Increasing microbial carbon use efficiency with nitrogen addition resulting from plant-mineral interaction

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>

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.


2020 ◽  
Author(s):  
Johannes Rousk

<p>During the decomposition of organic matter (OM), microorganisms use the assimilated carbon (C) for biomass production or respiration, and the fraction of growth to total assimilation defines the microbial carbon-use efficiency (CUE). Therefore, microbial CUEs have direct consequences for the balance of C between atmosphere and soil, and is as such a central parameter to represent the global C cycle well in Global Cycling Models (GCMs). Despite its enormous leverage this factor remains critically underexplored. Based on the physiology of cultured microorganisms, it is anticipated that (H1) high nutrient availabilities will increase microbial CUE, (H2) that higher quality substrate will increase microbial CUE, (H3) that microbial communities more dominated by fungi will have higher CUE, and (H4) that microbial CUE will decrease in response to environmental stress. We combined extensive field surveys with experimental treatments in microcosms to assess our hypotheses. We sampled temperate forest soils, temperate agricultural soils, and subarctic forest soils, encompassing a wide range of soil pHs (4.0-7.1), nutrient availabilities (10<soil C/N<33), and soil OM qualities (7-fold differences in respiration per SOM). We also surveyed environmental pollution gradients where metallurgy had contaminated soil with high heavy metal concentrations in boreal forest and temperate grassland sites. We also subjected selected soils to microcosm experiments where soil pH (liming), mineral N (50 kg N ha<sup>-1</sup>), OM quality (plant litter), or heavy metal stress were manipulated and the resulting bacterial and fungal growth, respiration, and CUE were monitored over the course of 2 months.</p><p> </p><p>Fungal-to-bacterial growth ratios (F:B) ranged from 0.02 to 0.44 across the studied ecosystems, and that the fungal dominance was higher in soils with lower C:N ratio and higher C-quality. CUE ranged from 0.03 to 0.30, and values clustered most strongly according to site rather than level of soil N. CUE was higher in soil with high C:N ratios and high C-qualities. However, within each land-use type, a high mineral N-content did result in lower F:B and higher resulting CUE. In the microcosm experiments, plant litter addition stimulated the growth of fungi more than bacteria, while increasing soil pH stimulated bacteria more than fungi. Mineral N additions inhibited bacterial growth and stimulated fungal growth. This resulted in microbial CUE estimates in real time that ranged from ca 0.05 to 0.55, and where increased pH and litter increased values while mineral N supplements decreased values. Long-term exposure to heavy metals decreased microbial CUE, but only marginally, even at very high rates of metal exposure. Short-term exposure to metal stimulated microbial CUE in soil from contaminated sites, while CUE was reduced in soil with no history of metal contamination. In conclusion, a higher site soil C-quality coincided with lower F:B and higher CUE across the surveyed sites, while a higher N availability did not. A higher site N availability resulted in higher CUE and lower F:B within each site, while mineral N supplements in the microcosm induced the opposite response, suggesting that site-specific differences associated with fertility such as the effect of plant communities, overrode the influence of mineral N-availability.</p>


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>


2018 ◽  
Vol 123 ◽  
pp. 64-73 ◽  
Author(s):  
Marie Sauvadet ◽  
Gwenaëlle Lashermes ◽  
Gonzague Alavoine ◽  
Sylvie Recous ◽  
Matthieu Chauvat ◽  
...  

mBio ◽  
2020 ◽  
Vol 11 (1) ◽  
Author(s):  
Grace Pold ◽  
Luiz A. Domeignoz-Horta ◽  
Eric W. Morrison ◽  
Serita D. Frey ◽  
Seeta A. Sistla ◽  
...  

ABSTRACT The strategy that microbial decomposers take with respect to using substrate for growth versus maintenance is one essential biological determinant of the propensity of carbon to remain in soil. To quantify the environmental sensitivity of this key physiological trade-off, we characterized the carbon use efficiency (CUE) of 23 soil bacterial isolates across seven phyla at three temperatures and with up to four substrates. Temperature altered CUE in both an isolate-specific manner and a substrate-specific manner. We searched for genes correlated with the temperature sensitivity of CUE on glucose and deemed those functional genes which were similarly correlated with CUE on other substrates to be validated as markers of CUE. Ultimately, we did not identify any such robust functional gene markers of CUE or its temperature sensitivity. However, we found a positive correlation between rRNA operon copy number and CUE, opposite what was expected. We also found that inefficient taxa increased their CUE with temperature, while those with high CUE showed a decrease in CUE with temperature. Together, our results indicate that CUE is a flexible parameter within bacterial taxa and that the temperature sensitivity of CUE is better explained by observed physiology than by genomic composition across diverse taxa. We conclude that the bacterial CUE response to temperature and substrate is more variable than previously thought. IMPORTANCE Soil microbes respond to environmental change by altering how they allocate carbon to growth versus respiration—or carbon use efficiency (CUE). Ecosystem and Earth System models, used to project how global soil C stocks will continue to respond to the climate crisis, often assume that microbes respond homogeneously to changes in the environment. In this study, we quantified how CUE varies with changes in temperature and substrate quality in soil bacteria and evaluated why CUE characteristics may differ between bacterial isolates and in response to altered growth conditions. We found that bacterial taxa capable of rapid growth were more efficient than those limited to slow growth and that taxa with high CUE were more likely to become less efficient at higher temperatures than those that were less efficient to begin with. Together, our results support the idea that the CUE temperature response is constrained by both growth rate and CUE and that this partly explains how bacteria acclimate to a warming world.


2020 ◽  
Author(s):  
Thomas P. Smith ◽  
Tom Clegg ◽  
Thomas Bell ◽  
Samrāt Pawar

Understanding the temperature dependence of carbon use efficiency (CUE) is critical for understanding microbial physiology, population dynamics, and community-level responses to changing environmental temperatures 1,2. Currently, microbial CUE is widely assumed to decrease with temperature 3,4. However, this assumption is based largely on community-level data, which are influenced by many confounding factors 5, with little empirical evidence at the level of individual strains. Here, we experimentally characterise the CUE thermal response for a diverse set of environmental bacterial isolates. We find that contrary to current thinking, bacterial CUE typically responds either positively to temperature, or has no discernible temperature response, within biologically meaningful temperature ranges. Using a global data-synthesis, we show that our empirical results are generalisable across a much wider diversity of bacteria than have previously been tested. This systematic variation in the thermal responses of bacterial CUE stems from the fact that relative to respiration rates, bacterial population growth rates typically respond more strongly to temperature, and are also subject to weaker evolutionary constraints. Our results provide fundamental new insights into microbial physiology, and a basis for more accurately modelling the effects of shorter-term thermal fluctuations as well as longer-term climatic warming on microbial communities.


2019 ◽  
Vol 16 (14) ◽  
pp. 2891-2904
Author(s):  
Tianpeng Li ◽  
Heyong Liu ◽  
Ruzhen Wang ◽  
Xiao-Tao Lü ◽  
Junjie Yang ◽  
...  

Abstract. Sulfur (S) availability plays a vital role in driving functions of terrestrial ecosystems, which can be largely affected by soil inorganic S fractions and pool size. Enhanced nitrogen (N) input can significantly affect soil S availability, but it still remains largely unknown if the N effect varies with frequency of N addition and mowing management in grasslands. To investigate changes in the soil S pool and inorganic S fractions (soluble S, adsorbed S, available S, and insoluble S), we conducted a field experiment with different frequencies (two times per year vs. monthly additions per year) and intensities (i.e., 0, 1, 2, 3, 5, 10, 15, 20, and 50 g N m−2 yr−1) of NH4NO3 addition and mowing (unmown vs. mown) over 6 years in a temperate grassland of northern China. Generally, N addition frequency, N intensity, and mowing significantly interacted with each other to affect most of the inorganic S fractions. Specifically, a significant increase in soluble S was only found at high N frequency with the increasing intensity of N addition. Increasing N addition intensity enhanced adsorbed S and available S concentrations at low N frequency in unmown plots; however, both fractions were significantly increased with N intensity at both N frequencies in mown plots. The high frequency of N addition increased the concentrations of adsorbed S and available S in comparison to the low frequency of N addition only in mown plots. Changes in soil S fractions were mainly related to soil pH, N availability, soil organic carbon (SOC), and plant S uptake. Our results suggested that N input could temporarily replenish soil-available S by promoting dissolution of soil-insoluble S with decreasing soil pH and mineralization of organic S due to increasing plant S uptake. However, the significant decrease in organic S and total S concentrations with N addition intensity in mown plots indicated that N addition together with biomass removal would eventually cause soil S depletion in this temperate grassland in the long term. Our results further indicated that using large and infrequent N additions to simulate N deposition can overestimate the main effects of N deposition and mowing management on soil S availability in semiarid grasslands.


2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Zhi Chen ◽  
Guirui Yu

AbstractCarbon use efficiency (CUE), one of the most important eco-physiological parameters, represents the capacity of plants to transform carbon into new biomass. Understanding the variations and controls of CUE is crucial for regional carbon assessment. Here, we used 15-years of continuous remote sensing data to examine the variations of CUE across broad geographic and climatic gradients in China. The results showed that the vegetation CUE was averaged to 0.54 ± 0.11 with minor interannual variation. However, the CUE greatly varied with geographic gradients and ecosystem types. Forests have a lower CUE than grasslands and croplands. Evergreen needleleaf forests have a higher CUE than other forest types. Climate factors (mean annual temperature (MAT), precipitation (MAP) and the index of water availability (IWA)) dominantly regulated the spatial variations of CUE. The CUE exhibited a linear decrease with enhanced MAT and MAP and a parabolic response to the IWA. Furthermore, the responses of CUE to environmental change varied with individual ecosystem type. In contrast, precipitation exerted strong control on CUE in grassland, while in forest and cropland, the CUE was mainly controlled by the available water. This study identifies the variations and response of CUE to environmental drivers in China, which will be valuable for the regional assessment of carbon cycling dynamics under future climate change.


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