Abstract
Arizona and New Mexico receive half of their annual precipitation during the summer monsoon season, making this large-scale rain event critical for ecosystem productivity. We used the monsoon rains to explore the responses of soil bacterial and fungal communities to natural moisture pulses in a semiarid grassland. Through 454 pyrosequencing of the 16S rRNA gene and ITS region, we phylogenetically characterized these communities at 22 time points during a summer season. Relative humidity increased before the rains arrived, creating conditions in soil that allowed for the growth of microorganisms. During the course of the study, the relative abundances of most bacterial phyla showed little variation, though some bacterial populations responded immediately to an increase in soil moisture once the monsoon rains arrived. The Firmicutes phylum experienced over a sixfold increase in relative abundance with increasing water availability. Conversely, Actinobacteria, the dominant taxa at our site, were negatively affected by the increase in water availability. No relationship was found between bacterial diversity and soil water potential. Bacterial community structure was unrelated to all environmental variables that we measured, with the exception of a significant relationship with atmospheric relative humidity. Relative abundances of fungal phyla fluctuated more throughout the season than bacterial abundances did. Variation in fungal community structure was unrelated to soil water potential and to most environmental variables. However, ordination analysis showed a distinct fungal community structure late in the season, probably due to plant senescence.
Similar content being viewed by others
References
Bryson R, Lowry WP (1955) Synoptic climatology of the Arizona summer precipitation singularity. Bull Am Meteorol Soc 36:329–339
Adams DK, Comrie AC (1997) The North American monsoon. Bull Am Meteorol Soc 78:2197–2213
Hales JE (1972) Surges of maritime tropical air northward over the Gulf of California. Mon Weather Rev 100:298–306
Brenner IS (1974) A surge of maritime tropical air—Gulf of California to the southwestern United States. Mon Weather Rev 102:375–389
Climate Assessment for the Southwest. University of Arizona. http://www.climas.arizona.edu/sw-climate/monsoon. Accessed 30 Nov 2012
Seager R, Ting M, Held I, Kushnir Y, Lu J, Vecci G et al (2007) Model projections of an imminent transition to a more arid climate in southwestern North America. Science 316:1181–1184
Southwest Climate Change Network. Institute of the Environment, University of Arizona. http://www.southwestclimatechange.org/climate/southwest/precipitation-changes. Accessed 15 Jan 2013
Harris RF (1981) Effect of water potential on microbial growth and activity. In: Parr JF, Gardner WR, Elliott LF (eds) Water potential relations in soil microbiology. Soil Science Society of America, Madison, pp 23–95
Lynch JM, Whipps JM (1990) Substrate flow in the rhizosphere. Plant Soil 129:1–10
Griffin DM (1981) Water and microbial stress. Adv Microb Ecol 5:91–136
Schimel JP, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394
Griffin DM (1981) Water potential as a selective factor in the microbial ecology of soils. In: Parr JF, Gardner WR, Elliott LF (eds) Water potential relations in soil microbiology. Soil Science Society of America, Madison, pp 141–151
Castro HF, Classen AT, Austin EE, Norby RJ, Schadt CW (2010) Soil microbial community responses to multiple experimental change drivers. Appl Environ Microbiol 76:999–1007
Cregger MA, Schadt CW, McDowell NG, Pockman WT, Classen AT (2012) Response of the soil microbial community to changes in precipitation in a semiarid ecosystem. Appl Environ Microbiol 78:8587–8594
Griffiths RI, Whiteley AS, O’Donnell AG, Bailey MJ (2003) Physiological and community responses of established grassland bacterial populations to water stress. Appl Environ Microbiol 69:6961–6968
Williams MA (2007) Response of microbial communities to water stress in irrigated and drought-prone tallgrass prairie soils. Soil Biol Biochem 39:2750–2757
Cruz-Martinez K, Suttle KB, Brodie EL, Power ME, Andersen GL, Banfield JF (2009) Despite strong seasonal responses, soil microbial consortia are more resilient to long-term changes in rainfall than overlying grassland. ISME J 3:738–744
Landesman WJ, Dighton J (2010) Response of soil microbial communities and the production of plant-available nitrogen to a two-year rainfall manipulation in the New Jersey Pinelands. Soil Biol Biochem 42:1751–1758
Fierer N, Schimel JP, Holden PA (2003) Influence of drying-rewetting frequency on soil bacterial community structure. Microb Ecol 45:63–71
Allison SD, Martiny JBH (2008) Resistance, resilience, and redundancy in microbial communities. Proc Natl Acad Sci 105:11512–11519
Taylor DR (1983) Soil survey of Coconino County Area Arizona, central part. United States Department of Agriculture, Soil Conservation Service in Cooperation with Arizona Agricultural Experiment Station, Washington
Dowd SE, Callaway TR, Wolcott RD, Sun Y, McKeehan T, Hagevoort RG et al (2008) Evaluation of the bacterial diversity in the feces of cattle using 16S rRNA bacterial tag-encoded FLX amplicon pyrosequencing. BMC Microbiol 8:125
Acosta-Martinez V, Dowd S, Sun Y, Allen V (2008) Tag-encoded pyrosequencing analysis of bacterial diversity in a single soil type as affected by management and land use. Soil Biol Biochem 40:2762–2770
Brookes PC, Landman A, Pruden G, Jenkinson DS (1985) Chloroform fumigation and the release of soil nitrogen, a rapid direct extraction method to measure microbial biomass nitrogen in soil. Soil Biol Biochem 17:837–842
Haubensak KA, Hart SC, Stark JM (2002) Influences of chloroform exposure time and soil water content on C and N release in forest soils. Soil Biol Biochem 34:1549–1562
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK et al (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336
Fierer N, Hamady M, Lauber CL, Knight R (2008) The influence of sex, handedness, and washing on the diversity of hand surface bacteria. Proc Natl Acad Sci 105:17994–17999
Lauber CL, Hamady M, Knight R, Fierer N (2009) Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol 75:5111–5120
Evans S, Wallenstein MD (2012) Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter? Biogeochemistry 109:101–116
Edgar RC (2010) Search and clustering orders of magnitude faster than BLAST. Bioinformatics 26:2460–2461
Caporaso JG, Bittinger K, Bushman FD, DeSantis TZ, Andersen GL, Knight R (2010) PyNAST: a flexible tool for aligning sequences to a template alignment. Bioinformatics 26:266–267
Faith DP, Baker AM (2007) Phylogenetic diversity (PD) and biodiversity conservation: some bioinformatics challenges. Evol Bioinformatics Online 2:121–128
Lozupone C, Knight R (2005) UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71:8228–8235
Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:1–9
Dai A (2012) Increasing drought under global warming in observations and models. Nat Clim Chang 3:52–58
Adair KL, Schwartz E (2008) Evidence that ammonia-oxidizing archaea are more abundant than ammonia-oxidizing bacteria in semiarid soils of Northern Arizona, USA. Microb Ecol 56:420–426
Dijkstra P, Menyailo OV, Doucett RR, Hart SC, Schwartz E, Hungate BA (2006) C and N availability affects the 15N natural abundance of the soil microbial biomass across a cattle manure gradient. Eur J Soil Sci 57:468–475
Schwartz E, Blazewicz S, Doucett R, Hungate BA, Hart SC, Dijkstra P (2007) Natural abundance of δ15N and δ13C of DNA extracted from soil. Soil Biol Biochem 39:3101–3107
Dijkstra P, Thomas SC, Heinrich PL, Koch GW, Schwartz E, Hungate BA (2011) Effect of temperature on metabolic activity of intact microbial communities: evidence for altered metabolic pathway activity but not for increased maintenance respiration and reduced carbon use efficiency. Soil Biol Biochem 43:2023–2031
Cameron RE, Conrow HP (1969) Soil moisture, relative humidity, and microbial abundance in dry valleys of southern Victoria Land. Antarct J US 4:23–28
Austin AT, Yahdjian ML, Stark JM, Belnap J, Porporato A, Norton U et al (2004) Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141:221–235
Schwinning S, Sala OE (2004) Hierarchy of responses to resource pulses in arid and semi-arid ecosystems. Oecologia 141:211–220
Reynolds JF, Kemp PR, Ogle K, Fernandez RJ (2004) Modifying the “pulse-reserve” paradigm for deserts of North America: precipitation pulses, soil water and plant responses. Oecologia 141:194–210
Collins SL, Sinsabaugh RL, Crenshaw C, Green L, Porras-Alfaro A, Stursova M, Zeglin LH (2008) Pulse dynamics and microbial processes in aridland ecosystems. J Ecol 96:413–420
Borken W, Matzner E (2009) Reappraisal of drying and wetting effects on C and N mineralization and fluxes in soils. Glob Chang Biol 15:808–824
Parker SS, Schimel JP (2011) Soil nitrogen availability and transformations differ between the summer and the growing season in a California grassland. Appl Soil Ecol 48:185–192
Clarholm M (1981) Protozoan grazing of bacteria in soil—impact and importance. Microb Ecol 7:343–350
Bernard RL, Osborne CA, Firestone ME (2013) Responses of soil bacterial and fungal communities to extreme desiccation and rewetting. ISME J 7:2229–2241
Placella SA, Brodie EL, Firestone MK (2012) Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups. Proc Natl Acad Sci 109:10931–10936
Youssef N, Sheik CS, Krumholz LR, Najar FZ, Roe BA, Elshahed MS (2009) Comparison of species richness estimates obtained using nearly complete fragments and simulated pyrosequencing-generated fragments in 16S rRNA gene-based environmental surveys. Appl Environ Microbiol 75:5227–5236
Alvarez HM, Silva RA, Cesari AC, Zamit AL, Peressutti SR, Reichelt R, Keller U, Malkus U, Rasch C, Maskow T, Mayer F, Steinbüchel A (2004) Physiological and morphological responses of the soil bacterium Rhodococcus opacus strain PD630 to water stress. FEMS Microbiol Ecol 50:75–86
LeBlanc JC, Goncalves ER, Mohn WW (2008) Global response to desiccation stress in the soil actinomycete Rhodococcus jostii RHA1. Appl Environ Microbiol 74:2627–2636
Acknowledgments
A National Science Foundation CAREER Award (EF-0747397) to E Schwartz funded this research. T McHugh was supported by a National Science Foundation IGERT Fellowship (DGE-0549505). We thank Paul Dijkstra and Amy Welty-Bernard for the lab assistance and helpful suggestions.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Fig. S1
Visual observations of the grassland before (Julian Day 174), during (Julian Day 201), and after (Julian Day 224) monsoon rains (PPTX 616 kb)
Fig. S2
A moisture release curve for our clay soil (PPTX 39 kb)
Fig. S3
Nitrate and ammonium concentrations during the study period.Error bars are standard error for means (n = 5) (PPTX 43 kb)
Rights and permissions
About this article
Cite this article
McHugh, T.A., Koch, G.W. & Schwartz, E. Minor Changes in Soil Bacterial and Fungal Community Composition Occur in Response to Monsoon Precipitation in a Semiarid Grassland. Microb Ecol 68, 370–378 (2014). https://doi.org/10.1007/s00248-014-0416-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00248-014-0416-3