pH and exchangeable aluminum are major regulators of microbial energy flow and carbon use efficiency in soil microbial communities

Davey L. Jones, Emily C. Cooledge, Frances C. Hoyle, Robert I. Griffiths, Daniel V. Murphy

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Abstract

The microbial partitioning of organic carbon (C) into either anabolic (i.e. growth) or catabolic (i.e. respiration) metabolic pathways represents a key process regulating the amount of added C that is retained in soil. The factors regulating C use efficiency (CUE) in agricultural soils, however, remain poorly understood. The aim of this study was to investigate substrate CUE from a wide range of soils (n = 970) and geographical area (200,000 km2) to determine which soil properties most influenced C retention within the microbial community. Using a 14C-labeling approach, we showed that the average CUE across all soils was 0.65 ± 0.003, but that the variation in CUE was relatively high within the sample population (CV 14.9%). Of the major properties measured in our soils, we found that pH and exchangeable aluminum (Al) were highly correlated with CUE. We identified a critical pH transition point at which CUE declined (pH 5.5). This coincided exactly with the point at which Al3+ started to become soluble. In contrast, other soil factors [e.g. total C and nitrogen (N), dissolved organic C (DOC), clay content, available calcium, phosphorus (P) and sulfur (S), total base cations] showed little or no relationship with CUE. We also found no evidence to suggest that nutrient stoichiometry (C:N, C:P and C:S ratios) influenced CUE in these soils. Based on current evidence, we postulate that the decline in microbial CUE at low pH and high Al reflects a greater channeling of C into energy intensive metabolic pathways involved in overcoming H+/Al3+ stress (e.g. cell repair and detoxification). The response may also be associated with shifts in microbial community structure, which are known to be tightly associated with soil pH. We conclude that maintaining agricultural soils above pH 5.5 maximizes microbial energy efficiency.

Original languageEnglish
Article number107584
JournalSoil Biology and Biochemistry
Volume138
DOIs
Publication statusPublished - 1 Nov 2019

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exchangeable aluminum
energy flow
Aluminum
microbial communities
microbial community
Soil
Carbon
aluminum
carbon
soil
agricultural soils
biochemical pathways
agricultural soil
dissolved organic nitrogen
Metabolic Networks and Pathways
energy efficiency
stoichiometry
detoxification
soil pH
soil properties

Cite this

@article{4e3ffeafe3db4981bc29ade114a4d238,
title = "pH and exchangeable aluminum are major regulators of microbial energy flow and carbon use efficiency in soil microbial communities",
abstract = "The microbial partitioning of organic carbon (C) into either anabolic (i.e. growth) or catabolic (i.e. respiration) metabolic pathways represents a key process regulating the amount of added C that is retained in soil. The factors regulating C use efficiency (CUE) in agricultural soils, however, remain poorly understood. The aim of this study was to investigate substrate CUE from a wide range of soils (n = 970) and geographical area (200,000 km2) to determine which soil properties most influenced C retention within the microbial community. Using a 14C-labeling approach, we showed that the average CUE across all soils was 0.65 ± 0.003, but that the variation in CUE was relatively high within the sample population (CV 14.9{\%}). Of the major properties measured in our soils, we found that pH and exchangeable aluminum (Al) were highly correlated with CUE. We identified a critical pH transition point at which CUE declined (pH 5.5). This coincided exactly with the point at which Al3+ started to become soluble. In contrast, other soil factors [e.g. total C and nitrogen (N), dissolved organic C (DOC), clay content, available calcium, phosphorus (P) and sulfur (S), total base cations] showed little or no relationship with CUE. We also found no evidence to suggest that nutrient stoichiometry (C:N, C:P and C:S ratios) influenced CUE in these soils. Based on current evidence, we postulate that the decline in microbial CUE at low pH and high Al reflects a greater channeling of C into energy intensive metabolic pathways involved in overcoming H+/Al3+ stress (e.g. cell repair and detoxification). The response may also be associated with shifts in microbial community structure, which are known to be tightly associated with soil pH. We conclude that maintaining agricultural soils above pH 5.5 maximizes microbial energy efficiency.",
keywords = "Agroecosystem, Carbon sequestration, SOM dynamics, Texture, Tipping point",
author = "Jones, {Davey L.} and Cooledge, {Emily C.} and Hoyle, {Frances C.} and Griffiths, {Robert I.} and Murphy, {Daniel V.}",
year = "2019",
month = "11",
day = "1",
doi = "10.1016/j.soilbio.2019.107584",
language = "English",
volume = "138",
journal = "Soil Biology & Biochemistry",
issn = "0038-0717",
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TY - JOUR

T1 - pH and exchangeable aluminum are major regulators of microbial energy flow and carbon use efficiency in soil microbial communities

AU - Jones, Davey L.

AU - Cooledge, Emily C.

AU - Hoyle, Frances C.

AU - Griffiths, Robert I.

AU - Murphy, Daniel V.

PY - 2019/11/1

Y1 - 2019/11/1

N2 - The microbial partitioning of organic carbon (C) into either anabolic (i.e. growth) or catabolic (i.e. respiration) metabolic pathways represents a key process regulating the amount of added C that is retained in soil. The factors regulating C use efficiency (CUE) in agricultural soils, however, remain poorly understood. The aim of this study was to investigate substrate CUE from a wide range of soils (n = 970) and geographical area (200,000 km2) to determine which soil properties most influenced C retention within the microbial community. Using a 14C-labeling approach, we showed that the average CUE across all soils was 0.65 ± 0.003, but that the variation in CUE was relatively high within the sample population (CV 14.9%). Of the major properties measured in our soils, we found that pH and exchangeable aluminum (Al) were highly correlated with CUE. We identified a critical pH transition point at which CUE declined (pH 5.5). This coincided exactly with the point at which Al3+ started to become soluble. In contrast, other soil factors [e.g. total C and nitrogen (N), dissolved organic C (DOC), clay content, available calcium, phosphorus (P) and sulfur (S), total base cations] showed little or no relationship with CUE. We also found no evidence to suggest that nutrient stoichiometry (C:N, C:P and C:S ratios) influenced CUE in these soils. Based on current evidence, we postulate that the decline in microbial CUE at low pH and high Al reflects a greater channeling of C into energy intensive metabolic pathways involved in overcoming H+/Al3+ stress (e.g. cell repair and detoxification). The response may also be associated with shifts in microbial community structure, which are known to be tightly associated with soil pH. We conclude that maintaining agricultural soils above pH 5.5 maximizes microbial energy efficiency.

AB - The microbial partitioning of organic carbon (C) into either anabolic (i.e. growth) or catabolic (i.e. respiration) metabolic pathways represents a key process regulating the amount of added C that is retained in soil. The factors regulating C use efficiency (CUE) in agricultural soils, however, remain poorly understood. The aim of this study was to investigate substrate CUE from a wide range of soils (n = 970) and geographical area (200,000 km2) to determine which soil properties most influenced C retention within the microbial community. Using a 14C-labeling approach, we showed that the average CUE across all soils was 0.65 ± 0.003, but that the variation in CUE was relatively high within the sample population (CV 14.9%). Of the major properties measured in our soils, we found that pH and exchangeable aluminum (Al) were highly correlated with CUE. We identified a critical pH transition point at which CUE declined (pH 5.5). This coincided exactly with the point at which Al3+ started to become soluble. In contrast, other soil factors [e.g. total C and nitrogen (N), dissolved organic C (DOC), clay content, available calcium, phosphorus (P) and sulfur (S), total base cations] showed little or no relationship with CUE. We also found no evidence to suggest that nutrient stoichiometry (C:N, C:P and C:S ratios) influenced CUE in these soils. Based on current evidence, we postulate that the decline in microbial CUE at low pH and high Al reflects a greater channeling of C into energy intensive metabolic pathways involved in overcoming H+/Al3+ stress (e.g. cell repair and detoxification). The response may also be associated with shifts in microbial community structure, which are known to be tightly associated with soil pH. We conclude that maintaining agricultural soils above pH 5.5 maximizes microbial energy efficiency.

KW - Agroecosystem

KW - Carbon sequestration

KW - SOM dynamics

KW - Texture

KW - Tipping point

UR - http://www.scopus.com/inward/record.url?scp=85072245138&partnerID=8YFLogxK

U2 - 10.1016/j.soilbio.2019.107584

DO - 10.1016/j.soilbio.2019.107584

M3 - Article

VL - 138

JO - Soil Biology & Biochemistry

JF - Soil Biology & Biochemistry

SN - 0038-0717

M1 - 107584

ER -