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Title: The Transcriptional Response of Soil Bacteria to Long-Term Warming and Short-Term Seasonal Fluctuations in a Terrestrial Forest

Journal Article · · Frontiers in Microbiology
 [1];  [2];  [2];  [3];  [2];  [2];  [4];  [2]
  1. Keene State College, NH (United States); OSTI
  2. Univ. of Massachusetts, Amherst, MA (United States)
  3. Univ. of South Carolina, Columbia, SC (United States)
  4. Marine Biological Laboratory, Woods Hole, MA (United States)

Terrestrial ecosystems are an important carbon store, and this carbon is vulnerable to microbial degradation with climate warming. After 30 years of experimental warming, carbon stocks in a temperate mixed deciduous forest were observed to be reduced by 30% in the heated plots relative to the controls. In addition, soil respiration was seasonal, as was the warming treatment effect. We therefore hypothesized that long-term warming will have higher expressions of genes related to carbohydrate and lipid metabolism due to increased utilization of recalcitrant carbon pools compared to controls. Because of the seasonal effect of soil respiration and the warming treatment, we further hypothesized that these patterns will be seasonal. We used RNA sequencing to show how the microbial community responds to long-term warming (~30 years) in Harvard Forest, MA. Total RNA was extracted from mineral and organic soil types from two treatment plots (+5°C heated and ambient control), at two time points (June and October) and sequenced using Illumina NextSeq technology. Treatment had a larger effect size on KEGG annotated transcripts than on CAZymes, while soil types more strongly affected CAZymes than KEGG annotated transcripts, though effect sizes overall were small. Although, warming showed a small effect on overall CAZymes expression, several carbohydrate-associated enzymes showed increased expression in heated soils (~68% of all differentially expressed transcripts). Further, exploratory analysis using an unconstrained method showed increased abundances of enzymes related to polysaccharide and lipid metabolism and decomposition in heated soils. Compared to long-term warming, we detected a relatively small effect of seasonal variation on community gene expression. Together, these results indicate that the higher carbohydrate degrading potential of bacteria in heated plots can possibly accelerate a self-reinforcing carbon cycle-temperature feedback in a warming climate.

Research Organization:
Marine Biological Laboratory, Woods Hole, MA (United States)
Sponsoring Organization:
National Science Foundation (NSF); USDOE Office of Science (SC)
Grant/Contract Number:
SC0010740
OSTI ID:
1904475
Journal Information:
Frontiers in Microbiology, Journal Name: Frontiers in Microbiology Vol. 12; ISSN 1664-302X
Publisher:
Frontiers Research FoundationCopyright Statement
Country of Publication:
United States
Language:
English

References (76)

Data from: Cross-biome patterns in soil microbial respiration predictable from evolutionary theory on thermal adaptation dataset January 2019
Data from "Soil microbial respiration adapts to ambient temperature in global drylands" dataset January 2019
A meta-analysis of responses of soil biota to global change journal January 2011
A meta-analysis of the response of soil respiration, net nitrogen mineralization, and aboveground plant growth to experimental ecosystem warming journal February 2001
Soil warming and nitrogen deposition alter soil organic matter composition at the molecular-level journal February 2015
Use of Internal Standards for Quantitative Metatranscriptome and Metagenome Analysis book January 2013
EMBOSS: The European Molecular Biology Open Software Suite journal June 2000
Proteomic analysis of the adaptation to warming in the Antarctic bacteria Shewanella frigidimarina journal December 2014
Changes of soil properties regulate the soil organic carbon loss with grassland degradation on the Qinghai-Tibet Plateau journal October 2018
Climate change feedbacks to microbial decomposition in boreal soils journal December 2011
Bacterial enzymes involved in lignin degradation journal October 2016
Changes in the seasonal snow cover of alpine regions and its effect on soil processes: A review journal March 2007
Seasonal changes in the soil microbial community in a grassland plant diversity gradient four years after establishment journal October 2008
Microbial biomass, functional capacity, and community structure after 12 years of soil warming journal November 2008
Soil microbial community changes and their linkages with ecosystem carbon exchange under asymmetrically diurnal warming journal June 2011
Seasonal variation in functional properties of microbial communities in beech forest soil journal May 2013
Decomposition of particulate organic matter is more sensitive to temperature than the mineral associated organic matter journal March 2014
Soil microbes and their response to experimental warming over time: A meta-analysis of field studies journal April 2017
Changes in substrate availability drive carbon cycle response to chronic warming journal July 2017
iPath: interactive exploration of biochemical pathways and networks journal March 2008
Decreased Soil Organic Matter in a Long‐Term Soil Warming Experiment Lowers Soil Water Holding Capacity and Affects Soil Thermal and Hydrological Buffering journal April 2020
Acclimatization of soil respiration to warming in a tall grass prairie journal October 2001
Quantitative analysis of a deeply sequenced marine microbial metatranscriptome journal September 2010
Effect of warming and drought on grassland microbial communities journal March 2011
Active and total microbial communities in forest soil are largely different and highly stratified during decomposition journal July 2011
Responses of soil bacterial and fungal communities to extreme desiccation and rewetting journal July 2013
Forest harvesting reduces the soil metagenomic potential for biomass decomposition journal April 2015
Microbial mediation of carbon-cycle feedbacks to climate warming journal December 2011
Increased cuticular carbon sequestration and lignin oxidation in response to soil warming journal November 2008
Fast and sensitive protein alignment using DIAMOND journal November 2014
Soil microbial respiration adapts to ambient temperature in global drylands journal January 2019
Cross-biome patterns in soil microbial respiration predictable from evolutionary theory on thermal adaptation journal January 2019
Monitoring global messenger RNA changes in externally controlled microarray experiments journal April 2003
Soil warming, carbon-nitrogen interactions, and forest carbon budgets journal May 2011
Different tradeoffs result from alternate genetic adaptations to a common environment journal August 2014
Forest age improves understanding of the global carbon sink journal February 2019
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data journal November 2009
FLASH: fast length adjustment of short reads to improve genome assemblies journal September 2011
SortMeRNA: fast and accurate filtering of ribosomal RNAs in metatranscriptomic data journal October 2012
Trimmomatic: a flexible trimmer for Illumina sequence data journal April 2014
MATAM: reconstruction of phylogenetic marker genes from short sequencing reads in metagenomes journal October 2017
HMMER web server: interactive sequence similarity searching journal May 2011
dbCAN: a web resource for automated carbohydrate-active enzyme annotation journal May 2012
The carbohydrate-active enzymes database (CAZy) in 2013 journal November 2013
MEGAN analysis of metagenomic data journal February 2007
Does declining carbon-use efficiency explain thermal acclimation of soil respiration with warming? journal October 2012
Microbial physiology and soil CO 2 efflux after 9 years of soil warming in a temperate forest - no indications for thermal adaptations journal September 2015
Terrestrial ecosystems and the carbon cycle journal February 1995
Soil respiration under prolonged soil warming: are rate reductions caused by acclimation or substrate loss? journal November 2004
Temperature and soil organic matter decomposition rates - synthesis of current knowledge and a way forward journal August 2011
Thermal adaptation of soil microbial respiration to elevated temperature journal December 2008
No evidence for compensatory thermal adaptation of soil microbial respiration in the study of Bradford et al. (2008) journal July 2009
VEGAN, a package of R functions for community ecology journal April 2003
Soil Warming and Carbon-Cycle Feedbacks to the Climate System journal December 2002
A Large and Persistent Carbon Sink in the World's Forests journal July 2011
Long-term pattern and magnitude of soil carbon feedback to the climate system in a warming world journal October 2017
Naive Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy journal June 2007
Long-Term Warming Alters Carbohydrate Degradation Potential in Temperate Forest Soils journal September 2016
Soil Microbial Community Responses to Multiple Experimental Climate Change Drivers journal December 2009
Forest Soil Bacteria: Diversity, Involvement in Ecosystem Processes, and Response to Global Change journal April 2017
Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria journal January 2020
Climate–Carbon Cycle Feedback Analysis: Results from the C 4 MIP Model Intercomparison journal July 2006
WGCNA: an R package for weighted correlation network analysis journal December 2008
Feed in summer, rest in winter: microbial carbon utilization in forest topsoil journal September 2017
Functional Assays and Metagenomic Analyses Reveals Differences between the Microbial Communities Inhabiting the Soil Horizons of a Norway Spruce Plantation journal February 2013
Seasonal dynamics of soil respiration and N mineralization in chronically warmed and fertilized soils journal March 2011
Multiple Climate Change Factors Interact to Alter Soil Microbial Community Structure in an Old-Field Ecosystem journal January 2011
Responses of Trace Gas Fluxes and N Availability to Experimentally Elevated Soil Temperatures journal August 1994
Fundamentals of Microbial Community Resistance and Resilience journal January 2012
Long-term forest soil warming alters microbial communities in temperate forest soils journal February 2015
Two decades of warming increases diversity of a potentially lignolytic bacterial community journal May 2015
Warming Alters Expressions of Microbial Functional Genes Important to Ecosystem Functioning journal May 2016
Soil Metatranscriptomes Under Long-Term Experimental Warming and Drying: Fungi Allocate Resources to Cell Metabolic Maintenance Rather Than Decay journal August 2019
Isolation and Identification of a Bacterial Strain Producing Thermostable α- Amylase journal January 2011
Global soil carbon: understanding and managing the largest terrestrial carbon pool journal February 2014
Seasonal changes in and relationship between soil microbial and microfaunal communities in a Tamarix chinensis community in the Yellow River Delta journal December 2011