Microbial growth and carbon use efficiency in soil: Links to fungal-bacterial dominance, SOC-quality and stoichiometry

2019 ◽  
Vol 131 ◽  
pp. 195-205 ◽  
Author(s):  
Margarida Soares ◽  
Johannes Rousk
2020 ◽  
Author(s):  
Arjun Chakrawal ◽  
Anke M. Herrmann ◽  
Stefano Manzoni

<p>Soil organic carbon (SOC) represents both a source of energy (catabolism) and a building material for biosynthesis (anabolism) for microorganisms. Microbial carbon use efficiency (CUE) – the ratio of C used for biosynthesis over C consumed – measures the partitioning between anabolic and catabolic processes. While most work on CUE has been based on C mass flows, the role of SOC energy content, microbial energy demand, and general energy flows on CUE have been rarely considered. Thus, a bioenergetics perspective on CUE could provide new insights on how microorganisms utilize C substrates and ultimately allow C to be stabilized in soils.</p><p>The microbial growth reactions are generally associated with a negative enthalpy change, which results in heat dissipation from the system. This heat can be measured using an isothermal calorimeter, which is often coupled with respiration measurements. This coupled system allows studying energy and C exchanges, and calculating their ratio referred to as the calorespirometric ratio (CR). Here, we formulate a coupled mass and energy balance model for microbial growth and provide a generalized relationship between CUE and CR. In the model, we consider two types of organic C in soils, the added substrate (i.e., glucose) and the native SOC. Furthermore, we assume that glucose is taken up via aerobic (AE) and two fermentation metabolic pathways – glucose to ethanol (F1) and glucose to lactic acid (F2); for simplicity, only aerobic growth on the native SOC was adopted. We use this model as a framework to generalize previous formulations and generate hypotheses on the expected variations in CR as a function of substrate type, metabolic pathways, and microbial properties (specifically CUE). In turn, the same equations can be used to estimate CUE from measured CR.</p><p>Our results show that in a non-growing system, CR depends only on the rates of different metabolic pathways (AE, F1, and F2). While in growing systems, CR is a function of rates as well as growth yields for these metabolic pathways. Under purely aerobic conditions, our model predicts that CUE increases with increasing CR when the degree of reduction of the substrate is higher than that of the microbial biomass. Similarly, CUE decreases with increasing CR when the degree of reduction of substrate is lower than that of the biomass. In the case of combined metabolism – aerobic and fermentation simultaneously – CUE is not only a function of CR and the degree of reduction of substrates but also the rates and growth yields of all metabolic pathways involved. To summarize, in this contribution we illustrate how calorespirometry can become an efficient tool to evaluate CUE and the role of different metabolic pathways in soil systems.</p>


2020 ◽  
Vol 26 (9) ◽  
pp. 5333-5341 ◽  
Author(s):  
Alberto Canarini ◽  
Wolfgang Wanek ◽  
Margarete Watzka ◽  
Taru Sandén ◽  
Heide Spiegel ◽  
...  

2020 ◽  
Vol 3 (1) ◽  
Author(s):  
Eva Simon ◽  
Alberto Canarini ◽  
Victoria Martin ◽  
Joana Séneca ◽  
Theresa Böckle ◽  
...  

Abstract Microbial growth and carbon use efficiency (CUE) are central to the global carbon cycle, as microbial remains form soil organic matter. We investigated how future global changes may affect soil microbial growth, respiration, and CUE. We aimed to elucidate the soil microbial response to multiple climate change drivers across the growing season and whether effects of multiple global change drivers on soil microbial physiology are additive or interactive. We measured soil microbial growth, CUE, and respiration at three time points in a field experiment combining three levels of temperature and atmospheric CO2, and a summer drought. Here we show that climate change-driven effects on soil microbial physiology are interactive and season-specific, while the coupled response of growth and respiration lead to stable microbial CUE (average CUE = 0.39). These results suggest that future research should focus on microbial growth across different seasons to understand and predict effects of global changes on soil carbon dynamics.


2021 ◽  
Author(s):  
Xuehui Feng ◽  
Jie Hu ◽  
Yuanhe Yang ◽  
Leiyi Chen

<p>Elucidating the mechanisms underlying the changes in microbial physiology under anthropogenic nitrogen (N) input is of fundamental importance for understanding the carbon-N interaction under global environmental change. Carbon use efficiency (CUE), the ratio of microbial growth to assimilation, represents a critical microbial metabolic parameter that controls the fate of soil C. Despite the recognized importance of mineral protection as a driver of soil C cycling in terrestrial ecosystems, little is known on how mineral-organic association will modulate the response of microbial CUE to increasing N availability. Here, by combining a 6-year N‐manipulation experiment and <sup>18</sup>O isotope incubation, mineral analysis and a two-pool C decomposition model, we evaluate how N-induced modification in mineral protection affect the changes in microbial growth, respiration and CUE. Our results showed that microbial CUE increased under N enrichment due to the enhanced microbial growth and decreased respiration. Such changes in microbial physiology further led to a significant decrease in CO<sub>2</sub>-C release from the slow C pool under high N input. More importantly, the disruption in mineral-organic association induced by elevated root exudates is the foremost reason for the enhanced microbial growth and CUE under high N input. Taken together, these findings provide an empirical evidence for the linkage between soil mineral protection and microbial physiology, and highlight the need to consider the plant-mineralogy-microbial interactions in Earth system models to improve the prediction of soil C fate under global N deposition.</p>


PLoS ONE ◽  
2014 ◽  
Vol 9 (4) ◽  
pp. e93282 ◽  
Author(s):  
Evgenia Blagodatskaya ◽  
Sergey Blagodatsky ◽  
Traute-Heidi Anderson ◽  
Yakov Kuzyakov

2021 ◽  
Author(s):  
Alberto Canarini ◽  
Lucia Fuchslueger ◽  
Jörg Schnecker ◽  
Margarete Watzka ◽  
Erich M. Pötsch ◽  
...  

<p>The raise of atmospheric CO<sub>2</sub> concentrations, with consequent increase in global warming and the likelihood of severe droughts, is altering the terrestrial biogeochemical carbon (C) cycle, with potential feedback to climate change.  Microbial physiology, i.e. growth, turnover and carbon use efficiency, control soil carbon fluxes to the atmosphere. Thus, improving our ability to accurately quantify microbial physiology, and how it is affected by climate change, is essential. Recent advances in the field have allowed the quantification of community-level microbial growth and carbon use efficiency in dry conditions via an <sup>18</sup>O water vapor equilibration technique, allowing for the first time to evaluate microbial growth rates under drought conditions.</p><p>We modified the water vapor equilibration method using <sup>2</sup>H-labelled water to estimate microbial community growth via deuterium incorporation into fatty acids. First, we verified that a rapid equilibration of <sup>2</sup>H with soil water is possible. Then, we applied this approach to soil samples collected from a long-term climate change experiment (https://www.climgrass.at/) where warming, elevated atmospheric CO<sub>2</sub> (eCO<sub>2</sub>) and drought are manipulated in a full factorial combination. Samples were taken in the field during peak drought and one week after rewetting. We used a high-throughput method to extract phospho- and neutral- lipid fatty acids (PLFA and NLFA) and we measured <sup>2</sup>H enrichment in these compounds via GC-IRMS.</p><p>Our results show that within 48 h, <sup>2</sup>H in water vapor was in equilibrium with soil water and was detectable in microbial PLFA and NLFAs. We were able to quantify growth rates for different groups of microorganisms (Gram-positive, Gram-negative, Fungi and Actinobacteria) and calculate community level carbon use efficiency. We showed that a reduction of carbon use efficiency in the combined warming + eCO<sub>2</sub> treatment was caused by a reduced growth of fungi and overall higher respiration rates. During drought, all groups showed a reduction in growth rates, albeit the reduction was stronger in bacteria than in fungi. Moreover, fungi accumulated high amounts of <sup>2</sup>H into NLFAs, representing up to one third of the amount in PLFAs and indicating enhanced investment into storage compounds. This investment was still higher than in control plots two days after rewetting and returned to control levels within a week.</p><p>Our study demonstrates that climate change can have strong effects on microbial physiology, with group-specific responses to different climate change factors. Our approach has the benefit of using fatty acid biomarkers to improve resolution into community level growth responses to climate change. This allowed a quantification of group-specific growth rates and concomitantly a measurement of investment into reserve compounds.</p>


2020 ◽  
Author(s):  
Alberto Canarini ◽  
Wolfgang Wanek ◽  
Margarete Watzka ◽  
Taru Sandén ◽  
Heide Spiegel ◽  
...  

<p>As the global hydrological cycle intensifies with future warming, more severe droughts will alter the terrestrial biogeochemical carbon (C) cycle. As soil microbial physiology controls the large fluxes of C from soil to the atmosphere, improving our ability to accurately quantify microbial physiological parameters in soil is essential. However, currently available methods to determine microbial C metabolism in soil require the addition of water, which makes it practically impossible to measure microbial physiology in dry soil samples without stimulating microbial growth and respiration (namely, the “Birch effect”).</p><p>We developed a new method based on in vivo <sup>18</sup>O water vapor equilibration to minimize soil re-wetting effects. This method allows the isotopic labelling of soil water without any liquid water or dissolved substrate addition to the sample. This was compared to the main current method (<sup>18</sup>O-water application method) in soil samples either at near-optimal water holding capacity or in air dry soils. We generated time curves of the isotopic equilibration between liquid soil water and water vapor and calculated the average atom percent <sup>18</sup>O excess over incubation time, which is necessary to calculate microbial growth rates. We tested isotopic equilibration patterns in nine different soils (natural and artificially constructed ones) covering a wide range of soil texture and organic matter content. We then measured microbial growth, respiration and carbon use efficiency in three natural soils (either dry or at near-optimal water holding capacity). The proposed <sup>18</sup>O vapor equilibration method provides similar results as the currently widely used method of liquid <sup>18</sup>O water addition to determine microbial growth when used a near-optimal water holding capacity. However, when applied to dry soils the liquid <sup>18</sup>O water addition method overestimated growth by up to 250%, respiration by up to 500%, and underestimated carbon use efficiency by up to 40%.</p><p>Finally, we applied the new method to undisturbed biocrust samples, at field water content (1-3%), and show for the first time real microbial growth rates and CUE values in such arid ecosystems. We describe new insights into biogeochemical cycling of C that the new method can help uncover and consider the wide range of questions regarding microbial physiology and its response to global change that can now be proposed and addressed.</p>


2020 ◽  
Vol 86 (24) ◽  
Author(s):  
K. Taylor Cyle ◽  
Annaleise R. Klein ◽  
Ludmilla Aristilde ◽  
Carmen Enid Martínez

ABSTRACT We used time-resolved metabolic footprinting, an important technical approach used to monitor changes in extracellular compound concentrations during microbial growth, to study the order of substrate utilization (i.e., substrate preferences) and kinetics of a fast-growing soil isolate, Paraburkholderia sp. strain 1N. The growth of Paraburkholderia sp. 1N was monitored under aerobic conditions in a soil-extracted solubilized organic matter medium, representing a realistic diversity of available substrates and gradient of initial concentrations. We combined multiple analytical approaches to track over 150 compounds in the medium and complemented this with bulk carbon and nitrogen measurements, allowing estimates of carbon use efficiency throughout the growth curve. Targeted methods allowed the quantification of common low-molecular-weight substrates: glucose, 20 amino acids, and 9 organic acids. All targeted compounds were depleted from the medium, and depletion followed a sigmoidal curve where sufficient data were available. Substrates were utilized in at least three distinct temporal clusters as Paraburkholderia sp. 1N produced biomass at a cumulative carbon use efficiency of 0.43. The two substrates with highest initial concentrations, glucose and valine, exhibited longer usage windows, at higher biomass-normalized rates, and later in the growth curve. Contrary to hypotheses based on previous studies, we found no clear relationship between substrate nominal oxidation state of carbon (NOSC) or maximal growth rate and the order of substrate depletion. Under soil solution conditions, the growth of Paraburkholderia sp. 1N induced multiauxic substrate depletion patterns that could not be explained by the traditional paradigm of catabolite repression. IMPORTANCE Exometabolomic footprinting methods have the capability to provide time-resolved observations of the uptake and release of hundreds of compounds during microbial growth. Of particular interest is microbial phenotyping under environmentally relevant soil conditions, consisting of relatively low concentrations and modeling pulse input events. Here, we show that growth of a bacterial soil isolate, Paraburkholderia sp. 1N, on a dilute soil extract resulted in a multiauxic metabolic response, characterized by discrete temporal clusters of substrate depletion and metabolite production. Our data did not support the hypothesis that compounds with lower energy content are used preferentially, as each cluster contained compounds with a range of nominal oxidation states of carbon. These new findings with Paraburkholderia sp. 1N, which belongs to a metabolically diverse genus, provide insights on ecological strategies employed by aerobic heterotrophs competing for low-molecular-weight substrates in soil solution.


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