Deuterium stable isotope probing of fatty acids reveals climate change effects on soil microbial physiology.

2021 ◽  
Author(s):  
Alberto Canarini ◽  
Lucia Fuchslueger ◽  
Jörg Schnecker ◽  
Margarete Watzka ◽  
Erich M. Pötsch ◽  
...  
Keyword(s):  
Climate Change ◽  
Fatty Acids ◽  
Water Vapor ◽  
Soil Water ◽  
Growth Rates ◽  
Microbial Growth ◽  
Community Level ◽  
Microbial Physiology ◽  
Carbon Use Efficiency ◽  
Use Efficiency

<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>

scholarly journals Microbial growth and carbon use efficiency show seasonal responses in a multifactorial climate change experiment

2020 ◽  
Vol 3 (1) ◽  
Author(s):  
Eva Simon ◽  
Alberto Canarini ◽  
Victoria Martin ◽  
Joana Séneca ◽  
Theresa Böckle ◽  
...  
Keyword(s):  
Climate Change ◽  
Microbial Growth ◽  
Future Research ◽  
Global Changes ◽  
Summer Drought ◽  
Microbial Physiology ◽  
Soil Microbial ◽  
Carbon Use Efficiency ◽  
Use Efficiency ◽  
Climate Change Drivers

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.

Quantifying microbial growth and carbon use efficiency in dry soil environments via 18O water vapor equilibration

2020 ◽  
Author(s):  
Alberto Canarini ◽  
Wolfgang Wanek ◽  
Margarete Watzka ◽  
Taru Sandén ◽  
Heide Spiegel ◽  
...  
Keyword(s):  
Water Vapor ◽  
Microbial Growth ◽  
Water Holding Capacity ◽  
New Method ◽  
Water Addition ◽  
Microbial Physiology ◽  
Carbon Use Efficiency ◽  
Wide Range ◽  
Use Efficiency ◽  
Water Holding

<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>

scholarly journals Systematic variation in the temperature dependence of bacterial carbon use efficiency

2020 ◽  
Author(s):  
Thomas P. Smith ◽  
Tom Clegg ◽  
Thomas Bell ◽  
Samrāt Pawar
Keyword(s):  
Temperature Dependence ◽  
Temperature Response ◽  
Thermal Response ◽  
Thermal Fluctuations ◽  
Community Level ◽  
Systematic Variation ◽  
Microbial Physiology ◽  
Population Growth Rates ◽  
Carbon Use Efficiency ◽  
Use Efficiency

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.

scholarly journals Quantifying microbial growth and carbon use efficiency in dry soil environments via 18 O water vapor equilibration

2020 ◽  
Vol 26 (9) ◽  
pp. 5333-5341 ◽  
Author(s):  
Alberto Canarini ◽  
Wolfgang Wanek ◽  
Margarete Watzka ◽  
Taru Sandén ◽  
Heide Spiegel ◽  
...  
Keyword(s):  
Water Vapor ◽  
Microbial Growth ◽  
Carbon Use Efficiency ◽  
Use Efficiency ◽  
Dry Soil

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

2021 ◽  
Author(s):  
Xuehui Feng ◽  
Jie Hu ◽  
Yuanhe Yang ◽  
Leiyi Chen
Keyword(s):  
Microbial Growth ◽  
Global Environmental Change ◽  
Terrestrial Ecosystems ◽  
Metabolic Parameter ◽  
N Availability ◽  
Microbial Physiology ◽  
Soil C ◽  
Carbon Use Efficiency ◽  
N Input ◽  
Use Efficiency

<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>

Warming affects seasonal dynamics of microorganisms and reduces the N storage capacity of soil microbes in winter

2021 ◽  
Author(s):  
Philipp Gündler ◽  
Alberto Canarini ◽  
Sara Marañón Jiménez ◽  
Gunnhildur Gunnarsdóttir ◽  
Páll Sigurðsson ◽  
...  
Keyword(s):  
Microbial Biomass ◽  
Growth Rates ◽  
Seasonal Dynamics ◽  
Soil Microbes ◽  
Storage Capacity ◽  
Ambient Conditions ◽  
Soil Warming ◽  
Carbon Use Efficiency ◽  
Use Efficiency ◽  
C And N

<p>Seasonality of soil microorganisms plays a critical role in terrestrial carbon (C) and nitrogen (N) cycling. The asynchrony of immobilization by microbes and uptake by plants may be important for N retention during winter, when plants are inactive. Meanwhile, the known warming effects on soil microbes (decreasing biomass and increasing growth rates) may affect microbial seasonal dynamics and nutrient retention during winter.</p><p>We sampled soils from a geothermal warming site in Iceland (www.forhot.is) which includes three in situ warming levels (ambient, +3 °C, +6 °C). We harvested soil samples at 9 time points over one year and measured the seasonal variation in microbial biomass carbon (Cmic) and nitrogen (Nmic) and microbial physiology (growth and carbon use efficiency) by an <sup>18</sup>O-labelling technique.</p><p>We observed that Cmic and Nmic peaked in winter, followed by a decline in spring and summer. In contrast growth and respiration rates were higher in summer than winter. The observed biomass peak at lower growth rates, suggests that microbial death rates must have declined even more than growth rates. Soil warming increased biomass-specific microbial activity (i.e., growth, respiration, and turnover rates per unit of microbial biomass), prolonging the period of higher microbial activity found in summer into autumn and winter. Microbial carbon use efficiency was unaltered by soil warming. Throughout the seasons, warming reduced Cmic and Nmic, albeit with a stronger effect in winter than summer and restrained winter biomass accumulation by up to 78% compared to ambient conditions. We estimated a reduced microbial winter N storage capacity by 45.5 and 94.6 kg ha<sup>-1</sup> at +3 °C and +6 °C warming respectively compared to ambient conditions. This reduction represents 1.57% and 3.26% of total soil N stocks, that could potentially be lost per year from these soils.</p><p>Our results clearly demonstrate that soil warming strongly decreases microbial C and N immobilization when plants are inactive, potentially leading to higher losses of C and N from warmed soils over winter. These results have important implications as increased N losses may restrict increased plant growth in a future climate.</p>

New insights on carbon use efficiency using calorespirometry – a bioenergetics-based model

2020 ◽  
Author(s):  
Arjun Chakrawal ◽  
Anke M. Herrmann ◽  
Stefano Manzoni
Keyword(s):  
Metabolic Pathways ◽  
Microbial Growth ◽  
Energy Content ◽  
Growth Yields ◽  
Balance Model ◽  
Organic C ◽  
Degree Of Reduction ◽  
Carbon Use Efficiency ◽  
Use Efficiency

<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>

How relevant are microbial traits to understand soil biogeochemical cycles? 

2021 ◽  
Author(s):  
Tessa Camenzind ◽  
Johannes Lehmann ◽  
Anika Lehmann ◽  
Carlos A. Aguilar-Trigueros ◽  
Matthias C. Rillig
Keyword(s):  
Enzymatic Activity ◽  
Fungal Growth ◽  
Biogeochemical Cycles ◽  
Model Organisms ◽  
Soil System ◽  
Microbial Physiology ◽  
Carbon Use Efficiency ◽  
N Supply ◽  
Use Efficiency

<p>Our knowledge about the role of microbial organisms as drivers of soil biogeochemical cycles is mainly based on soil analyses, and the physiological information that exists for few microbial model organisms. In soil, measurements of process rates and element contents can be related to the apparent activity of the microbial community, though conclusions are often indirect - actual microbial physiology and diversity remains hidden. By contrast, analyses of microbial physiology under controlled conditions are hardly representative of the vast diversity of microorganisms in soil, and a transfer of these findings to complex soil systems is challenging. Thus, we argue that a better exchange among these ecological disciplines will lead to a valuable transfer of relevant questions, knowledge and improved understanding of the role of microbes in soil and its responses to environmental change. <br>Here, we provide examples of an evaluation of microbial parameters relevant in soil biogeochemical cycles, analysing traits in a collection of 31 saprobic fungi in response to varying substrate conditions. The large dataset allowed to test several assumptions and conclusions derived from soil system analyses exemplarily for soil fungi. Specifically, we (1) evaluated the optimum C:N:P (carbon:nitrogen:phosphorus) substrate ratio for fungal growth and activity, (2) assessed the responses in carbon-use efficiency and enzyme activity to N deficiency, (3) analyzed the relevance of C versus N supply for fungal growth and activity under varying substrate conditions and (4) tested the assumption of microbial stoichiometric homeostasis, that represents a basic principle in soil ecological stoichiometry. <br>Fungal responses to changes in N and C availability were partly consistent with expectations, e.g. regarding general nutrient demands, though as often discussed C availability appeared more relevant for growth especially in complex substrates. Enzymatic activity and respiration also positively correlated with N availability, resulting in decreased carbon-use efficiency at high N supply. These findings, for example, contradict certain conclusions in soil analyses, namely that N limitations will result in “N mining” (high enzymatic activity), while the excess of C causes “overflow respiration” and reduced CUE. Regarding fungal C:N:P ratios, those were only related to nutrient demands when growing in simple media, while in soil substrate such relations seem more complex. Contradicting the assumption of microbial homeostasis in soil, fungal individuals showed more flexible C:N:P ratios than expected, though the degree of flexibility varied among isolates. In general, the results also reveal a large trait variation among different isolates, with several traits showing a phylogenetic signal, indicating variations in microbial activity depending on community composition.<br>Finally, we want to raise and discuss several emerging questions: How relevant is a deeper understanding of microbial physiology to understand soil biogeochemical processes? How do we include the variability of traits in diverse soil communities – are average values informative, or can we proceed with useful categories? And how can methods in soil science and microbial ecology be merged best to allow fruitful knowledge transfer?</p>

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