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MicrobiologySoil Biology and Biochemistry
Peer-reviewed journal article

Soil microbes prefer organic acids over sugars in simulated root exudation

Julia WiesenbaueriD, Stefan GorkaiD, Kian JenabiD, Raphael SchusteriD, Naresh KumariD, Cornelia RottensteineriD, Alexander KönigiD, Stephan M. KraemeriD, Erich InselsbacheriD, Christina KaiseriD

Abstract

Sugars and organic acids, primary components in plant root exudates, are thought to enhance microbial decomposition of organic matter in the rhizosphere. However, their specific impacts on microbial activity and nutrient mobilisation remain poorly understood. Here, we simulated passive root exudation to investigate the distinct effects of sugars and organic acids on microbial metabolism in the rhizosphere. We released 13C- labelled sugars and/or organic acids via reverse microdialysis into intact meadow and forest soils over 6-hours. We measured substrate-induced microbial respiration, soil organic matter mineralization, metabolite concentrations, and substrate incorporation into lipid-derived fatty acids. Our results reveal a pronounced microbial preference for organic acids over sugars, with organic acids being removed faster from the exudation spot and preferentially respired by microbes. Unlike sugars, organic acids increased concentrations of microbial metabolic byproducts and cations (K, Ca, Mg) near the exudation spot. Our results challenge the prevailing assumption that sugars are the most readily available and rapidly consumed substrates for soil microbes. Microbial preference for organic acids indicates a trade-off between rapid biomass growth and ATP yield. Our findings underscore the significant role of exudate composition in influencing microbial dynamics and nutrient availability, and emphasize the importance of biotic and abiotic feedback mechanisms in the rhizosphere in regulating root exudation.

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Claude Opus 5.5 · xhigh effort · 8 Nov 2026 · from the full text of version 1 (3 Dec 2024) · CC BY 4.0

In intact meadow and forest soil cores, 13C-labelled acetate and succinate released by reverse microdialysis left the exudation spot faster and were respired more than glucose and fructose.

How sugars and organic acids in root exudates separately shape microbial activity and nutrient release in the rhizosphere is poorly resolved, and sugars are widely assumed to be what soil microbes consume most readily. Unlike mass-flow artificial roots, reverse microdialysis releases compounds by diffusion into undisturbed soil, so release rates themselves report how quickly each compound is removed; the two classes are tested alone and combined in two contrasting soils.

Key results

  1. ShownIn both soils, microbes respired much more substrate carbon when the exudate contained organic acids than when it held only sugars. Respiration of soil organic matter (SOM) stayed at control levels.

    Substrate-derived (13C) respiration peaked during the pulse. It was about 4-8 times higher with organic acids (alone or mixed) than with sugars only; mixed and organic-acid-only differed slightly and non-significantly. SOM-derived respiration matched controls over 18 days. Extrapolating 3 h of measurement to the 6-h pulse, about 8, 10 and 9% of released C was respired (sugar, organic acid, mixed); n = 5. · 3.1 Microbes preferentially respired organic…; Figure legends

  2. ShownAcetate and succinate diffused from the probe into intact soil far more readily than glucose and fructose. In meadow soil, much less of them was recovered afterwards. Both point to faster removal from the exudation spot.

    Transfer: acetate 55-67%, succinate 39-41% vs glucose 7-17%, fructose 14-23%; over 6 h, 430-490 vs 90-110 nmol C released (acids vs sugars). 12-h retrieval: <1% of all compounds in forest soil; meadow <1% acetate, about 6% succinate, 28-42% glucose, 21-25% fructose. (The discussion [S17] instead describes high sugar back-retrieval in forest soil, which conflicts with the results section.) · 3.2 Higher passive release for organic acids…; 4.1 Disparity in sugar and organic acid release

  3. ShownOrganic acids, alone or with sugars, raised short-chain fatty acids (SCFAs) and cations around the probe during the pulse, a pattern largely consistent across both soils (K in forest soil only). Sugars alone produced no change relative to controls.

    Butyrate, lactate and propionate rose significantly about 3 h into the pulse. In forest soil, lactate rose 10-fold with organic acids alone, a much larger response than with the mixed exudate. NH4, K, Mg and Ca also rose significantly during the pulse (K in forest soil only, per the discussion). Effects at later time points (days 2-18) were inconsistent across soils and treatments. · 3.3 Organic acids, but not sugars, induced…; 4.5 Organic acid induced mobilization of cations

  4. SuggestedExudate carbon reached microbial lipids only weakly in soil more than 2.5 mm from the probe. Biomass did not change, and the clearest 13C uptake was in meadow soil given the mixed exudate.

    Total phospholipid fatty acids (PLFAs) and group markers (gram-negative, gram-positive, fungi, actinobacteria) were unchanged. Meadow, mixed: neutral lipid fatty acids (NLFAs, storage proxy) rose, mainly in general NLFA biomarkers such as 16:0, and PLFAs were 13C-enriched. Meadow, sugars only: 13C-enriched NLFAs. Forest, organic acids: PLFA 13C trend significant only for general and gram-negative markers. · 3.4 Combined sugars and organic acids are…; 4.3 Microbial incorporation of substrate-C into…

  5. ClaimedThe authors read the preference as microbes trading ATP yield for faster ATP production. They also propose that gluconeogenesis is the default pathway in most soil microbes, and that hydroponic sampling may overestimate root sugar exudation.

    The argument rests on stated aerobic yields (about 28-32 ATP per hexose vs about 12 per acetate), the lowest 13C respiration under sugars only, and the feedback inherent in passive diffusion. No pathway-level or O2 measurements are presented. · 4.2 Preferential utilization of organic acids…; 4.6 Implications of rhizosphere feedback on root…

Methods, data and reproducibility

13C-labelled glucose plus fructose, acetate plus succinate, or all four (500 µmol C l^-1 each), or water, were released for 6 h by reverse microdialysis into paired intact meadow and beech forest soil cores. Over 18 days, dialysate sugars, anions and cations (HPLC), substrate- vs soil-organic-matter-derived respiration (13C-CO2) and 13C in phospholipid and neutral lipid fatty acids were tracked.

  • Intact meadow soil cores (Cambisol, loamy sand; extensively managed meadow, Gumpenstein, Austria; upper 6 cm, sampled July 2019) · soil microbial community · n = 5 large cores from five spots along an 8 m transect; n = 5 per treatment
  • Intact beech (Fagus sylvatica) forest soil cores (Dystric Cambisol, silty clay; Klausen-Leopoldsdorf, Austria; upper 6 cm, sampled July 2019) · soil microbial community · n = 5 large cores from random spots in a 5 x 5 m plot; n = 5 per treatment
  • Deposited study data (Zenodo) · 10.5281/zenodo.13338424
Methods & tools
CMA 20 microdialysis probes (20 kDa cut-off), CMA 4004 syringe pumps, Dionex ICS 5000+ HPLC, GasBench II with Delta V Advantage IRMS, Agilent 5110 ICP-OES, Trace GC Ultra with ISQ mass spectrometer, GC-IRMS (Finnigan Delta-V), PLFA/NLFA extraction (Gorka et al. 2023), chloroform fumigation extraction, R 4.2.2, ggplot2, Kruskal-Wallis and Dunn's tests
Data & accessions
https://doi.org/10.5281/zenodo.13338424
Reagents & environment
Statistics in R version 4.2.2; figures made with ggplot2 (version not given).
Reproducibility gaps
No analysis code is linked. The mixing-model calculations, HPLC methods and lipid extraction details are in supporting information (Methods S1-S6), which is not included in this text; post-hoc statistics are in Tables S1-S3.
Limitations (6)
  • Lipid fatty acids were measured only in soil more than 2.5 mm from the membrane, because the central soil was used for earlier work. The 13C signal in PLFAs and NLFAs is therefore low and a conservative estimate. · stated by the authors
  • It is unresolved whether the butyrate, propionate and lactate came from succinate breakdown or from induced SOM decomposition. The anoxic-hotspot explanation is a hypothesis, since O2 was not monitored. · stated by the authors
  • Localised increases in SOM-derived respiration near the probe may have gone undetected. · stated by the authors
  • Because acetate and succinate are charged, their faster removal may partly reflect sorption to minerals rather than only microbial uptake. · stated by the authors
  • Organic acids delivered far more C than sugars (430-490 vs 90-110 nmol C), yet a similar share was respired (about 8, 10 and 9%). Higher organic-acid respiration may therefore largely track delivery, and the preference argument leans on the release rate itself. · noted in this summary
  • The results report <1% retrieval of all compounds from forest soil, but the discussion cites high sugar back-retrieval in forest soil, so the retrieval evidence for faster acid removal is internally inconsistent for that soil. No sterilised control separates sorption from microbial uptake. · noted in this summary

Who should read:Read this if you study rhizosphere carbon cycling or root exudation and want intact-soil evidence, from diffusion-based reverse microdialysis, that microbes remove and respire organic acids faster than sugars.

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