Drought impacts on microbial trait distribution and feedback to soil carbon cycling

Malik, Ashish A.; Bouskill, Nicholas J.

doi:10.1111/1365-2435.14010

Title: Drought impacts on microbial trait distribution and feedback to soil carbon cycling

Abstract

Abstract Quantifying the impact of drought on microbial processes and its consequences for soil carbon cycling is hindered by the lack of underlying mechanistic understanding. Therefore, there is a need to scale up the physiological response to changing water status from individual soil microbes to collective communities across different ecosystems. Here we propose the use of a framework that incorporates trait‐based ecology to link drought‐impacted microbial processes to rates of soil carbon decomposition and stabilisation. We briefly synthesise existing knowledge on the effects of drought on microbial physiology at the individual to community scale, before integrating this understanding within a framework incorporating life‐history strategy, ecological strategy and biochemistry. This framework highlights a dynamic allocation to high yield (Y), resource acquisition (A) and stress tolerance (S) pathways as environmental conditions change. Y‐A‐S strategies represent sets of traits that tend to correlate due to physiological or evolutionary trade‐offs. This framework enables assessment of microbial processes along two key environmental gradients of water and resource availability, both of which are constrained by drought. The variable chemistry of biomass and necromass produced under different physiological strategies in response to drying–rewetting impacts organic matter decomposition and stabilisation in soils, and should also be considered whenmore »« less

Authors:

^[1]; Bouskill, Nicholas J. ^[2]

School of Biological Sciences University of Aberdeen Aberdeen UK
Climate and Ecosystem Sciences Division Lawrence Berkeley National Laboratory Berkeley California USA

Publication Date:: Sun Feb 06 00:00:00 EST 2022

Research Org.:: Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Org.:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

OSTI Identifier:: 1871355

Alternate Identifier(s):: OSTI ID: 1855202; OSTI ID: 1996437

Grant/Contract Number:: Early Career Research Program #FP00005182; DE‐SC0020382; AC02-05CH11231

Resource Type:: Published Article

Journal Name:: Functional Ecology

Additional Journal Information:: Journal Name: Functional Ecology Journal Volume: 36 Journal Issue: 6; Journal ID: ISSN 0269-8463

Publisher:: Wiley-Blackwell

Country of Publication:: United Kingdom

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES; drought; drying–rewetting; microbial traits; soil carbon; water stress

Citation Formats


                    Malik, Ashish A., and Bouskill, Nicholas J. Drought impacts on microbial trait distribution and feedback to soil carbon cycling.  United Kingdom: N. p., 2022. 
Web.  doi:10.1111/1365-2435.14010.

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                    Malik, Ashish A., & Bouskill, Nicholas J. Drought impacts on microbial trait distribution and feedback to soil carbon cycling.  United Kingdom.  https://doi.org/10.1111/1365-2435.14010

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                    Malik, Ashish A., and Bouskill, Nicholas J. Sun .  
"Drought impacts on microbial trait distribution and feedback to soil carbon cycling".  United Kingdom.  https://doi.org/10.1111/1365-2435.14010.

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@article{osti_1871355,

  title        = {Drought impacts on microbial trait distribution and feedback to soil carbon cycling},

  author       = {Malik, Ashish A. and Bouskill, Nicholas J.},

  abstractNote = {Abstract Quantifying the impact of drought on microbial processes and its consequences for soil carbon cycling is hindered by the lack of underlying mechanistic understanding. Therefore, there is a need to scale up the physiological response to changing water status from individual soil microbes to collective communities across different ecosystems. Here we propose the use of a framework that incorporates trait‐based ecology to link drought‐impacted microbial processes to rates of soil carbon decomposition and stabilisation. We briefly synthesise existing knowledge on the effects of drought on microbial physiology at the individual to community scale, before integrating this understanding within a framework incorporating life‐history strategy, ecological strategy and biochemistry. This framework highlights a dynamic allocation to high yield (Y), resource acquisition (A) and stress tolerance (S) pathways as environmental conditions change. Y‐A‐S strategies represent sets of traits that tend to correlate due to physiological or evolutionary trade‐offs. This framework enables assessment of microbial processes along two key environmental gradients of water and resource availability, both of which are constrained by drought. The variable chemistry of biomass and necromass produced under different physiological strategies in response to drying–rewetting impacts organic matter decomposition and stabilisation in soils, and should also be considered when quantifying soil carbon balance. We highlight that diversion of resources away from microbial growth can alter soil organic matter chemistry and its persistence depending on the kind of microbial compounds produced. To advance such a framework, we highlight avenues of research that would enable the further identification and quantification of traits linked to Y‐A‐S strategies and the physiological outcomes at the community level under drought and rewetting, and conclude by hypothesising how ecosystem‐level changes might feedback on to the soil carbon cycle. A scalable understanding of microbial drought‐response mechanisms affecting soil carbon cycling will transform the way microbial physiology is represented in ecosystem studies. Read the free Plain Language Summary for this article on the Journal blog.},

  doi          = {10.1111/1365-2435.14010},

  journal      = {Functional Ecology},

  number       = 6,

  volume       = 36,

  place        = {United Kingdom},

  year         = {Sun Feb 06 00:00:00 EST 2022},

  month        = {Sun Feb 06 00:00:00 EST 2022}

}

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Genome-resolved metagenomics reveals role of iron metabolism in drought-induced rhizosphere microbiome dynamics
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Leizeaga, Ainara; Hicks, Lettice C.; Manoharan, Lokeshwaran
Journal of Ecology, Vol. 109, Issue 9
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Ecology Letters, Vol. 22, Issue 5
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Similar Records

Title: Drought impacts on microbial trait distribution and feedback to soil carbon cycling

Abstract

Citation Formats

Drought and plant litter chemistry alter microbial gene expression and metabolite production journal, May 2020

Response of Escherichia coli growth rate to osmotic shock journal, May 2014

Enzyme activities along a climatic transect in the Judean Desert journal, November 2003

Metaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations journal, August 2019

Xerotolerant bacteria: surviving through a dry spell journal, March 2017

A theoretical analysis of microbial eco-physiological and diffusion limitations to carbon cycling in drying soils journal, June 2014

Molecular insights into the initiation of sporulation in Gram-positive bacteria: new technologies for an old phenomenon journal, April 2005

Increasing impacts of extreme droughts on vegetation productivity under climate change journal, November 2019

Response of osmolytes in soil to drying and rewetting journal, March 2014

Drying and rewetting effects on organic matter mineralisation of contrasting soils after 36 years of storage journal, May 2019

Decoupling the direct and indirect effects of climate on plant litter decomposition: Accounting for stress-induced modifications in plant chemistry journal, January 2018

Life in Dry Soils: Effects of Drought on Soil Microbial Communities and Processes journal, November 2018

Drought decreases soil enzyme activity in a Mediterranean Quercus ilex L. forest journal, March 2005

Microbiomes in light of traits: A phylogenetic perspective journal, November 2015

Glucosylglycerol, a Compatible Solute, Sustains Cell Division under Salt Stress journal, April 2003

Bacterial Mechanosensors journal, February 2018

Global patterns of drought recovery journal, August 2017

Microbial extracellular polysaccharide production and aggregate stability controlled by switchgrass (Panicum virgatum) root biomass and soil water potential journal, April 2020

Roles of Cytoplasmic Osmolytes, Water, and Crowding in the Response of Escherichia coli to Osmotic Stress: Biophysical Basis of Osmoprotection by Glycine Betaine † journal, November 2003

Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups journal, June 2012

Estimating maximal microbial growth rates from cultures, metagenomes, and single cells via codon usage patterns journal, March 2021

Microbial abundance and composition influence litter decomposition response to environmental change journal, March 2013

Trait-Based Representation of Biological Nitrification: Model Development, Testing, and Predicted Community Composition journal, January 2012

Responses of Microorganisms to Osmotic Stress journal, September 2019

Static osmolyte concentrations in microbial biomass during seasonal drought in a California grassland journal, February 2013

Energy Coupling Efficiency in the Type I ABC Transporter GlnPQ journal, March 2018

Belowground Response to Drought in a Tropical Forest Soil. II. Change in Microbial Function Impacts Carbon Composition journal, March 2016

Prolonged drought changes the bacterial growth response to rewetting journal, September 2015

Osmosensing and osmoregulatory compatible solute accumulation by bacteria journal, October 2001

Microbial community response to varying magnitudes of desiccation in soil: A test of the osmolyte accumulation hypothesis journal, February 2013

Social dynamics within decomposer communities lead to nitrogen retention and organic matter build-up in soils journal, December 2015

Effects of salinity on microbial tolerance to drying and rewetting journal, November 2011

Spatial constraints within the chlamydial host cell inclusion predict interrupted development and persistence journal, January 2008

Stress-induced growth rate reduction restricts metabolic resource utilization to modulate osmo-adaptation time journal, March 2021

Increasing drought under global warming in observations and models journal, August 2012

Severe drought conditions modify the microbial community structure, size and activity in amended and unamended soils journal, July 2012

Responses of soil carbon decomposition to drying-rewetting cycles: A meta-analysis journal, March 2020

Mechanisms of bacterial persistence during stress and antibiotic exposure journal, December 2016

Pathways of mineral‐associated soil organic matter formation: Integrating the role of plant carbon source, chemistry, and point of entry journal, November 2018

Developing a molecular picture of soil organic matter–mineral interactions by quantifying organo–mineral binding journal, August 2017

Environmental filtering of bacterial functional diversity along an aridity gradient journal, January 2019

Molecular Mechanisms of Two-Component Signal Transduction journal, September 2016

Effects of drying–rewetting frequency on soil carbon and nitrogen transformations journal, June 2002

Are we really studying persister cells? journal, June 2020

Growth and death of bacteria and fungi underlie rainfall-induced carbon dioxide pulses from seasonally dried soil journal, May 2014

Ecological memory of recurrent drought modifies soil processes via changes in soil microbial community journal, September 2021

On the origin of carbon dioxide released from rewetted soils journal, October 2016

Soil respiration and microbial biomass in multiple drying and rewetting cycles – Effect of glucose addition journal, November 2017

Microbial growth responses upon rewetting soil dried for four days or one year journal, November 2013

Understanding how microbiomes influence the systems they inhabit journal, August 2018

Weaker soil carbon–climate feedbacks resulting from microbial and abiotic interactions journal, November 2014

Model exploration of interactions between algal functional diversity and productivity in chemostats to represent open ponds systems across climate gradients journal, August 2019

Harnessing rhizosphere microbiomes for drought-resilient crop production journal, April 2020

Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change journal, September 2019

Predicting the optimal growth temperatures of prokaryotes using only genome derived features journal, January 2019

The effect of soil drying on humus decomposition and nitrogen availability journal, September 1958

A dormancy state in nonspore-forming bacteria journal, January 2009

Microbial enzymatic responses to drought and to nitrogen addition in a southern California grassland journal, September 2013

The effects of osmotic upshock on the intracellular solute pools of Bacillus subtilis journal, December 1990

Next-generation experiments linking community structure and ecosystem functioning: Crystal ball journal, November 2018

Cell-to-cell bacterial interactions promoted by drier conditions on soil surfaces journal, September 2018

Altered precipitation regime affects the function and composition of soil microbial communities on multiple time scales journal, October 2013

Next generation modeling of microbial souring – Parameterization through genomic information journal, January 2018

Soil bacterial networks are less stable under drought than fungal networks journal, August 2018

Wake up! Peptidoglycan lysis and bacterial non-growth states journal, June 2006

Microbial community changes in heathland soil communities along a geographical gradient: interaction with climate change manipulations journal, October 2005

Consequences of drought tolerance traits for microbial decomposition in the DEMENT model journal, April 2017

Recent European drought extremes beyond Common Era background variability journal, March 2021

Responses of extracellular enzymes to simple and complex nutrient inputs journal, May 2005

A trait-based approach for modelling microbial litter decomposition journal, May 2012

Rapid evolution destabilizes species interactions in a fluctuating environment journal, October 2020

A trait-based framework for predicting when and where microbial adaptation to climate change will affect ecosystem functioning journal, September 2011

Growth, compatible solute and salt accumulation of five mycorrhizal fungal species grown over a range of NaCl concentrations journal, October 2005

Mechanosensitive channels in bacteria: signs of closure? journal, June 2007

Physical constraints affecting bacterial habitats and activity in unsaturated porous media – a review journal, June 2007

Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls journal, November 2016

Persistence of soil organic matter as an ecosystem property journal, October 2011

Drought and plant litter chemistry alter microbial gene expression and metabolite production
journal, May 2020

Response of Escherichia coli growth rate to osmotic shock
journal, May 2014

Enzyme activities along a climatic transect in the Judean Desert
journal, November 2003

Metaphenomic Responses of a Native Prairie Soil Microbiome to Moisture Perturbations
journal, August 2019

Xerotolerant bacteria: surviving through a dry spell
journal, March 2017

A theoretical analysis of microbial eco-physiological and diffusion limitations to carbon cycling in drying soils
journal, June 2014

Molecular insights into the initiation of sporulation in Gram-positive bacteria: new technologies for an old phenomenon
journal, April 2005

Increasing impacts of extreme droughts on vegetation productivity under climate change
journal, November 2019

Response of osmolytes in soil to drying and rewetting
journal, March 2014

Drying and rewetting effects on organic matter mineralisation of contrasting soils after 36 years of storage
journal, May 2019

Decoupling the direct and indirect effects of climate on plant litter decomposition: Accounting for stress-induced modifications in plant chemistry
journal, January 2018

Life in Dry Soils: Effects of Drought on Soil Microbial Communities and Processes
journal, November 2018

Drought decreases soil enzyme activity in a Mediterranean Quercus ilex L. forest
journal, March 2005

Microbiomes in light of traits: A phylogenetic perspective
journal, November 2015

Glucosylglycerol, a Compatible Solute, Sustains Cell Division under Salt Stress
journal, April 2003

Bacterial Mechanosensors
journal, February 2018

Global patterns of drought recovery
journal, August 2017

Microbial extracellular polysaccharide production and aggregate stability controlled by switchgrass (Panicum virgatum) root biomass and soil water potential
journal, April 2020

Roles of Cytoplasmic Osmolytes, Water, and Crowding in the Response of Escherichia coli to Osmotic Stress: Biophysical Basis of Osmoprotection by Glycine Betaine ^†
journal, November 2003

Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups
journal, June 2012

Estimating maximal microbial growth rates from cultures, metagenomes, and single cells via codon usage patterns
journal, March 2021

Microbial abundance and composition influence litter decomposition response to environmental change
journal, March 2013

Trait-Based Representation of Biological Nitrification: Model Development, Testing, and Predicted Community Composition
journal, January 2012

Responses of Microorganisms to Osmotic Stress
journal, September 2019

Static osmolyte concentrations in microbial biomass during seasonal drought in a California grassland
journal, February 2013

Energy Coupling Efficiency in the Type I ABC Transporter GlnPQ
journal, March 2018

Belowground Response to Drought in a Tropical Forest Soil. II. Change in Microbial Function Impacts Carbon Composition
journal, March 2016

Prolonged drought changes the bacterial growth response to rewetting
journal, September 2015

Osmosensing and osmoregulatory compatible solute accumulation by bacteria
journal, October 2001

Microbial community response to varying magnitudes of desiccation in soil: A test of the osmolyte accumulation hypothesis
journal, February 2013

Social dynamics within decomposer communities lead to nitrogen retention and organic matter build-up in soils
journal, December 2015

Effects of salinity on microbial tolerance to drying and rewetting
journal, November 2011

Spatial constraints within the chlamydial host cell inclusion predict interrupted development and persistence
journal, January 2008

Stress-induced growth rate reduction restricts metabolic resource utilization to modulate osmo-adaptation time
journal, March 2021

Increasing drought under global warming in observations and models
journal, August 2012

Severe drought conditions modify the microbial community structure, size and activity in amended and unamended soils
journal, July 2012

Responses of soil carbon decomposition to drying-rewetting cycles: A meta-analysis
journal, March 2020

Mechanisms of bacterial persistence during stress and antibiotic exposure
journal, December 2016

Pathways of mineral‐associated soil organic matter formation: Integrating the role of plant carbon source, chemistry, and point of entry
journal, November 2018

Developing a molecular picture of soil organic matter–mineral interactions by quantifying organo–mineral binding
journal, August 2017

Environmental filtering of bacterial functional diversity along an aridity gradient
journal, January 2019

Molecular Mechanisms of Two-Component Signal Transduction
journal, September 2016

Effects of drying–rewetting frequency on soil carbon and nitrogen transformations
journal, June 2002

Are we really studying persister cells?
journal, June 2020

Growth and death of bacteria and fungi underlie rainfall-induced carbon dioxide pulses from seasonally dried soil
journal, May 2014

Ecological memory of recurrent drought modifies soil processes via changes in soil microbial community
journal, September 2021

On the origin of carbon dioxide released from rewetted soils
journal, October 2016

Soil respiration and microbial biomass in multiple drying and rewetting cycles – Effect of glucose addition
journal, November 2017

Microbial growth responses upon rewetting soil dried for four days or one year
journal, November 2013

Understanding how microbiomes influence the systems they inhabit
journal, August 2018

Weaker soil carbon–climate feedbacks resulting from microbial and abiotic interactions
journal, November 2014

Model exploration of interactions between algal functional diversity and productivity in chemostats to represent open ponds systems across climate gradients
journal, August 2019

Harnessing rhizosphere microbiomes for drought-resilient crop production
journal, April 2020

Defining trait-based microbial strategies with consequences for soil carbon cycling under climate change
journal, September 2019

Predicting the optimal growth temperatures of prokaryotes using only genome derived features
journal, January 2019

The effect of soil drying on humus decomposition and nitrogen availability
journal, September 1958

A dormancy state in nonspore-forming bacteria
journal, January 2009

Microbial enzymatic responses to drought and to nitrogen addition in a southern California grassland
journal, September 2013

The effects of osmotic upshock on the intracellular solute pools of Bacillus subtilis
journal, December 1990

Next-generation experiments linking community structure and ecosystem functioning: Crystal ball
journal, November 2018

Cell-to-cell bacterial interactions promoted by drier conditions on soil surfaces
journal, September 2018

Altered precipitation regime affects the function and composition of soil microbial communities on multiple time scales
journal, October 2013

Next generation modeling of microbial souring – Parameterization through genomic information
journal, January 2018

Soil bacterial networks are less stable under drought than fungal networks
journal, August 2018

Wake up! Peptidoglycan lysis and bacterial non-growth states
journal, June 2006

Microbial community changes in heathland soil communities along a geographical gradient: interaction with climate change manipulations
journal, October 2005

Consequences of drought tolerance traits for microbial decomposition in the DEMENT model
journal, April 2017

Recent European drought extremes beyond Common Era background variability
journal, March 2021

Responses of extracellular enzymes to simple and complex nutrient inputs
journal, May 2005

A trait-based approach for modelling microbial litter decomposition
journal, May 2012

Rapid evolution destabilizes species interactions in a fluctuating environment
journal, October 2020

A trait-based framework for predicting when and where microbial adaptation to climate change will affect ecosystem functioning
journal, September 2011

Growth, compatible solute and salt accumulation of five mycorrhizal fungal species grown over a range of NaCl concentrations
journal, October 2005

Mechanosensitive channels in bacteria: signs of closure?
journal, June 2007

Physical constraints affecting bacterial habitats and activity in unsaturated porous media – a review
journal, June 2007

Direct evidence for microbial-derived soil organic matter formation and its ecophysiological controls
journal, November 2016

Persistence of soil organic matter as an ecosystem property
journal, October 2011

Belowground Response to Drought in a Tropical Forest Soil. I. Changes in Microbial Functional Potential and Metabolism
journal, April 2016

The legacy of mixed planting and precipitation reduction treatments on soil microbial activity, biomass and community composition in a young tree plantation
journal, September 2018

Regulation of microbial growth by turgor pressure
journal, April 2018