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 ◽  
...  

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):  
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>


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>


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 ◽  
Author(s):  
Noah Sokol ◽  
Steve Blazewicz ◽  
Megan Foley ◽  
Alex Greenlon ◽  
Jennifer Pett-Ridge

<p>Carbon use efficiency (CUE) is theorized to be positively associated with the formation of microbially-derived, mineral-associated soil carbon.  Yet few empirical studies have directly tested this relationship. Moreover, it is unclear: (1) how differences between distinct soil microbial communities (for example, differences in competitive interactions and/or growth rate among rhizosphere, detritusphere, and bulk soil communities) may yield different relationships between carbon-use efficiency and soil carbon formation, and (2) how microbial ecophysiology – such as physiological changes induced by drought – may modulate the strength and/or direction of the CUE-soil carbon relationship.</p><p>To investigate these questions, we conducted a 12-week <sup>13</sup>C tracer study to track the movement of two dominant sources of plant carbon – rhizodeposition and root detritus – into soil microbial communities and carbon pools under normal moisture vs drought conditions. Using a continuous <sup>13</sup>CO<sub>2</sub>-labeling system, we grew the Mediterranean annual grass <em>Avena barbata</em> in controlled growth chambers and measured the formation of organic matter from <sup>13</sup>C-enriched rhizodeposition. As the plants grew, we harvested rhizosphere and bulk soil at three time points (4, 8, and 12 weeks) to capture changes in soil carbon pools and microbial community dynamics. In parallel microcosms, we tracked the formation of soil carbon derived from <sup>13</sup>C-enriched <em>A. barbata</em> root detritus during 12 weeks of decomposition; harvesting detritusphere and bulk soil at 4,8, and 12 weeks. In all microcosms, we manipulated soil moisture to generate drought (7.8 ± 2.1 % soil moisture) and ‘normal moisture’ (15.1 ± 4.2 % soil moisture) treatments.</p><p>In all samples (over 150 observations), we measured CUE via the <sup>18</sup>O-H<sub>2</sub>O method, and quantified the formation of different <sup>13</sup>C-soil organic carbon pools via density fractionation. Here we will present data on how soil moisture influences CUE in rhizosphere, detritusphere, and bulk soil communities, and whether differences in CUE are correlated with the formation of mineral-associated soil organic carbon. These results will help to illustrate whether CUE acts as a lynchpin variable with predictive power for stable soil carbon formation, or whether other microbial traits may require consideration.</p><p> </p><p> </p>


Elem Sci Anth ◽  
2020 ◽  
Vol 8 (1) ◽  
Author(s):  
Grace Pold ◽  
Luiz A. Domeignoz-Horta ◽  
Kristen M. DeAngelis

Soils store more carbon than the biosphere and atmosphere combined, and the efficiency to which soil microorganisms allocate carbon to growth rather than respiration is increasingly considered a proxy for the soil capacity to store carbon. This carbon use efficiency (CUE) is measured via different methods, and more recently, the 18O-H2O method has been embraced as a significant improvement for measuring CUE of soil microbial communities. Based on extrapolating 18O incorporation into DNA to new biomass, this measurement makes various implicit assumptions about the microbial community at hand. Here we conducted a literature review to evaluate how viable these assumptions are and then developed a mathematical model to test how violating them affects estimates of the growth component of CUE in soil. We applied this model to previously collected data from two kinds of soil microbial communities. By changing one parameter at a time, we confirmed our previous observation that CUE was reduced by fungal removal. Our results also show that depending on the microbial community composition, there can be substantial discrepancies between estimated and true microbial growth. Of the numerous implicit assumptions that might be violated, not accounting for the contribution of sources of oxygen other than extracellular water to DNA leads to a consistent underestimation of CUE. We present a framework that allows researchers to evaluate how their experimental conditions may influence their 18O-H2O-based CUE measurements and suggest the parameters that need further constraining to more accurately quantify growth and CUE.


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.


2022 ◽  
Author(s):  
Paul Dijkstra ◽  
Weichao Wu ◽  
Michaela Dippold ◽  
Egbert Schwartz ◽  
Bruce Hungate ◽  
...  

Abstract Biochemistry is an essential yet often undervalued aspect of soil ecology, especially in soil C cycling. We assume based on tradition, intuition or hope that the complexity of biochemistry is confined to the microscopic world, and can be ignored when dealing with whole soil systems. This opinion paper draws attention to patterns caused by basic biochemical processes that permeate the world of ecosystem processes. From these patterns, we can estimate activities of the biochemical reactions of the central C metabolic network and gain insights into the ecophysiology of microbial biosynthesis and growth and maintenance energy requirements; important components of Carbon Use Efficiency (CUE).The biochemical pathways used to metabolize glucose vary from soil to soil, with mostly glycolysis in some soils, and pentose phosphate or Entner-Doudoroff pathways in others. However, notwithstanding this metabolic diversity, glucose use efficiency is high and thus substrate use for maintenance energy and overflow respiration is low in these three soils. These results contradict current dogma based on four decades of research in soil ecology. We identify three main shortcomings in our current understanding of substrate use efficiency: 1) in numeric and conceptual models, we lack appreciation of the strategies that microbes employ to quickly reduce energy needs in response to starvation; 2) production of exudates and microbial turnover affect whole-soil CUE more than variation in maintenance energy demand; and 3) whether tracer experiments can be used to measure the long-term substrate use efficiency of soil microbial communities depends critically on the ability of non-growing cells to take up tracer substrates, how biosynthesis responds to these substrates, as well as on how cellular activities scale to the community level.To move the field of soil ecology forward, future research must consider the details of microbial ecophysiology and develop new tools that enable direct measurement of microbial functioning in intact soils. We submit that 13C metabolic flux analysis is one of those new tools.


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