Energy use efficiency of soil microorganisms: Driven by carbon recycling and reduction

Chaoqun Wang; Yakov Kuzyakov

doi:10.1111/gcb.16925

journal article Open Access Aug 30, 2023

Energy use efficiency of soil microorganisms: Driven by carbon recycling and reduction

Chaoqun Wang

Yakov Kuzyakov

Global Change Biology Vol. 29 No. 22 pp. 6170-6187 · Wiley

View at Publisher Save 10.1111/gcb.16925

Abstract

AbstractCarbon use efficiency (CUE) is being intensively applied to quantify carbon (C) cycling processes from microbial cell to global scales. Energy use efficiency (EUE) is at least as important as the CUE because (i) microorganisms use organic C mainly as an energy source and not as elemental C per se, and (ii) microbial growth and maintenance are limited by energy, but not by C as a structural element. We conceptualize and review the importance of EUE by soil microorganisms and focus on (i) the energy content in organic compounds depending on the nominal oxidation state of carbon (NOSC), (ii) approaches to assess EUE, (iii) similarities and differences between CUE and EUE, and (iv) discuss mechanisms responsible for lower EUE compared to CUE. The energy content per C atom (enthalpy of combustion, the total energy stored in a compound) in organic compounds is very closely (R2 = 0.98) positively related to NOSC and increases by 108 kJ mol−1 C per one NOSC unit. For the first time we assessed the NOSC of microbial biomass in soil (−0.52) and calculated the corresponding energy content of −510 kJ mol−1 C. We linked CUE and EUE considering the NOSC of microbial biomass and element compositions of substrates utilized by microorganisms. The mean microbial EUE (0.32–0.35) is 18% lower than CUE (0.41) using glucose as a substrate. This definitely indicates that microbial growth is limited by energy relative to C. Based on the comparison of a broad range of processes of C and energy utilization for cell growth and maintenance, as well as database of experimental CUE from various compounds, we clearly explained five mechanisms and main factors why EUE is lower than CUE. The two main mechanisms behind lower EUE versus CUE are: (i) microbial recycling: C can be microbially recycled, whereas energy is always utilized only once, and (ii) chemical reduction of organic and inorganic compounds: Energy is used for reduction, which is ongoing without C utilization.

Topics

No keywords indexed for this article. Browse by subject →

References

126

[1]

Alberts B. (2002)

[2]

Allison S. D. (2011)

[3]

10.1007/b135786

[4]

10.1016/j.soilbio.2013.08.005

[5]

10.1016/j.soilbio.2014.09.005

[6]

Atkins P. (2006)

[7]

10.1007/s10533‐016‐0246‐0

[8]

10.3390/app11114962

[9]

10.1016/s0301‐4622(03)00059‐0

[10]

10.5194/bg‐12‐5929‐2015

[11]

10.1128/aem.02473‐10

[12]

10.15252/msb.20209478

[13]

10.1016/j.soilbio.2013.08.024

[14]

10.1128/jb.183.8.2672‐2676.2001

[15]

10.1016/j.wasman.2007.09.015

[16]

Soil enzymes in a changing environment: Current knowledge and future directions

Richard G. Burns, Jared L. DeForest, Jürgen Marxsen et al.

Soil Biology and Biochemistry 10.1016/j.soilbio.2012.11.009

[17]

10.1073/pnas.2107668118

[18]

Calvin M. (1962)

[19]

10.3389/fmicb.2022.859063

[20]

10.1016/j.soilbio.2020.107945

[21]

10.1016/j.soilbio.2019.01.017

[22]

10.1002/9780470122518.ch7

[23]

10.1016/j.tibtech.2015.06.010

[24]

10.1016/j.soilbio.2020.107720

[25]

10.1016/j.epsl.2007.09.026

[26]

10.1038/nature04514

[27]

10.1016/s0038‐0717(01)00020‐7

[28]

10.1016/j.tim.2009.12.008

[29]

10.1146/annurev.ecolsys.29.1.503

[30]

10.1016/s0301‐4622(02)00069‐8

[31]

10.1016/j.soilbio.2017.01.017

[32]

10.1016/j.soilbio.2015.06.021

[33]

10.1007/s002030050616

[34]

10.1007/s11104‐013‐1764‐3

[35]

10.1038/s41467‐020‐17502‐z

[36]

Duclaux E. (1990)

[37]

10.1002/bit.260210405

[38]

10.1016/j.cell.2016.06.012

[39]

10.1073/pnas.55.4.928

[40]

10.1016/j.mib.2010.03.003

[41]

10.1016/j.soilbio.2009.10.015

[42]

10.1038/nclimate1796

[43]

10.1016/b978-0-12-820202-9.00013-7

[44]

Diversity meets decomposition

Mark O. Gessner, Christopher M. Swan, Christian K. Dang et al.

Trends in Ecology & Evolution 10.1016/j.tree.2010.01.010

[45]

10.1016/s0146‐6380(01)00166‐8

[46]

10.1002/bit.260320112

[47]

10.1111/j.1574‐6976.2010.00253.x

[48]

10.1016/j.soilbio.2021.108225

[49]

10.1016/j.soilbio.2014.06.029

[50]

10.1016/j.soilbio.2015.07.021

Showing 50 of 126 references

Cited By

114

Research on the mechanism of Eucalyptus tannins inhibiting soil respiration

Miaoling Wang, Gairen Yang · 2026

Applied Soil Ecology

Increased Mineral‐Associated Organic Carbon and Persistent Molecules in Allochthonous Blue Carbon Ecosystems

Yuan Li, Chuancheng Fu · 2025

Global Change Biology

Micro‐Faunal and Edaphic Controls on Microbial Carbon Cycling Across Primary and Secondary Successional Trajectories

Lei Du, Roland Bol · 2025

Global Change Biology

Microbial Carbon Use Efficiency and Growth Rates in Soil: Global Patterns and Drivers

Junxi Hu, Yongxing Cui · 2025

Global Change Biology

Effect of degradable microplastics, biochar and their coexistence on soil organic matter decomposition: A critical review

Junjie Lin, Qitai Cheng · 2025

TrAC Trends in Analytical Chemistry

Long-term conservation tillage and straw return affect thermal stability of soil organic matter

Ekaterina Filimonenko, Zhen Liu · 2025

Science of The Total Environment

Dicranopteris pedata improves soil quality by enhancing nutrient deposition, decreasing metal concentration, and boosting microbial diversity on abandoned rare earth elements mining sites

Xi-Wen Cui, Zhen-An Xu · 2024

Journal of Environmental Chemical E...

Soil organic matter priming: The pH effects

Chaoqun Wang, Yakov Kuzyakov · 2024

Global Change Biology

Microbial adaption to stoichiometric imbalances regulated the size of soil mineral-associated organic carbon pool under continuous organic amendments

Xiali Mao, Tao Sun · 2024

Geoderma

“Energy and enthalpy” for microbial energetics in soil

Chaoqun Wang, Yakov Kuzyakov · 2024

Global Change Biology

Metrics

114

Citations

126

References

Details

Published: Aug 30, 2023
Vol/Issue: 29(22)
Pages: 6170-6187
License: View

Authors

C

Chaoqun Wang

Biogeochemistry of Agroecosystems University of Goettingen Goettingen Germany; Faculty of Land and Food Systems University of British Columbia Vancouver Canada

Y

Yakov Kuzyakov

Department of Soil Science of Temperate Ecosystems, Department of Agricultural Soil Science University of Goettingen Goettingen Germany

Cite This Article

Chaoqun Wang, Yakov Kuzyakov (2023). Energy use efficiency of soil microorganisms: Driven by carbon recycling and reduction. Global Change Biology, 29(22), 6170-6187. https://doi.org/10.1111/gcb.16925

Energy use efficiency of soil microorganisms: Driven by carbon recycling and reduction

You May Also Like