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.
KeywordsDrought Soil Microbial community Drying/re-wet Bacteria
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.
- 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 58:811–821Google Scholar
- 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.Google Scholar
- 12.Schimel JP, Schaeffer SM (2012) Microbial control over carbon cycling in soil. Front Microbiol 3. https://doi.org/10.3389/fmicb.2012.00348
- 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
- 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.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
- 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
- 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 19–34Google Scholar
- 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 7:335–336CrossRefGoogle Scholar
- 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.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
- 51.Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:1442–9993Google Scholar
- 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
- 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.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
- 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
- 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–p95Google Scholar
- 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 46:63–72CrossRefGoogle Scholar
- 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
- 70.Potts M (1994) Dessication tolerance of prokaryotes. Microbiol Rev 58:755–805Google Scholar
- 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