Glucose triggers strong taxon‐specific responses in microbial growth and activity: insights from <scp>DNA</scp> and <scp>RNA qSIP</scp>

Papp, Katerina; Hungate, Bruce A.; Schwartz, Egbert

doi:10.1002/ecy.2887

Cited by 21 publications

(13 citation statements)

References 78 publications

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“…However, care must be taken in not over interpreting these results as we investigated only one fungal PLFA in comparison to four PLFAs for gram-positive bacteria. Furthermore, even though incorporation of 13 C-glucose into bacterial and microeukaryote populations has been shown earlier through rRNA stable isotope probing (Kramer et al, 2016), a non-uniform labeling of soil microbial biomass through the glucose must be kept in mind while interpreting our results (Papp et al, 2020). Nevertheless, our results support the established idea of bacteria as dominant consumers of highly labile C (Castro et al, 2010;Vries and de Caruso, 2016), although it was recently shown that specific fungi quickly utilize labile rhizodeposits (Hünninghaus et al, 2019).…”

Section: Incorporation Into Key Players Of Carbon Decomposition and Its Turnoversupporting

confidence: 51%

Soil Properties Control Microbial Carbon Assimilation and Its Mean Residence Time

Ali

Poll

Kandeler

2020

Front. Environ. Sci.

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Microbial assimilation and stabilization of soil organic carbon (SOC) is an important process in global carbon cycling. For an improved understanding of climate-induced changes in ecosystem C dynamics, it is important to know the group-specific turnover of microbial C. Consequently, we wanted to answer the questions if fungi store newly assimilated C longer than bacteria and if climatic and edaphic properties of different regions affect microbial C assimilation and its subsequent release. This study presents results from a 112-day long field experiment where endogenous microorganisms from two agricultural soils were labeled with 13 C labeled glucose to follow the dynamics of newly assimilated C. Both soils were representative for the respective study regions (Kraichgau and Swabian Alb). Whereas, microbial assimilation of newly added C was higher in Kraichgau than in Swabian Alb, the opposite result was obtained for the mean residence time (MRT) of microbial biomass C (76 days in Kraichgau and 93 days in Swabian Alb). The accelerated turnover rates of microbial C in the warmer soil of Kraichgau with lower clay content might be an important mechanism explaining the differences in SOC content between both regions. Gram-positive bacteria assimilated more 13 C-glucose into their biomass than fungi and the MRT of C was higher in bacteria as compared to fungi in both regions. Beside these dynamic substrate utilization strategies, we observed possible cross feeding by gram-negative bacteria. Carbon MRT in fungi was region specific and was best represented by a two-pool model; the initial MRT ranged between 5 and 39 days and was, in the end, higher than 4 years. This hints toward a functional separation of the fungal community; fast growing fungi dominant in the early phase and internal redistribution of C in the second phase of decomposition. Our study identified microbial group and region specific MRT of freshly assimilated C as an important parameter, which might help to explain the commonly found variation in soil respiration and SOC stabilization.

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Section: Incorporation Into Key Players Of Carbon Decomposition and Its Turnoversupporting

confidence: 51%

Soil Properties Control Microbial Carbon Assimilation and Its Mean Residence Time

Ali

Poll

Kandeler

2020

Front. Environ. Sci.

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“…However, it must be kept in mind that gene expression levels do not necessarily correlate with protein abundance, enzyme activity, or respiratory-based physiological approaches (Nannipieri et al, 2003). Recently, qSIP was proposed as an approach to quantify the metabolic activity of all specific groups of microorganisms that contribute to the substrate conversion process (Hungate et al, 2015;Papp et al, 2020).…”

Section: Destructive Approachesmentioning

confidence: 99%

Bridging Microbial Functional Traits With Localized Process Rates at Soil Interfaces

et al. 2021

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In this review, we introduce microbially-mediated soil processes, players, their functional traits, and their links to processes at biogeochemical interfaces [e.g., rhizosphere, detritusphere, (bio)-pores, and aggregate surfaces]. A conceptual view emphasizes the central role of the rhizosphere in interactions with other biogeochemical interfaces, considering biotic and abiotic dynamic drivers. We discuss the applicability of three groups of traits based on microbial physiology, activity state, and genomic functional traits to reflect microbial growth in soil. The sensitivity and credibility of modern molecular approaches to estimate microbial-specific growth rates require further development. A link between functional traits determined by physiological (e.g., respiration, biomarkers) and genomic (e.g., genome size, number of ribosomal gene copies per genome, expression of catabolic versus biosynthetic genes) approaches is strongly affected by environmental conditions such as carbon, nutrient availability, and ecosystem type. Therefore, we address the role of soil physico-chemical conditions and trophic interactions as drivers of microbially-mediated soil processes at relevant scales for process localization. The strengths and weaknesses of current approaches (destructive, non-destructive, and predictive) for assessing process localization and the corresponding estimates of process rates are linked to the challenges for modeling microbially-mediated processes in heterogeneous soil microhabitats. Finally, we introduce a conceptual self-regulatory mechanism based on the flexible structure of active microbial communities. Microbial taxa best suited to each successional stage of substrate decomposition become dominant and alter the community structure. The rates of decomposition of organic compounds, therefore, are dependent on the functional traits of dominant taxa and microbial strategies, which are selected and driven by the local environment.

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“…Microbial communities experience sudden changes in C and N availability associated with plant root exudation ( 13 ), trophic interactions ( 14 , 15 ), and litter leachate ( 16 ). Since soil microbes are typically limited by labile C and energy ( 17 – 19 ), the addition of a C-rich substrate is expected to stimulate growth and activity ( 20 ), increasing the demand for N ( 21 ). Whether N is derived from the uptake of organic N present in the substrate or mineral N available in the soil depends largely on the C-to-N (C:N) ratio of the substrate ( 22 ).…”

Section: Introductionmentioning

confidence: 99%

Rapid Response of Nitrogen Cycling Gene Transcription to Labile Carbon Amendments in a Soil Microbial Community

et al. 2021

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Episodic inputs of labile carbon (C) to soil can rapidly stimulate nitrogen (N) immobilization by soil microorganisms. However, the transcriptional patterns that underlie this process remain unclear. In order to better understand the regulation of N cycling in soil microbial communities, we conducted a 48-h laboratory incubation with agricultural soil where we stimulated the uptake of inorganic N by amending the soil with glucose. We analyzed the metagenome and metatranscriptome of the microbial communities at four time points that corresponded with changes in N availability. The relative abundances of genes remained largely unchanged throughout the incubation. In contrast, glucose addition rapidly increased the transcription of genes encoding ammonium and nitrate transporters, enzymes responsible for N assimilation into biomass, and genes associated with the N regulatory network. This upregulation coincided with an increase in transcripts associated with glucose breakdown and oxoglutarate production, demonstrating a connection between C and N metabolism. When concentrations of ammonium were low, we observed a transient upregulation of genes associated with the nitrogen-fixing enzyme nitrogenase. Transcripts for nitrification and denitrification were downregulated throughout the incubation, suggesting that dissimilatory transformations of N may be suppressed in response to labile C inputs in these soils. These results demonstrate that soil microbial communities can respond rapidly to changes in C availability by drastically altering the transcription of N cycling genes. IMPORTANCE A large portion of activity in soil microbial communities occurs in short time frames in response to an increase in C availability, affecting the biogeochemical cycling of nitrogen. These changes are of particular importance as nitrogen represents both a limiting nutrient for terrestrial plants as well as a potential pollutant. However, we lack a full understanding of the short-term effects of labile carbon inputs on the metabolism of microbes living in soil. Here, we found that soil microbial communities responded to labile carbon addition by rapidly transcribing genes encoding proteins and enzymes responsible for inorganic nitrogen acquisition, including nitrogen fixation. This work demonstrates that soil microbial communities respond within hours to carbon inputs through altered gene expression. These insights are essential for an improved understanding of the microbial processes governing soil organic matter production, decomposition, and nutrient cycling in natural and agricultural ecosystems.

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Glucose triggers strong taxon‐specific responses in microbial growth and activity: insights from DNA and RNA qSIP

Cited by 21 publications

References 78 publications

Soil Properties Control Microbial Carbon Assimilation and Its Mean Residence Time

Soil Properties Control Microbial Carbon Assimilation and Its Mean Residence Time

Bridging Microbial Functional Traits With Localized Process Rates at Soil Interfaces

Rapid Response of Nitrogen Cycling Gene Transcription to Labile Carbon Amendments in a Soil Microbial Community

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