How relevant are microbial traits to understand soil biogeochemical cycles? 

Author(s):  
Tessa Camenzind ◽  
Johannes Lehmann ◽  
Anika Lehmann ◽  
Carlos A. Aguilar-Trigueros ◽  
Matthias C. Rillig

<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>

2005 ◽  
Vol 56 (416) ◽  
pp. 1499-1515 ◽  
Author(s):  
Stephen M. Sieger ◽  
Brian K. Kristensen ◽  
Christine A. Robson ◽  
Sasan Amirsadeghi ◽  
Edward W. Y. Eng ◽  
...  

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.


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 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.


2003 ◽  
Vol 141 (1) ◽  
pp. 17-29 ◽  
Author(s):  
H. KAGE ◽  
C. ALT ◽  
H. STÜTZEL

Based on studies concerning dry matter (DM) partitioning, DM production, root growth, nitrogen (N) contents of cauliflower organs and soil nitrate availability (first part of the paper Kage et al. 2003b), an integrated simulation model for the cauliflower/soil system is constructed, parameterized and evaluated.Dry matter production of cauliflower is described and predicted using a simple light use efficiency (LUE) based approach assuming a linear decrease of light use efficiency with increasing differences between actual, NCAProt, and ‘optimal’, NCAoptProt area based leaf protein concentrations. For 2 experimental years the decline of LUE with decreasing nitrogen concentration was at 0·82 and 0·75 (g DM×m2/(MJ×g N)). Using the parameters obtained from the first experimental year shoot DM production data of cauliflower from five independent experiments with varied N supply containing intermediate harvests could be predicted with a residual mean square error (RMSE) of 72 g/m2 for intermediate harvest DM values ranging from about 50 to 900 g/m2. Nitrogen uptake and partitioning of cauliflower was simulated using functions describing an organ size dependent decline of N content. Leaf nitrate was considered explicitly as a radiation intensity dependent pool, mobilized first under N deficiency. The curd was assumed to have a sink priority for nitrogen. The model predicted shoot N uptake including data of intermediate harvest with a RMSE of 2·4 g/m2 for intermediate harvest N values ranging from about 3 to 30 g/m2. Nitrogen uptake of cauliflower at final harvest was correlated to final leaf number.A scenario simulation was carried out to quantify seasonal variation in N uptake of cauliflower cultivars under unrestricted N availability. Due to variations in the length of the vernalization phase, simulated shoot N uptake ranged from about 260 kg N/ha for spring planted crops to about 290 kg N/ha for summer planted crops of the cultivar ‘Fremont’. The cultivar ‘Linday’, which shows a more severe delay of vernalization under high temperatures, shows on average a larger shoot N uptake for summer planted crops of about 320 kg N/ha and a much larger variation of shoot N uptake.


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):  
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>


2020 ◽  
Author(s):  
Luiz A. Domeignoz-Horta ◽  
Grace Pold ◽  
Xiao-jun A. Liu ◽  
Serita D. Frey ◽  
Jerry M. Melillo ◽  
...  

<div> <div> <div> <p>Empirical evidence for the response of soil carbon cycling to the combined effects of warming, drought and diversity loss is scarce. Microbial carbon use efficiency (CUE) plays a central role in regulating the flow of carbon through soil, yet how biotic and abiotic factors interact to drive it remains unclear. Here, we combined distinct community inocula (biotic factor) with different temperature and moisture conditions (abiotic factors) to manipulate microbial diversity and community structure within a model soil system. Abiotic factors indirectly influenced CUE through their impacts on diversity and community structure, which were the strongest predictors of CUE. We also found that abiotic factors modulated the relationship between diversity and CUE, with CUE being positively correlated with bacterial diversity under high moisture. Altogether these results indicate that drier soils diminished the synergistic effect between diversity and CUE, with potential consequences for the fate of C in soils.</p> </div> </div> </div>


2015 ◽  
Vol 5 (11) ◽  
pp. 960-961 ◽  
Author(s):  
M. Fernández-Martínez ◽  
S. Vicca ◽  
I. A. Janssens ◽  
J. Sardans ◽  
S. Luyssaert ◽  
...  

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