to nitric oxide emissions from a sagebrush-steppe ecosystem. Biogeochemistry 47:63–86
Smith JL, Halvorson J, Bolton H (1994) Spatial relationships of soil microbial biomass and C and N mineralization in a semi-arid shrub-steppe ecosystem. Soil Biol Biochem 26:1151–1159
Smith JL, Halvorson JJ, Bolton HJ (2002) Soil properties and microbial activity across a 500 m elevation gradient in a semi-arid environment. Soil Biol Biochem 34:1749–1757
Stark JM, Norton JM (2015) The invasive annual cheatgrass increases nitrogen availability in 24-year-old replicated field plots. Oecologia 177:799–809. doi:10.1007/s00442-014-3093-5
Stringham TK, Krueger WC, Shaver PL (2003) State and transition modeling: an ecological process approach. J Range Manag 56:106–113. doi:10.2307/4003893
Thiele-Bruhn S, Beck IC (2005) Effects of sulfonamide and tetracycline antibiotics on soil microbial activity and microbial biomass. Chemosphere 59:457–465. doi:10.1016/j.chemosphere.2005.01.023
Vasquez E, Sheley R, Svejcar T (2008) Nitrogen enhances the competitive ability of cheatgrass (Bromus tectorum) relative to native grasses. Invasive Plant Science and Management 1:287–295. doi:10.1614/Ipsm-08-062.1
Witwicki DL, Doescher PS, Pyke DA, DeCrappeo NM, Perakis SS (2013) Nitrogen limitation, 15N tracer retention, and growth response in intact and Bromus tectorum-invaded Artemisia tridentata ssp wyomingensis communities. Oecologia 171:1013–1023. doi:10.1007/s00442-012-2442-5
Acknowledgements
The authors thank Elizabeth Brewer, Stephanie Yarwood, Rocky Yarwood, and David Myrold for substantial help with the methods and analytical portions of this study, which was funded by the US Geological Survey Forest and Rangeland Ecosystem Science Center Coordinated Intermountain Restoration Project. Any use of trade names is for descriptive purposes only and does not imply endorsement by the U.S. Government.
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DeCrappeo, N.M., DeLorenze, E.J., Giguere, A.T. et al. Fungal and bacterial contributions to nitrogen cycling in cheatgrass-invaded and uninvaded native sagebrush soils of the western USA. Plant Soil 416, 271–281 (2017). https://doi.org/10.1007/s11104-017-3209-x
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DOI: https://doi.org/10.1007/s11104-017-3209-x