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Linking Microbial Community Structure and Function to Seasonal Differences in Soil Moisture and Temperature in a Chihuahuan Desert Grassland

  • Soil Microbiology
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Abstract

Global and regional climate models predict higher air temperature and less frequent, but larger precipitation events in arid regions within the next century. While many studies have addressed the impact of variable climate in arid ecosystems on plant growth and physiological responses, fewer studies have addressed soil microbial community responses to seasonal shifts in precipitation and temperature in arid ecosystems. This study examined the impact of a wet (2004), average (2005), and dry (2006) year on subsequent responses of soil microbial community structure, function, and linkages, as well as soil edaphic and nutrient characteristics in a mid-elevation desert grassland in the Chihuahuan Desert. Microbial community structure was classified as bacterial (Gram-negative, Gram-positive, and actinomycetes) and fungal (saprophytic fungi and arbuscular mycorrhiza) categories using (fatty acid methyl ester) techniques. Carbon substrate use and enzymic activity was used to characterize microbial community function annually and seasonally (summer and winter). The relationship between saprophytic fungal community structure and function remained consistent across season independent of the magnitude or frequency of precipitation within any given year. Carbon utilization by fungi in the cooler winter exceeded use in the warmer summer each year suggesting that soil temperature, rather than soil moisture, strongly influenced fungal carbon use and structure and function dynamics. The structure/function relationship for AM fungi and soil bacteria notably changed across season. Moreover, the abundance of Gram-positive bacteria was lower in the winter compared to Gram-negative bacteria. Bacterial carbon use, however, was highest in the summer and lower during the winter. Enzyme activities did not respond to either annual or seasonal differences in the magnitude or timing of precipitation. Specific structural components of the soil microbiota community became uncoupled from total microbial function during different seasons. This change in the microbial structure/function relationship suggests that different components of the soil microbial community may provide similar ecosystem function, but differ in response to seasonal temperature and precipitation. As soil microbes encounter increased soil temperatures and altered precipitation amounts and timing that are predicted for this region, the ability of the soil microbial community to maintain functional resilience across the year may be reduced in this Chihuahuan Desert ecosystem.

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References

  1. Bernstein L, et al (2007) An assessment of the intergovernmental panel on climate change. Valencia, Spain, p 52

  2. Stanley EH, Valett HM (1992) Interactions between drying and the hyporheic zone of a desert stream, in global climate change and freshwater ecosystems. Springer, New York, NY, p 211-233

  3. NAST, N.A.S.T., US Global Change Research Program (2000) Climate change impacts on the united states: the potential consequences of climate variability and change. Cambridge University Press, New York, NY

    Google Scholar 

  4. Johns TC et al (1996) The second Hadley Centre coupled ocean-atmosphere GCM: model description, spinup and validation. Clim Dyn 13:103–134

    Article  Google Scholar 

  5. Seager R et al (2007) Model projections of an imminent transition to a more arid climate in southwestern North America. Science 316:1181–1184

    Article  PubMed  CAS  Google Scholar 

  6. Easterling DR et al (2000) Climate extremes: observations, modeling, and impacts. Science 289:2068–2074

    Article  PubMed  CAS  Google Scholar 

  7. Noy-Meir I (1973) Desert ecosystems: environment and producers. Ann Rev Ecolog Syst 4:25–51

    Article  Google Scholar 

  8. Rapport DJ, Whitford WG (1999) How ecosystems respond to stress. BioScience 49(3):193–203

    Article  Google Scholar 

  9. Schwinning S, Ehleringer JR (2001) Water use trade-offs and optimal adaptations to pulse-driven arid ecosystems. J Ecol 89:464–480

    Article  Google Scholar 

  10. Cable JM, Huxman TE (2004) Precipitation pulse size effects on Sonoran Desert soil microbial crusts. Oecologia 141:317–324

    Article  PubMed  Google Scholar 

  11. Belnap J et al (2005) Linkages between microbial and hydrologic processes in arid and semiarid watersheds. Ecology 86(2):298–307

    Article  Google Scholar 

  12. Mooney HA, Canadell J, Chapin FS, Ehleringer JR, and Korner C (2000) Ecosystem physiology responses to global change. Pages 141-189 in B. H. Walker, W. Steffen, J. Canadell, and J. Ingram, editors. The Terrestrial Biosphere and Global Change. Cambridge University Press, Cambridge, MA.

  13. Huxman TE et al (2004) Convergence across biomes to a common rain-use efficiency. Nature 429:651–654

    Article  PubMed  CAS  Google Scholar 

  14. Groffman PM, Bohlen PJ (1999) Soil and sediment biodiversity: cross-system comparisons and large scale effects. BioScience 49:139–148

    Article  Google Scholar 

  15. Zak JC, Sinsabaugh R, MacKay W (1995) Windows of opportunity in desert ecosystems: their implications to fungal community development. Can J Bot 73:S1407–S1414

    Article  Google Scholar 

  16. Tilman D (1994) Competition and biodiversity in spatially structured habitats. Ecology 75(1):2–16

    Article  Google Scholar 

  17. Tilman D et al (2001) Diversity and productivity in a long-term grassland experiment. Science 294:843–845

    Article  PubMed  CAS  Google Scholar 

  18. Symstad AJ et al (2003) Long-term and large-scale perspectives on the relationship between biodiversity and ecosystem functioning. Bioscience 53:89–98

    Article  Google Scholar 

  19. Zak DR et al (2003) Plant diversity, soil microbial communities, and ecosystem function: are there any links? Ecology 84(8):2042–2050

    Article  Google Scholar 

  20. Belnap J, Phillips SL, Miller ME (2004) Response of desert biological soil crusts to alterations in precipitation frequency. Oecologia 141:306–316

    Article  PubMed  Google Scholar 

  21. Vishnevetsky S, Steinberger Y (1997) Bacterial and fungal dynamics and their contribution to microbial biomass in desert soil. J Arid Environ 37:83–90

    Article  Google Scholar 

  22. Collins SL et al (2008) Pulse dynamics and microbial processes in aridland ecosystems. J Ecol 96:413–420

    Article  Google Scholar 

  23. Behan-Pelleteir VM, Newton G (1999) Linking soil biodiversity and ecosystem function—the taxonomic dilemma. BioScience 49(2):149–153

    Article  Google Scholar 

  24. Groffman PM, Zaady E, Shachak M (2005) Microbial contributors to biodiversity in deserts. In: Perevolotsky A (ed) Biodiversity in drylands. Oxford University Press, New York, NY, pp 109–121

    Google Scholar 

  25. Zak JC et al (1994) Functional diversity of microbial communities: a quantitative approach. Soil Biol Biochem 26(9):1101–1108

    Article  Google Scholar 

  26. Parker LW et al (1984) Carbon and nitrogen dynamics during the decomposition of litter and roots of a Chihuahuan desert annual, Lepidium lasiocarpum. Ecol Monogr 54:339–360

    Article  CAS  Google Scholar 

  27. Schlesinger WH, Fonteyn PJ, Marion GM (1987) Soil moisture content and plant transpiration in the Chihuahuan Desert of New Mexico. J Arid Environ 12:119–126

    Google Scholar 

  28. Peterjohn WT (1991) Denitrification: enzyme content and activity in desert soils. Soil Biol Biochem 23:845–855

    Article  CAS  Google Scholar 

  29. Fliesbach A, Sarig S, Steinberger Y (1994) Effects of water pulses and climatic conditions on microbial biomass kinetics and microbial activity in a Yermosol of the central Negev. Arid Soil Res Rehabil 8:353–362

    Google Scholar 

  30. Steinberger Y et al (1999) Phospholipid fatty acid profiles as indicators for microbial community structure in soils along a climatic transect in the Judean Desert. Biol Fertil Soils 28:292–300

    Article  CAS  Google Scholar 

  31. Zaady E, Groffman PM, Shachak M (1996) Release and consumption of nitrogen from snail feces in Negev Desert soils. Biol Fertil Soils 23:399–405

    Article  CAS  Google Scholar 

  32. Zaady E, Groffman PM, Shachak M (1996) Litter as a regulator of nitrogen and carbon dynamics in macrophytic patches in Negev Desert soils. Soil Biol Biochem 28:39–46

    Article  CAS  Google Scholar 

  33. Kennedy AC, Gewin VL (1997) Soil microbial diversity: present and future. Soil Sci 162:607–617

    Article  CAS  Google Scholar 

  34. Zak JC, Visser S (1996) An appraisal of soil fungal biodiversity: the crossroads between taxonomic and functional biodiversity. Biodivers Conserv 5:169–183

    Article  Google Scholar 

  35. Sobek E, Zak JC (2003) The soil FungiLog procedure: method and analytical approaches toward understanding fungal functional diversity. Mycologia 95:590–602

    Article  Google Scholar 

  36. Konopka A, Oliver L, Turco RF (1998) The use of carbon substrate utilization patterns in environmental and ecological microbiology. Microb Ecol 35:103–115

    Article  PubMed  CAS  Google Scholar 

  37. Smalla K et al (1998) Analysis of Biolog GN substrate utilization patterns by microbial communities. Appl Environ Microbiol 64:1220–1225

    PubMed  CAS  Google Scholar 

  38. Bell CW et al (2008) Soil microbial responses to temporal variations of moisture and temperature in a Chihuahuan Desert grassland. Microb Ecol 56(1):153–167

    Article  PubMed  Google Scholar 

  39. Trasar-Cepeda C, Leiros MC, Gil-Sotres F (2000) Biochemical properties of acid soils under climax vegetation (Atlantic oakwood) in an area of the European temperate-humid zone (Galicia, NW Spain): specific parameters. Soil Biol Biochem 32:747–755

    Article  CAS  Google Scholar 

  40. Ndiaye EL et al (2000) Integrative biological indicators for detecting change in soil quality. Am J Altern Agric 15:26–36

    Article  Google Scholar 

  41. Klose S, Moore JM, Tabatabai MA (1999) Arylsulfatase activity of microbial biomass in soils as affected by cropping systems. Biol Fertil Soils 29:46–54

    Article  CAS  Google Scholar 

  42. Moore JM, Klose S, Tabatabai MA (2000) Soil Microbial biomass carbon and nitrogen as affected by cropping systems. Biol Fertil Soils 31:200–210

    Article  CAS  Google Scholar 

  43. Pavel R, Doyle J, Steinberger Y (2003) Seasonal patterns of cellulose concentration in desert soil. Soil Biol Biochem 36:549–554

    Article  CAS  Google Scholar 

  44. Moorhead DL, Sinsabaugh R (1999) Simulated patterns of little decay predict patterns of extracellular enzyme activities. Appl Soil Ecol 14:71–79

    Article  Google Scholar 

  45. Kieft TL et al (1997) Survival and phospholipids fatty acid profiles of surface and subsurface bacteria in nature sediment microcosms. Appl Environ Microbiol 63:1531–1542

    PubMed  CAS  Google Scholar 

  46. Fierer N, Schimel JP, Holden PA (2003) Variations in microbial community composition through two soil depth profiles. Soil Biol Biochem 35:167–176

    Article  CAS  Google Scholar 

  47. Zak JC et al (1997) Big Bend National Park watershed program monitoring microbial activity and diversity along an elevational gradient. In 9th Conference on Research and Resource Management in Parks and on Public Lands. Albuquerque, NM

  48. Robertson TR et al (2008) Precipitation timing and magnitude differentially affect aboveground annual net primary productivity in three perennial species in a Chihuahuan Desert grassland. New Phytol 181(1):230–242

    Article  Google Scholar 

  49. Patrick L et al (2009) Physiological responses of two contrasting desert plant species to precipitation variability are differentially regulated by soil moisture and nitrogen dynamics. Glob Chang Biol 15(5):1214–1229

    Article  Google Scholar 

  50. Jarrell WM et al (1999) Soil water and temperature status. In: Sollins P (ed) Standard soil methods for long-term ecological research. Oxford University Press, New York, NY, pp 55–73

    Google Scholar 

  51. Onset CC (2004) Hobo-H8 pro-series user’s manual. Onset Computer Corporation, Bourne, MA

    Google Scholar 

  52. Robertson GP et al (1999) Soil carbon and nitrogen availability: nitrogen mineralization, nitrification, and soil respiration potentials. In: Sollins P (ed) Standard soil methods for long-term ecological research. Oxford University Press, New York, NY, pp 258–271

    Google Scholar 

  53. Sollins P et al (1999) Soil carbon and nitrogen. In: Sollins P (ed) Standard soil methods for long-term ecological research. Oxford University Press, New York, pp 89–105

    Google Scholar 

  54. Miller RH, Keeney DR (1982) Methods of soil analysis, 2nd edn. Academic, Madison, WI

    Google Scholar 

  55. Vance ED, Brookes PC, Jenkinson DS (1987) An extraction method for measuring soil microbial biomass C. Soil Biol Biochem 19(6):703–707

    Article  CAS  Google Scholar 

  56. Nunan N, Morgan MA, Herlihy M (1997) Ultraviolet absorbance (280 nm) of compounds released from soil during chloroform fumigation as an estimate of the microbial biomass. Soil Biol Biochem 30(12):1599–1603

    Article  Google Scholar 

  57. Garland JL, Millis AL (1991) Classification and characterization of heterotrophic microbial communities on the basis of patterns of community-level sole-carbon-source utilization. Appl Environ Microbiol 57:2351–2359

    PubMed  CAS  Google Scholar 

  58. Dobranic JK, Zak JC (1999) A microtiter plate procedure for evaluating fungal functional diversity. Mycologia 91:756–765

    Article  Google Scholar 

  59. Parham JA, Deng SP (2000) Detection, quantification and characterization of B-glucosaminidase activity in soil. Soil Biol Biochem 32:1183–1190

    Article  CAS  Google Scholar 

  60. Tabatabai MA (1994) Soil enzymes. In: Keeney DR (ed) Methods of soil analysis. American Society of Agronomy, Inc., Madison, WI, pp 903–947

    Google Scholar 

  61. Deacon J (2006) Fungal nutrition. In: Deacon J (ed) Fungal biology, 4th edn. Blackwell, Oxford, UK

    Google Scholar 

  62. Ekenler M, Tabatabai MA (2002) β-Glucosaminidase activity of soils: effect of cropping systems and its relationship to nitrogen mineralization. Biol Fertil Soils 35:1081–1094

    Google Scholar 

  63. Acosta-Martinez V, Zobek TM, Gill TE (2003) Enzyme activities and microbial community structure in semiarid agricultural soils. Biol Fertil Soils 38:216–227

    Article  CAS  Google Scholar 

  64. Sasser M (2001) Identification of bacteria by gas chromatography of cellular fatty acids. MIDI, Inc. Automated Microbial Identification Solutions, Newark, DE

    Google Scholar 

  65. Zak DR et al (1996) Soil microbial communities beneath Populus grandidentata grown under elevated atmospheric CO2. Ecol Appl 6:257–294

    Article  Google Scholar 

  66. Zogg GP et al (1997) Compositional and functional shifts in microbial communities due to soil warming. Soil Sci Soc Am 61:475–481

    CAS  Google Scholar 

  67. Ringelberg DB et al (1997) Consequences of rising atmospheric carbon dioxide levels for the belowground microbiota associated with white oak. J Environ Qual 26:495–503

    Article  CAS  Google Scholar 

  68. Pinkart HC et al (2002) Biochemical approaches to biomass measurements and community structure analysis. In: Hurst CJ (ed) Manual of environmental microbiology. ASM, Washington, DC, pp 101–113

    Google Scholar 

  69. Zelles L (1997) Phospholipid fatty acid profiles in selected members of soil microbial communities. Chemosphere 35:275–294

    Article  PubMed  CAS  Google Scholar 

  70. Madan R et al (2002) Use of fatty acids for identification of AM fungi and estimation of the biomass of AM spores in soil. Soil Biol Biochem 34:125–128

    Article  CAS  Google Scholar 

  71. Olsson PA (1999) Signature fatty acids provide tools for determination of the distribution and interactions of mycorrhizal fungi in soil. FEMS Microbiol Ecol 29:303–310

    Article  CAS  Google Scholar 

  72. Ruess L et al (2002) Fatty acids of fungi and nematodes-possible biomarkers in the soil food chain? Soil Biol Biochem 34:745–756

    Article  CAS  Google Scholar 

  73. Rateledge C, Wilkinson SG (1998) Microbial lipids. Academic, London, UK

    Google Scholar 

  74. Bardgett RD, Hobbs PJ, Frostegard A (1996) Changes in soil fungal:bacterial biomass ratios following reductions in the intensity of management of an upland grassland. Biol Fertil Soils 22:261–264

    Article  Google Scholar 

  75. Frostegard A, Baath E (1996) The use of phospholipid fatty acid analysis to estimate bacterial and fungal biomass in soil. Biol Fertil Soils 22:59–65

    Article  Google Scholar 

  76. Koppenstedt RM. The prokaryotes. Springer, New York, NY, p 1139–1156

  77. White DC, Stair JO, Ringelberg DB (1996) Quantitative comparisons or in situ microbial biodiversity by signature biomarker analysis. J Ind Microbiol 17:185–196

    Article  CAS  Google Scholar 

  78. Leps J, Smilauer P (2003) Mulitvariate analysis of ecological data using CANOCO. University of South Bohemia, Ceske Budejovice, Czech Republic

    Google Scholar 

  79. Vandenkoornhuyse P et al (2002) Arbuscular mycorrhizal community composition associated with two plant species in a grassland ecosystem. Mol Ecol 11:1555–1564

    Article  PubMed  CAS  Google Scholar 

  80. Treseder KK, Cross A (2006) Global distributions of arbuscular mycorrhizal fungi. Ecosystems 9:305–316

    Article  Google Scholar 

  81. Deacon J (2006) Fungal symbiosis. In: Deacon J (ed) Fungal biology, 4th edn. Blackwell, Oxford, UK, pp 279–308

    Google Scholar 

  82. Rillig MC (2004) Arbuscular mycorrhizae and terrestrial ecosystem processes. Ecol Lett 7:740–754

    Article  Google Scholar 

  83. Freise CF, Allen MF (1991) The spread of VA mycorrhizal fungal hyphae in the soil: inoculum types and external hyphal architecture. Mycologia 83:409–418

    Article  Google Scholar 

  84. Cui M, Caldwell M (1997) A large ephemeral release of nitrogen upon wetting of dry soil and corresponding root responses in the field. Plant Soil 191:291–299

    Article  CAS  Google Scholar 

  85. Brown AR, Webster S (2004) Orographic flow-blocking scheme characteristics. Q J R Meteorol Soc 130:3015–3028

    Article  Google Scholar 

  86. Sinsabaugh R et al (1999) Characterizing soil microbial communities. In: Sollins P (ed) Standard soil methods for long term ecological research. Oxford University Press, New York, NY

    Google Scholar 

  87. Jones DL (1998) Organic acids in the rhizosphere—a critical review. Plant Soil 205:25–44

    Article  CAS  Google Scholar 

  88. Bolton H Jr, Fredrickson JK (1993) Microbial ecology in the rhizosphere. In: Metting FB Jr (ed) Soil microbial ecology. NY, Marcel Decker, New York

    Google Scholar 

  89. Oren A, Steinberger Y (2008) Catabolic profiles of soil fungal communities along a geographic climate gradient in Israel. Soil Biol Biochem 40:2578–2587

    Article  CAS  Google Scholar 

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Acknowledgments

This research was funded by the USGS Global Climate Change Small Watershed Project (J. Zak) and US National Park Service (J. Zak, D. Tissue). Special thanks are extended to Joe Sirotnak along with the rest of the research staff at BBNP for continued support and cooperation. The authors would lastly like to extend thanks to Natasja Van Gestel and Heath Grizzle from Texas Tech University for their continued support as friends and peers throughout this research endeavor both in the field and in the lab.

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Authors and Affiliations

  1. Department of Biological Sciences, Texas Tech University, Lubbock, TX, 79409-3131, USA

    Colin W. Bell, Nancy E. McIntyre, David T. Tissue & John C. Zak

  2. Wind Erosion and Water Conservation Unit, USDA, 3810 4th Street, Lubbock, TX, 79415, USA

    Veronica Acosta-Martinez

  3. The Institute for Environment and Human Health, Texas Tech University, Lubbock, TX, 79409-3131, USA

    Stephen Cox

  4. Centre for Plant and Food Science, University of Western Sydney, Richmond, NSW, 2753, Australia

    David T. Tissue

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  1. Colin W. Bell
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  2. Veronica Acosta-Martinez
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  3. Nancy E. McIntyre
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  4. Stephen Cox
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  5. David T. Tissue
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Correspondence to Colin W. Bell.

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Bell, C.W., Acosta-Martinez, V., McIntyre, N.E. et al. Linking Microbial Community Structure and Function to Seasonal Differences in Soil Moisture and Temperature in a Chihuahuan Desert Grassland. Microb Ecol 58, 827–842 (2009). https://doi.org/10.1007/s00248-009-9529-5

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