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

Bouskill NJ, Wood TE, Baran R, Ye Z, Bowen BP, Lim H, Zhou J, Nostrand JD, Nico P, Northen TR, Silver WL, Brodie EL - Front Microbiol (2016)

Bottom Line: This approach reduced soil moisture by 13% and water potential by 0.14 MPa (from -0.2 to -0.34).Previous results from this experiment have demonstrated that the diversity and composition of these soil microbial communities are sensitive to even small changes in soil water.Subsequently, a microbial population emerges with a greater capacity for extracellular enzyme production targeting macromolecular carbon.

View Article: PubMed Central - PubMed

Affiliation: Earth Sciences Division, Ecology Department, Lawrence Berkeley National Laboratory Berkeley, CA, USA.

ABSTRACT
Global climate models predict a future of increased severity of drought in many tropical forests. Soil microbes are central to the balance of these systems as sources or sinks of atmospheric carbon (C), yet how they respond metabolically to drought is not well-understood. We simulated drought in the typically aseasonal Luquillo Experimental Forest, Puerto Rico, by intercepting precipitation falling through the forest canopy. This approach reduced soil moisture by 13% and water potential by 0.14 MPa (from -0.2 to -0.34). Previous results from this experiment have demonstrated that the diversity and composition of these soil microbial communities are sensitive to even small changes in soil water. Here, we show prolonged drought significantly alters the functional potential of the community and provokes a clear osmotic stress response, including the production of compatible solutes that increase intracellular C demand. Subsequently, a microbial population emerges with a greater capacity for extracellular enzyme production targeting macromolecular carbon. Significantly, some of these drought-induced functional shifts in the soil microbiota are attenuated by prior exposure to a short-term drought suggesting that acclimation may occur despite a lack of longer-term drought history.

No MeSH data available.


Related in: MedlinePlus

Canonical correspondence analysis (CCA) of the functional potential of the soils as indicated by genomic analysis following 10 months of throughfall exclusion. Data shown are restricted to four functional gene categories (carbon degradation, nitrogen and phosphorus cycling, and stress pathways), and the major functional groups within each these categories are ordinated onto the plot and grouped by color (as denoted by the inset in the upper right corner). The soils are also color-coordinated as either control (red), pre-excluded (green), and de novo soils (blue). The functional potential of the control and treatment soils are correlated against the collected physicochemical factors and the relationship projected onto the ordination. The directionality and length of the vectors is proportional to the direction and length of the chemical gradient sampled from the soil water. Vector identity is indicated by the abbreviated label at the tip of the arrow (NH4, ammonia; NO3, nitrate; K, potassium; Na, sodium; Mg, magnesium; WP, water potential; WC, water content; Fe, iron; P, phosphate; DOC, dissolved organic carbon; Ca, calcium).
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Figure 2: Canonical correspondence analysis (CCA) of the functional potential of the soils as indicated by genomic analysis following 10 months of throughfall exclusion. Data shown are restricted to four functional gene categories (carbon degradation, nitrogen and phosphorus cycling, and stress pathways), and the major functional groups within each these categories are ordinated onto the plot and grouped by color (as denoted by the inset in the upper right corner). The soils are also color-coordinated as either control (red), pre-excluded (green), and de novo soils (blue). The functional potential of the control and treatment soils are correlated against the collected physicochemical factors and the relationship projected onto the ordination. The directionality and length of the vectors is proportional to the direction and length of the chemical gradient sampled from the soil water. Vector identity is indicated by the abbreviated label at the tip of the arrow (NH4, ammonia; NO3, nitrate; K, potassium; Na, sodium; Mg, magnesium; WP, water potential; WC, water content; Fe, iron; P, phosphate; DOC, dissolved organic carbon; Ca, calcium).

Mentions: We subsequently focused our analyses on the response of a relevant subset of genes related to carbon degradation/transformation, nitrogen and phosphorus cycling, and physiological stress that explained 42% of the overall variance in functional potential. Prolonged drought (10 months) clearly shaped the functional potential (Figure 2), with the pre-excluded and de novo treatment soils becoming more similar to each other relative to the control soils for each gene category (Supplementary Figures S1B–E). CCA showed the separation of control and experimental soils could be explained by the differential distribution of specific gene categories (Figure 2 and Supplementary Figure S2). This included a higher relative abundance of genes involved in complex C-degradation (chitin, cellulose, and lignin), nutrient limitation and osmotic stress response in the de novo excluded soils relative to the controls. Genes involved in C-degradation correlated negatively with soil water content, but positively with nitrogen species. Genes related to P limitation were enriched in the de novo soils, and negatively correlated to soil water P concentration. Control soils had a higher relative abundance of genes related to O2 limitation and anaerobic processes [e.g., denitrification, dissimilatory nitrate (NO3) reduction; Figure 2 and Supplementary Figure S2]. The prevalence of these genes is likely related to the higher reduction potential of these soils, inferred from higher soluble Fe concentrations relative to the soils undergoing drought (Liptzin and Silver, 2009; Dubinsky et al., 2010; Bouskill et al., 2013). At a categorical level, genes related to hemicellulose decomposition ordinated alongside the control samples (Figure 2) implying a higher relative abundance compared to drought treatments. However, at finer resolution (i.e., individual genes coding for hydrolysis of specific hemi-cellulose polysaccharides) genes related to arabinan breakdown were higher within the control soils, while those related to xylan hydrolysis were enriched in drought soils (Supplementary Figure S3).


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

Bouskill NJ, Wood TE, Baran R, Ye Z, Bowen BP, Lim H, Zhou J, Nostrand JD, Nico P, Northen TR, Silver WL, Brodie EL - Front Microbiol (2016)

Canonical correspondence analysis (CCA) of the functional potential of the soils as indicated by genomic analysis following 10 months of throughfall exclusion. Data shown are restricted to four functional gene categories (carbon degradation, nitrogen and phosphorus cycling, and stress pathways), and the major functional groups within each these categories are ordinated onto the plot and grouped by color (as denoted by the inset in the upper right corner). The soils are also color-coordinated as either control (red), pre-excluded (green), and de novo soils (blue). The functional potential of the control and treatment soils are correlated against the collected physicochemical factors and the relationship projected onto the ordination. The directionality and length of the vectors is proportional to the direction and length of the chemical gradient sampled from the soil water. Vector identity is indicated by the abbreviated label at the tip of the arrow (NH4, ammonia; NO3, nitrate; K, potassium; Na, sodium; Mg, magnesium; WP, water potential; WC, water content; Fe, iron; P, phosphate; DOC, dissolved organic carbon; Ca, calcium).
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Related In: Results  -  Collection

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Figure 2: Canonical correspondence analysis (CCA) of the functional potential of the soils as indicated by genomic analysis following 10 months of throughfall exclusion. Data shown are restricted to four functional gene categories (carbon degradation, nitrogen and phosphorus cycling, and stress pathways), and the major functional groups within each these categories are ordinated onto the plot and grouped by color (as denoted by the inset in the upper right corner). The soils are also color-coordinated as either control (red), pre-excluded (green), and de novo soils (blue). The functional potential of the control and treatment soils are correlated against the collected physicochemical factors and the relationship projected onto the ordination. The directionality and length of the vectors is proportional to the direction and length of the chemical gradient sampled from the soil water. Vector identity is indicated by the abbreviated label at the tip of the arrow (NH4, ammonia; NO3, nitrate; K, potassium; Na, sodium; Mg, magnesium; WP, water potential; WC, water content; Fe, iron; P, phosphate; DOC, dissolved organic carbon; Ca, calcium).
Mentions: We subsequently focused our analyses on the response of a relevant subset of genes related to carbon degradation/transformation, nitrogen and phosphorus cycling, and physiological stress that explained 42% of the overall variance in functional potential. Prolonged drought (10 months) clearly shaped the functional potential (Figure 2), with the pre-excluded and de novo treatment soils becoming more similar to each other relative to the control soils for each gene category (Supplementary Figures S1B–E). CCA showed the separation of control and experimental soils could be explained by the differential distribution of specific gene categories (Figure 2 and Supplementary Figure S2). This included a higher relative abundance of genes involved in complex C-degradation (chitin, cellulose, and lignin), nutrient limitation and osmotic stress response in the de novo excluded soils relative to the controls. Genes involved in C-degradation correlated negatively with soil water content, but positively with nitrogen species. Genes related to P limitation were enriched in the de novo soils, and negatively correlated to soil water P concentration. Control soils had a higher relative abundance of genes related to O2 limitation and anaerobic processes [e.g., denitrification, dissimilatory nitrate (NO3) reduction; Figure 2 and Supplementary Figure S2]. The prevalence of these genes is likely related to the higher reduction potential of these soils, inferred from higher soluble Fe concentrations relative to the soils undergoing drought (Liptzin and Silver, 2009; Dubinsky et al., 2010; Bouskill et al., 2013). At a categorical level, genes related to hemicellulose decomposition ordinated alongside the control samples (Figure 2) implying a higher relative abundance compared to drought treatments. However, at finer resolution (i.e., individual genes coding for hydrolysis of specific hemi-cellulose polysaccharides) genes related to arabinan breakdown were higher within the control soils, while those related to xylan hydrolysis were enriched in drought soils (Supplementary Figure S3).

Bottom Line: This approach reduced soil moisture by 13% and water potential by 0.14 MPa (from -0.2 to -0.34).Previous results from this experiment have demonstrated that the diversity and composition of these soil microbial communities are sensitive to even small changes in soil water.Subsequently, a microbial population emerges with a greater capacity for extracellular enzyme production targeting macromolecular carbon.

View Article: PubMed Central - PubMed

Affiliation: Earth Sciences Division, Ecology Department, Lawrence Berkeley National Laboratory Berkeley, CA, USA.

ABSTRACT
Global climate models predict a future of increased severity of drought in many tropical forests. Soil microbes are central to the balance of these systems as sources or sinks of atmospheric carbon (C), yet how they respond metabolically to drought is not well-understood. We simulated drought in the typically aseasonal Luquillo Experimental Forest, Puerto Rico, by intercepting precipitation falling through the forest canopy. This approach reduced soil moisture by 13% and water potential by 0.14 MPa (from -0.2 to -0.34). Previous results from this experiment have demonstrated that the diversity and composition of these soil microbial communities are sensitive to even small changes in soil water. Here, we show prolonged drought significantly alters the functional potential of the community and provokes a clear osmotic stress response, including the production of compatible solutes that increase intracellular C demand. Subsequently, a microbial population emerges with a greater capacity for extracellular enzyme production targeting macromolecular carbon. Significantly, some of these drought-induced functional shifts in the soil microbiota are attenuated by prior exposure to a short-term drought suggesting that acclimation may occur despite a lack of longer-term drought history.

No MeSH data available.


Related in: MedlinePlus