Drought Shifts the Type of Carbon Emitted by Soil Microbes

The Science 

Microbes produce and release volatile organic compounds (VOCs) as metabolites, which can be either quickly used as carbon sources in the soil by other microbes or released into the atmosphere. In newly published research, a team of scientists used an isotopic carbon tracer to track carbon allocation in soils within an artificial tropical rainforest. They discovered microbes switch carbon allocation from growth to stress molecules under drought conditions. These results demonstrate the impact of drought on microbial activity, particularly on how the types of carbon in soil can change, leading to a loss of carbon to the atmosphere as carbon dioxide and VOCs.  

The Impact 

Drought impacts on soil microbial activity can change where carbon ends up, potentially leading to an increased loss of carbon to the atmosphere as VOCs. Characterizing microbe-mediated carbon flow from soil to the atmosphere is important for understanding soil VOCs in environmental conditions such as drought. In this study, researchers examined drought impacts on carbon allocation by soil microbes. They found that in drought conditions, microbially produced acetate, acetone, and C4H6O2 (diacetyl) soil emissions increased. Results of this research also suggest that some VOCs, such as acetate, acetone, and diacetyl, could signal soil microbial stress and even be used as bioindicators for specific microbial metabolic processes occurring belowground. As droughts in the tropics increase in frequency and duration, findings such as these are important for furthering understanding of how microbial activity can shift carbon cycling and storage pools during drought. 

Summary 

A multi-institutional team of scientists examined drought impacts on carbon allocation by soil microbes in the artificial tropical rainforest, Biosphere 2, by tracking 13C from position-specific 13C-pyruvate into CO₂  and VOCs and by employing multi-omics analyses. As microbes entered a stress-induced state, they switched their internal carbon allocation from growth to stress biomolecules, such as trehalose and other osmolytes, thereby leading to decreased efficiency in their carbon cycling and loss of volatile intermediate metabolites to the atmosphere. Researchers used nuclear magnetic resonance (NMR) and Fourier-transform ion cyclotron resonance (FTICR) mass spectrometry at the Environmental Molecular Sciences Laboratory, a Department of Energy (DOE), Office of Science user facility, to characterize soil metabolomics and organic matter profiles before and after drought. Results from NMR, which targets small metabolites, pointed to a sharp increase in osmolytes such as betaine and trehalose during drought, and a decrease in amino acids, confirming the team’s conclusions that microbes increased production of stress biomolecules during drought and decreased carbon allocation to biomass (including amino acids). FTICR results indicated a large shift in organic carbon pools with a decrease in more labile compounds such as carbohydrates, proteins, and amino sugars. Additionally, there was an increase in complex compounds such as lignins and tannins during drought, supporting conclusions that microbial activity shifted in parallel to changing carbon pools during drought. 

Contacts 

Linnea Honeker, Lawrence Livermore National Laboratory, honeker1@llnl.gov 

Giovanni Pugliese, University of Freiburg and Max Planck Institute for Chemistry, g.pugliese@mpic.de 

Malak Tfaily, University of Arizona, tfaily@arizona.edu 

David Hoyt, EMSL, david.hoyt@pnnl.gov 

Laura Meredith, University of Arizona, aurameredith@arizona.edu  

Funding 

A portion of this research was performed under the Facilities Integrating Collaborations for User Science program and used resources at EMSL and the Joint Genome Institute, both DOE Office of Science user facilities sponsored by the Biological and Environmental Research program. Research was also supported in part by the European Research Council and National Science Foundation CAREER Award, Biosphere 2 through the office of the senior vice president for research innovation and impact at the University of Arizona, the BIO5 Postdoctoral Fellowship, the German Federal Ministry of Education, and the Max Planck Society. Additional support was provided through the Philecology Foundation. 

Publication 

Honeker, L.K et al. “Drought re-routes soil microbial carbon metabolism towards emission of volatile metabolites in an artificial tropical rainforest.” Nature Microbiology 8, 1480–1494. (2023) [DOI: 10.1038/s41564-023-01432-9]