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Microbes and sunlight convert terrigenous dissolved organic matter (DOM) in surface waters to greenhouse gases. Prior studies show contrasting results about how biological and photochemical processes interact to contribute to the degradation of DOM. In this study, DOM leached from the organic layer of tundra soil was exposed to natural sunlight or kept in the dark, incubated in the dark with the natural microbial community, and analyzed for gene expression and DOM chemical composition. Microbial gene expression (metatranscriptomics) in light and dark treatments diverged substantially after 4 hours. Gene expression suggested that sunlight exposure of DOM initially stimulated microbial growth by (a) replacing the function of enzymes that degrade higher molecular weight DOM such as enzymes for aromatic carbon degradation, oxygenation, and decarboxylation, and (b) releasing low molecular weight compounds and inorganic nutrients from DOM. However, growth stimulation following sunlight exposure of DOM came at a cost. Sunlight depleted the pool of aromatic compounds that supported microbial growth in the dark treatment, ultimately causing slower growth in the light treatment over 5 days. These first measurements of microbial metatranscriptomic responses to photo-alteration of DOM provide a mechanistic explanation for how sunlight exposure of terrigenous DOM alters microbial processing and respiration of DOM.
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Experimental metatranscriptomics reveals the costs and benefits of dissolved organic matter photo‐alteration for freshwater microbes
This paper presents three novel findings about the interaction of sunlight and microbes during the degradation of terrigenous dissolved organic matter (DOM) in aquatic systems. First, it shows that sunlight can replace the function of certain microbial enzymes, which provides an energy savings for microbes and increases their investment in growth. Second, differential gene expression provides a new, genomics-based line of evidence for the mechanisms of photo-alteration of DOM and demonstrates the effects of these mechanisms on microbes and specific metabolic functions (through metatranscriptomics). Third, it provides the first evidence of how decarboxylation of DOM by sunlight impacts microbes.
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- PAR ID:
- 10169979
- Date Published:
- Journal Name:
- Environmental Microbiology
- ISSN:
- 1462-2912
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Dissolved organic matter (DOM) plays an important role in carbon cycling in natural waters. The processing of DOM in these waters can occur via photooxidation, or interaction with sunlight. This processing can lead to the production of CO2, and also the alteration of organic compounds that make up DOM. It is likely that the extent of photooxidation is at least partially determined by the chemical composition of DOM. Fourier-transform ion cyclotron resonance mass spectrometry (FT-ICR MS) was used to characterize the dissolved organic matter at the molecular level for all water samples, both before and after light exposure to better understand the photooxidation of DOM. Chemical formulas were assigned to mass to generated mass to charge ratios using a custom script in R, resulting in a list of chemical formula assignments for each DOM sample, at multiple light exposure time points.more » « less
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Tidal wetlands are a significant source of dissolved organic matter (DOM) to coastal ecosystems, which impacts nutrient cycling, light exposure, carbon dynamics, phytoplankton activity, microbial growth, and ecosystem productivity. There is a wide variety of research on the properties and sources of DOM; however, little is known about the characteristics and degradation of DOM specifically sourced from tidal wetland plants. By conducting microbial and combined UV exposure and microbial incubation experiments of leachates from fresh and senescent plants in Chesapeake Bay wetlands, it was demonstrated that senescent material leached more dissolved organic carbon (DOC) than fresh material (77.9 ± 54.3 vs 21.6 ± 11.8 mg DOC L−1, respectively). Degradation followed an exponential decay pattern, and the senescent material averaged 50.5 ± 9.45% biodegradable DOC (%BDOC), or the loss of DOC due to microbial degradation. In comparison, the fresh material averaged a greater %BDOC (72.6 ± 19.2%). Percent remaining of absorbance (83.3 ± 26.7% for fresh, 90.1 ± 10.8% for senescent) was greater than percent remaining DOC, indicating that colored DOM is less bioavailable than non-colored material. Concentrations of DOC leached, %BDOC, and SUVA280 varied between species, indicating that the species composition of the marsh likely impacts the quantity and quality of exported DOC. Comparing the UV + microbial to the microbial only incubations did not reveal any clear effects on %BDOC but UV exposure enhanced loss of absorbance during subsequent dark incubation. These results demonstrate the impacts of senescence on the quality and concentration of DOM leached from tidal wetland plants, and that microbes combined with UV impact the degradation of this DOM differently from microbes alone.more » « less
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Manganese (Mn) oxide solids widely exist in nature, serving as both electron donors and acceptors for a variety of redox reactions. Previous studies have highlighted the adsorption of dissolved organic matter (DOM) on Mn oxides, as well as the reduction of Mn oxides by DOM. Here, we show the underappreciated roles of photolytic reactions of DOM in Mn2+(aq) oxidation and its consequential formation of Mn oxide solids. During the photolysis of DOM, reactive intermediates including excited triplet state DOM (3DOM*), hydroxyl radical (•OH), superoxide radical (O2•−), hydrogen peroxide (H2O2), and singlet oxygen (1O2) can be generated. Among them, we found that O2•− was responsible for Mn oxidation. In addition, in the presence of bromide ions (Br−), the photolytic reactions between DOM and Br− formed reactive bromide radicals and facilitated the oxidation of Mn2+(aq) to Mn oxide solids. Moreover, the composition of DOM affected its oxidative capability. When DOM contained more aromatic functional groups, we observed more oxidation of Mn2+ to Mn oxides. These new findings advance our knowledge of natural Mn2+ oxidation and Mn(III/IV) oxide formation, as well as the hitherto overlooked oxidative role of DOM in the oxidation of metal ions in surface water under sunlight illumination.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1111/1462-2920.15121
