Growth and death of bacteria and fungi underlie rainfall-induced carbon dioxide pulses from seasonally dried soil.

The rapid increase in microbial activity that occurs when a dry soil is rewetted has been well documented and is of great interest due to implications of changing precipitation patterns on soil C dynamics. Several studies have shown minor net changes in microbial population diversity or abundance following wet-up, but the gross population dynamics of bacteria and fungi resulting from soil wet-up are virtually unknown. Here we applied DNA stable isotope probing with H218O coupled with quantitative PCR to characterize new growth, survival, and mortality of bacteria and fungi following the rewetting of a seasonally dried California annual grassland soil. Microbial activity, as determined by CO2 production, increased significantly within three hours of wet-up, yet new growth was not detected until after three hours, suggesting a pulse of nongrowth activity immediately following wet-up, likely due to osmo-regulation and resuscitation from dormancy in response to the rapid change in water potential. Total microbial abundance revealed little change throughout the seven-day post-wet incubation, but there was substantial turnover of both bacterial and fungal populations (49% and 52%, respectively). New growth was linear between 24 and 168 hours for both bacteria and fungi, with average growth rates of 2.3 x 10(8) bacterial 16S rRNA gene copies x [g dry mass](-1) x h(-1) and 4.3 x 10(7) fungal ITS copies x [g dry mass](-1) x h(-1). While bacteria and fungi differed in their mortality and survival characteristics during the seven-day incubation, mortality that occurred within the first three hours was similar, with 25% and 27% of bacterial and fungal gene copies disappearing from the pre-wet community, respectively. The rapid disappearance of gene copies indicates that cell death, occurring either during the extreme dry down period (preceding five months) or during the rapid change in water potential due to wet-up, generates a significant pool of available C that likely contributes to the large pulse in CO2 associated with wet-up. A dynamic assemblage of growing and dying organisms controlled the CO2 pulse, but the balance between death and growth resulted in relatively stable total population abundances, even after a profound and sudden change in environment.

[1]  David L. Jones,et al.  Bacterial growth and respiration responses upon rewetting dry forest soils: Impact of drought-legacy , 2013 .

[2]  Claudia M. Boot,et al.  Static osmolyte concentrations in microbial biomass during seasonal drought in a California grassland , 2013 .

[3]  Mark A. Williams,et al.  Microbial community response to varying magnitudes of desiccation in soil: A test of the osmolyte accumulation hypothesis , 2013 .

[4]  Andreas Richter,et al.  Environmental and stoichiometric controls on microbial carbon-use efficiency in soils. , 2012, The New phytologist.

[5]  Eoin L. Brodie,et al.  Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups , 2012, Proceedings of the National Academy of Sciences.

[6]  R. Vargas,et al.  Precipitation variability and fire influence the temporal dynamics of soil CO2 efflux in an arid grassland , 2012 .

[7]  R. Vargas,et al.  Effects of soil rewetting and thawing on soil gas fluxes: a review of current literature and suggestions for future research , 2011 .

[8]  J. Rousk,et al.  Growth of saprotrophic fungi and bacteria in soil. , 2011, FEMS microbiology ecology.

[9]  J. Lennon,et al.  Validation of Heavy-Water Stable Isotope Probing for the Characterization of Rapidly Responding Soil Bacteria , 2011, Applied and Environmental Microbiology.

[10]  S. Trumbore,et al.  Drying/rewetting cycles mobilize old C from deep soils from a California annual grassland , 2011 .

[11]  Karen L. Adair,et al.  Stable isotope probing with 18O-water to investigate growth and mortality of ammonia oxidizing bacteria and archaea in soil. , 2011, Methods in enzymology.

[12]  K. Xia,et al.  Characterization of the water soluble soil organic pool following the rewetting of dry soil in a drought-prone tallgrass prairie , 2009 .

[13]  E. Bååth,et al.  Effect of drying and rewetting on bacterial growth rates in soil. , 2008, FEMS microbiology ecology.

[14]  J. Rousk,et al.  Fungal biomass production and turnover in soil estimated using the acetate-in-ergosterol technique , 2007 .

[15]  Karen L. Adair,et al.  Bacterial community structure correlates with decomposition parameters along a Hawaiian precipitation gradient , 2007 .

[16]  Michael Wagner,et al.  Who eats what, where and when? Isotope-labelling experiments are coming of age , 2007, The ISME Journal.

[17]  R. B. Jackson,et al.  Toward an ecological classification of soil bacteria. , 2007, Ecology.

[18]  Josh D Neufeld,et al.  DNA stable-isotope probing , 2007, Nature Protocols.

[19]  S. Hsu,et al.  Stable Isotope Probing with 15N Achieved by Disentangling the Effects of Genome G+C Content and Isotope Enrichment on DNA Density , 2007, Applied and Environmental Microbiology.

[20]  P. Bodegom.  Microbial Maintenance: A Critical Review on Its Quantification , 2007, Microbial Ecology.

[21]  E. Schwartz.  Characterization of Growing Microorganisms in Soil by Stable Isotope Probing with H218O , 2007, Applied and Environmental Microbiology.

[22]  B. Jørgensen,et al.  The future of single-cell environmental microbiology. , 2007, Environmental microbiology.

[23]  M. Firestone,et al.  Seasonal Dynamics of Microbial Community Composition and Function in Oak Canopy and Open Grassland Soils , 2006, Microbial Ecology.

[24]  R. B. Jackson,et al.  Assessment of Soil Microbial Community Structure by Use of Taxon-Specific Quantitative PCR Assays , 2005, Applied and Environmental Microbiology.

[25]  J. Goksøyr,et al.  Effects of water fluctuations on microbial mass and activity in soil , 1980, Microbial Ecology.

[26]  H. Birch.  The effect of soil drying on humus decomposition and nitrogen availability , 1958, Plant and Soil.

[27]  Jianwu Tang,et al.  How soil moisture, rain pulses, and growth alter the response of ecosystem respiration to temperature , 2004 .

[28]  L. Tranvik,et al.  Ergosterol as a measure of living fungal biomass: persistence in environmental samples after fungal death. , 2004, Journal of microbiological methods.

[29]  X. Lee,et al.  Rapid and transient response of soil respiration to rain , 2004 .

[30]  J. Stark,et al.  Microbial dynamics and carbon and nitrogen cycling following re-wetting of soils beneath two semi-arid plant species , 2004, Oecologia.

[31]  H. Šantrůčková,et al.  Growth rate of bacteria is affected by soil texture and extraction procedure , 2003 .

[32]  N. Fierer,et al.  Influence of Drying–Rewetting Frequency on Soil Bacterial Community Structure , 2002, Microbial Ecology.

[33]  E. Bååth.  Estimation of fungal growth rates in soil using 14C-acetate incorporation into ergosterol , 2001 .

[34]  M. Firestone,et al.  Release of Intracellular Solutes by Four Soil Bacteria Exposed to Dilution Stress , 2000 .

[35]  T. Schmidt,et al.  rRNA Operon Copy Number Reflects Ecological Strategies of Bacteria , 2000, Applied and Environmental Microbiology.

[36]  E. Bååth.  Growth Rates of Bacterial Communities in Soils at Varying pH: A Comparison of the Thymidine and Leucine Incorporation Techniques , 1998, Microbial Ecology.

[37]  E. Paul,et al.  Measurement of bacterial growth rates in soil , 1994 .

[38]  E. Bååth.  Thymidine incorporation into macromolecules of bacteria extracted from soil by homogenization-centrifugation , 1992 .

[39]  E. Davidson,et al.  Sources of nitrous oxide production following wetting of dry soil , 1991 .

[40]  E. Bååth.  Thymidine incorporation into soil bacteria. , 1990 .

[41]  J. Fuhrman,et al.  Relationships between Biovolume and Biomass of Naturally Derived Marine Bacterioplankton , 1987 .

[42]  M. Firestone,et al.  Microbial biomass response to a rapid increase in water potential when dry soil is wetted , 1987 .

[43]  S. Conti,et al.  Germination of Single Bacterial Spores , 1969, Journal of bacteriology.

[44]  D. Harcourt.  The Development and Use of Life Tables in the Study of Natural Insect Populations , 1969 .

[45]  P. Allen.  METABOLIC ASPECTS OF SPORE GERMINATION IN FUNGI , 1965 .

[46]  H. S. Levinson,et al.  CORRELATION OF RESPIRATORY ACTIVITY WITH PHASES OF SPORE GERMINATION AND GROWTH IN BACILLUS MEGATERIUM AS INFLUENCED BY MANGANESE AND l-ALANINE , 1956, Journal of bacteriology.

[47]  S. Waksman,et al.  PARTIAL STERILIZATION OF SOIL, MICROBIOLOGICAL ACTIVITIES AND SOIL FERTILITY: II , 1923 .

[48]  R. Pearl,et al.  Experimental Studies on the Duration of Life. I. Introductory Discussion of the Duration of Life in Drosophila , 1921, The American Naturalist.