Historical Drought Affects Microbial Population Dynamics and Activity During Soil Drying and Re-Wet


A history of drought exposure promoted by variable precipitation regimes can select for drought-tolerant soil microbial taxa, but the mechanisms of survival and death of microbial populations through the selective stresses of soil drying and re-wet are not well understood. We subjected soils collected from a 15-year field drought experiment (“Altered” precipitation history with extended dry periods, versus the “Ambient” field control) to a laboratory drying/re-wetting experiment, to learn whether selective population survival, death, or maintenance of protein synthesis potential and microbial respiration through variable soil water conditions was affected by field drought legacy. Microbial community composition, as measured by Illumina MiSeq sequencing of the 16S rRNA and 16S rRNA gene, shifted with laboratory drying/re-wet and field drought treatments. In Ambient soils, there was a higher proportion of reduced OTU abundance (indicative of mortality) during re-wet, whereas Altered soils had a greater proportion of stable OTU populations that did not change in abundance (indicative of survival) through drying/re-wet. Altered soils also had a lower proportion of rRNA:rRNA genes (lower protein synthesis potential) during dry-down, a greater weighted mean rRNA operon number (potential growth rate and r-selection) which was associated with higher abundance of Firmicutes (order Bacillales), and lower average microbial respiration rates. These data demonstrate that soils with a weaker historical drought legacy exhibit a higher prevalence of microbial water-stress mortality and differential survival and death at OTU levels following short-term dryingand re-wetting, concurrent with higher carbon loss potential. This work provides novel insight into the mechanisms and consequences of soil microbial changes resulting from extended drought conditions.

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  1. 1.

    Austin AT, Yahdjian L, Stark JM, Belnap J, Porporato A, Norton U, Ravetta DA, Schaeffer SM (2004) Water pulses and biogeochemical cycles in arid and semiarid ecosystems. Oecologia 141:221–235

    PubMed  Google Scholar 

  2. 2.

    Schimel JP, Gulledge JM, Clein-Curley JS, Lindstrom JE, Braddock JF (1999) Moisture effects on microbial activity and community structure in decomposing birch litter in the Alaskan taiga. Soil Biol Biochem 31:831–838

    CAS  Google Scholar 

  3. 3.

    Huxman TE, Snyder KA, Tissue D, Leffler AJ, Ogle K, Pockman WT, Sandquist DR, Potts DL, Schwinning S (2004) Precipitation pulses and carbon fluxes in semiarid and arid ecosystems. Oecologia 141:254–268

    PubMed  Google Scholar 

  4. 4.

    Ma S, Baldocchi DD, Hatala JA, Detto M, Yuste JC (2012) Are rain-induced ecosystem respiration pulses enhanced by legacies of antecedent photodegradation in semi-arid environments? Agric For Meteorol 154:203–213

    Google Scholar 

  5. 5.

    Harper CW, Blair JM, Fay PA, Knapp AK, Carlisle JD (2005) Increased rainfall variability and reduced rainfall amount decreases soil CO2 flux in a grassland ecosystem. Glob Chang Biol 11:322–334

    Google Scholar 

  6. 6.

    Huntington TG (2006) Evidence for intensification of the global water cycle: review and synthesis. J Hydrol 319:83–95

    Google Scholar 

  7. 7.

    Knapp AK, Beier C, Briske DD, Classen AT, Luo Y, Reichstein M et al (2008) Consequences of more extreme precipitation regimes for terrestrial ecosystems. AIBS Bull 58:811–821

    Google Scholar 

  8. 8.

    Intergovernmental Panel on Climate Change (2014) Climate change 2014: synthesis report. In: Pachauri RK, Meyer LA (eds) Contribution of working groups I, II and III to the fifth assessment report of the intergovernmental panel on climate change. Geneva, Switzerland.

  9. 9.

    Meisner A, Rousk J, Bååth E (2015) Prolonged drought changes the bacterial growth response to rewetting. Soil Boil Biochem 88:314–322

    CAS  Google Scholar 

  10. 10.

    Hawkes CV, Keitt TH (2015) Resilience vs. historical contingency in microbial responses to environmental change. Ecol Lett 18:612–625

    PubMed  Google Scholar 

  11. 11.

    Schimel J, Balser TC, Wallenstein M (2007) Microbial stress-response physiology and its implications for ecosystem function. Ecology 88:1386–1394

    PubMed  Google Scholar 

  12. 12.

    Schimel JP, Schaeffer SM (2012) Microbial control over carbon cycling in soil. Front Microbiol 3. https://doi.org/10.3389/fmicb.2012.00348

  13. 13.

    Manzoni S, Schimel JP, Porporato A (2012) Reponses of soil microbial communities to water-stress: results from a meta-analysis. Ecology 93:930–938

    PubMed  Google Scholar 

  14. 14.

    Birch HF (1958) The effect of soil drying on humus decomposition and nitrogen availability. Plant Soil 10:9–31

    CAS  Google Scholar 

  15. 15.

    Fierer N, Schimel JP, Holden PA (2003) Influence of drying-rewetting frequency on soil bacterial community structure. Microb Ecol 45:63–71

    CAS  PubMed  Google Scholar 

  16. 16.

    Evans SE, Dieckmann U, Franklin O, Kaiser C (2016) Synergistic effects of diffusion and microbial physiology reproduce the Birch effect in a micro-scale model. Soil Biol Biochem 93:28–37

    CAS  Google Scholar 

  17. 17.

    Göransson H, Godbold DL, Jones DL, Rousk J (2013) Bacterial growth and respiration responses upon rewetting dry forest soils: impact of drought-legacy. Soil Biol Biochem 57:477–486

    Google Scholar 

  18. 18.

    Hawkes CV, Waring BG, Rocca JD, Kivlin SN (2017) Historical climate controls soil respiration responses to current soil moisture. Proc Natl Acad Sci U S A. https://doi.org/10.1073/pnas.1620811114

  19. 19.

    Evans SE, Wallenstein MD (2014) Climate change alters ecological strategies of soil bacteria. Ecol Lett 17:155–164

    PubMed  Google Scholar 

  20. 20.

    Wood JM, Bremer E, Csonka LN, Kraemer R, Poolman B, van der Heide T, Smith LT (2001) Osmosensing and osmoregulatory compatible solute accumulation by bacteria. Comp Biochem Phys A 130:437–460

    CAS  Google Scholar 

  21. 21.

    Manzoni S, Schaeffer SM, Katul G, Porporato A, Schimel JP (2014) A theoretical analysis of microbial eco-physiological and diffusion limitations to carbon cycling in drying soils. Soil Biol Biochem 73:69–83

    CAS  Google Scholar 

  22. 22.

    Evans SE, Wallenstein MD (2012) Soil microbial community response to drying and rewetting stress: does historical precipitation regime matter? Biogeochemistry 109:101–116

    Google Scholar 

  23. 23.

    Zeglin LH, Bottomley PJ, Jumpponen A, Rice CW, Arango M, Lindsley A, McGowan A, Mfombep P, Myrold DD (2013) Altered precipitation regime affects the function and composition of soil microbial communities on multiple time scales. Ecology 94:2334–2345

    CAS  PubMed  Google Scholar 

  24. 24.

    Meisner A, Jacquiod S, Snoek BL, Ten Hooven FC, Van Der Putten WH (2018) Drought legacy effects on the composition of soil fungal and prokaryote communities. Front Microbiol 9. https://doi.org/10.3389/fmicb.2018.00294

  25. 25.

    Shade A, Peter H, Allison SD, Baho DL, Berga M, Bürgmann H, Huber DH, Langenheder S, Lennon JT, Martiny JBH, Matulich KL, Schmidt TM, Handelsman J (2012) Fundamentals of microbial community resistance and resilience. Front Microbiol 3. https://doi.org/10.3389/fmicb.2012.00417

  26. 26.

    Martiny JBH, Martiny AC, Weihe C, Lu Y, Berlemont R, Brodie EL, Goulden ML, Treseder KK, Allison SD (2017) Microbial legacies alter decomposition in response to simulated global change. ISME J 11:490–499

    PubMed  Google Scholar 

  27. 27.

    Bouskill NJ, Lim HS, Borglin S, Salve R, Wood TE, Silver WL et al (2013) Pre-exposure to drought increases the resistance of tropical forest soil bacterial communities to extended drought. ISME J 7:384–394

    CAS  PubMed  Google Scholar 

  28. 28.

    Andrade-Linares DR, Lehmann A, Rillig MC (2016) Microbial stress priming: a meta-analysis. Environ Microbiol 18:1277–1288

    PubMed  Google Scholar 

  29. 29.

    Lennon JT, Aanderud ZT, Lehmkuhl BK, Schoolmaster DR (2012) Mapping the niche space of soil microorganisms using taxonomy and traits. Ecology 93:1867–1879

    PubMed  Google Scholar 

  30. 30.

    Litchman E, Klausmeier CA (2008) Trait-based community ecology of phytoplankton. Annu Rev Ecol Syst 39:615–639

    Google Scholar 

  31. 31.

    Lennon JT, Jones SE (2011) Microbial seed banks: the ecological and evolutionary implications of dormancy. Nat Rev Microbiol 9:119–130

    CAS  PubMed  Google Scholar 

  32. 32.

    Blazewicz SJ, Barnard RL, Daly RA, Firestone MK (2013) Evaluating rRNA as an indicator of microbial activity in environmental communities: limitations and uses. ISME J 7:2061–2068

    CAS  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Roller BK, Stoddard SF, Schmidt TM (2016) Exploiting rRNA operon copy number to investigate bacterial reproductive strategies. Nat Microbiol. https://doi.org/10.1038/nmicrobiol.2016.160

  34. 34.

    Klappenbach JA, Dunbar JM, Schmidt TM (2000) rRNA operon copy number reflects ecological strategies of bacteria. Appl Environ Microbiol 66:1328–1333

    CAS  PubMed  PubMed Central  Google Scholar 

  35. 35.

    Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821

    CAS  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Nemergut DR, Knelman JE, Ferrenburg S, Bilinski T, Melbourne B, Jiang L et al (2016) Decreases in average bacterial community rRNA operon copy number during succession. ISME J 10:1147–1156

    CAS  PubMed  Google Scholar 

  37. 37.

    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 U S A 109:10931–10936

    CAS  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Hayden BP (1998) Regional climate and the distribution of tallgrass prairie. In: Knapp AK, Briggs JM, Hartnet DC, Collins SL (eds) Grassland dynamics: long-term ecological research in tallgrass prairie. Oxford University Press, New York, pp 19–34

    Google Scholar 

  39. 39.

    Fay PA, Carlisle JD, Knapp AK, Blair JM, Collins SL (2000) Altering rainfall timing and quantity in a mesic grassland ecosystem: design and performance of rainfall manipulation shelters. Ecosystems 3:308–319

    Google Scholar 

  40. 40.

    Fay PA, Blair JM, Smith MD, Nippert JB, Carlisle JD, Knapp AK (2011) Relative effects of precipitation variability and warming on tallgrass prairie ecosystem function. Biogeosciences 8:3053–3068

    CAS  Google Scholar 

  41. 41.

    Zeglin LH, Myrold DD (2013) Fate of decomposed fungal cell wall material in organic horizons of old-growth Douglas-fir forest soils. Soil Sci Soc Am J 77:489–500

    CAS  Google Scholar 

  42. 42.

    DeAngelis KM, Silver WL, Thompson AW, Firestone MK (2010) Microbial communities acclimate to recurring changes in soil redox potential status. Environ Microbiol 12:3137–3149

    CAS  PubMed  Google Scholar 

  43. 43.

    Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Huntley J, Fierer N et al (2012) Ultra-high-throughput microbial community analysis on the Illumina HiSeq and MiSeq platforms. ISME J 6:1621–1624

    CAS  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Fierer N, Jackson JA, Vilgalys R, Jackson RB (2005) Assessment of soil microbial community structure by use of taxon-specific quantitative PCR assays. Appl Environ Microbiol 71:4117–4120

    CAS  PubMed  PubMed Central  Google Scholar 

  45. 45.

    Zeglin LH, Wang B, Waythomas C, Rainey F, Talbot SL (2016) Organic matter quantity and source affect microbial community structure and function following volcanic eruption on Kasatochi Island, Alaska. Environ Microbiol 18:146–158

    CAS  PubMed  Google Scholar 

  46. 46.

    Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336

    CAS  PubMed  PubMed Central  Google Scholar 

  47. 47.

    Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267

    CAS  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Gloor GB, Macklaim JM, Pawlowsky-Glahn V, Egozcue JJ (2017) Microbiome datasets are compositional and this is not optional. Front Microbiol 8. https://doi.org/10.3389/fmicb.2017.02224

  49. 49.

    Fierer N, Barberán A, Laughlin DC (2014) Seeing the forest for the genes: using metagenomics to infer the aggregated traits of microbial communities. Front Microbiol. https://doi.org/10.3389/fmicb.2014.00614

  50. 50.

    Garnier E, Cortez J, Billès G, Navas M, Roumet C, Debussche M et al (2004) Plant functional markers capture ecosystem properties during secondary succession. Ecology 85:2630–2637

    Google Scholar 

  51. 51.

    Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:1442–9993

    Google Scholar 

  52. 52.

    Pinherio J, Bates D, DebRoy S, Sarkar D, Heisterkamp S, Van Willigen B (2017) nlme: linear and nonlinear mixed effects models. R package version 3.1-131. https://CRAN.R-project.org/package-nlme

  53. 53.

    Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference of general parametric models. Biom J 50:346–363

    PubMed  Google Scholar 

  54. 54.

    Oksanen J, Blanchet FG, Friendly M, Kindt R, Legendre P, McGlinn D et al (2017) vegan: community ecology package. R package version 2.4-3. https://CRAN.R-project.org/package=vegan.

  55. 55.

    Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. https://doi.org/10.1186/s13059-014-0550-8

  56. 56.

    Yuste JC, Peñuelas J, Estiarte M, Garcia-Mas J, Mattana S, Ogaya R et al (2011) Drought-resistant fungi control soil organic matter decomposition and its response to temperature. Glob Chang Biol 17:1475–1486

    Google Scholar 

  57. 57.

    Fuchslueger L, Bahn M, Fritz K, Hasibeder R, Richter A (2014) Experimental drought reduces the transfer of recently fixed plant carbon to soil microbes and alters the bacterial community composition in a mountain meadow. New Phytol 201:916–927

    CAS  PubMed  Google Scholar 

  58. 58.

    Nunan N, Wu K, Young IM, Crawford JW, Ritz K (2002) In situ spatial patterns of soil bacterial populations, mapped at multiples scales, in an arable soil. Microb Ecol 44:296–305

    CAS  PubMed  Google Scholar 

  59. 59.

    Youssef NN, Couger MB, Elshahed MS (2010) Fine-scale bacterial beta diversity within a complex ecosystem (Zoldletone Spring, OK, USA): the role of the rare biosphere. PLoS One. https://doi.org/10.1371/journal.pone.0012414

  60. 60.

    O’Brien SL, Gibbons SM, Owens SM, Hampton-Marcell J, Johnston ER, Jastrow JD et al (2016) Spatial scale drives patterns in soil bacterial diversity. Environ Microbiol 18:2039–2051

    PubMed  PubMed Central  Google Scholar 

  61. 61.

    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. Madison, American Society of Agronomy, pp p23–p95

    Google Scholar 

  62. 62.

    Davinic M, Fultz LM, Acosta-Martinez V, Calderón FJ, Cox SB, Dowd SE, Allen VG, Zak JC, Moore-Kucera J (2012) Pyrosequencing and mid-infrared spectroscopy reveal distinct aggregate stratification of soil bacterial communities and organic matter composition. Soil Biol Biochem 46:63–72

    CAS  Google Scholar 

  63. 63.

    Bond-Lamberty B, Bolton H, Fansler S, Heredia-Langner A, Liu C, McCue LE, Smith J, Bailey V (2016) Soil respiration and bacterial structure and function after 17 years of a reciprocal soil transplant experiment. PLoS One. https://doi.org/10.1371/journal.pone.0150599

  64. 64.

    Williams MA, Rice CW (2007) Seven years of enhanced water availability influences the physiological, structural, and functional attributes of a soil microbial community. Appl Soil Ecol 35:535–545

    Google Scholar 

  65. 65.

    Pesaro M, Widmer F, Nicollier G, Zeyer J (2003) Effects of freeze-thaw stress during soil storage on microbial communities and methidathion degradation. Soil Biol Biochem 35:1049–1061

    CAS  Google Scholar 

  66. 66.

    Lee YB, Lorenz N, Dick LK, Dick RP (2007) Cold storage and pretreatment incubation effects on soil microbial properties. Soil Sci Soc Am J 71:1299–1305

    CAS  Google Scholar 

  67. 67.

    Allison SD, Goulden ML (2017) Consequences of drought tolerance traits on microbial decomposition in the DEMENT model. Soil Biol Biochem 107:104–113

    CAS  Google Scholar 

  68. 68.

    Blazewicz SJ, Schwartz E, Firestone MK (2014) Growth and death of bacteria and fungi underlie rainfall-induced carbon dioxide pulses from seasonally dried soil. Ecology 95:1162–1172

    PubMed  Google Scholar 

  69. 69.

    Stoddard SF, Smith BJ, Hein R, Roller BR, Schmidt TM (2015) rrnDB: improved tools for interpreting rNRA gene abundance in bacteria and archaea and a new foundation for future development. Nucleic Acids Res 43:593–598

    Google Scholar 

  70. 70.

    Potts M (1994) Dessication tolerance of prokaryotes. Microbiol Rev 58:755–805

    CAS  PubMed  PubMed Central  Google Scholar 

  71. 71.

    Volaire F (2018) A unified framework of plant adaptive strategies to drought: crossing scales and disciplines. Glob Chang Biol. https://doi.org/10.1111/gcb.14062

  72. 72.

    Meisner A, Leizeaga A, Rousk J, Bååth E (2017) Partial drying accelerates bacterial growth recovery to rewetting. Soil Biol Biochem 112:269–276

    CAS  Google Scholar 

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Thank you to the Konza Prairie Biological Station and the Long-Term Ecological Research program personnel who have maintained the RaMPs long-term field experiment; to Becky Malanchuk, Eduardo Santos, and Kyle Stropes for laboratory assistance; to Alina Akhunova and Yanni Lun at the K-State Integrated Genomics Facility; and to Drs. Myrold, Bottomley, Nippert, and Blair for supportive conversation on microbial and plant drought tolerance. We appreciate the thoughtful feedback of all reviewers of this manuscript.


This work was supported by a Kansas-NSF-EPSCoR FIRST grant (a sub-award of NSF #EPS-0903806) and support from the State of Kansas Board of Regents to LHZ. This report is based upon work supported by the National Science Foundation under award no. EPS-0903806 and the State of Kansas through the Kansas Board of Regents.

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Correspondence to Lydia H. Zeglin.

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Veach, A.M., Zeglin, L.H. Historical Drought Affects Microbial Population Dynamics and Activity During Soil Drying and Re-Wet. Microb Ecol 79, 662–674 (2020). https://doi.org/10.1007/s00248-019-01432-5

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  • Drought
  • Soil
  • Microbial community
  • Drying/re-wet
  • Bacteria