Does warming erode network stability and ecosystem multifunctionality?

Environmental warming is thought to alter food web stability and functioning, but whether warming reduces food web resistance and resilience to further climatic events remains surprisingly unexplored. Warming experiments that superimpose acute disturbances are urgently needed to understand how extreme events further threaten the stability and multifunctionality of ecological networks.

Thermal adaptation of soil microbial growth traits in response to chronic warming.

IMPORTANCE: Soils are the largest terrestrial carbon sink and the foundation of our food, fiber, and fuel systems. Healthy soils are carbon sinks, storing more carbon than they release. This reduces the amount of carbon dioxide released into the atmosphere and buffers against climate change. Soil microbes drive biogeochemical cycling and contribute to soil health through organic matter breakdown, plant growth promotion, and nutrient distribution. In this study, we determined how soil microbial growth traits respond to long-term soil warming. We found that bacterial isolates from warmed plots showed evidence of adaptation of optimum growth temperature. This suggests that increased microbial biomass and growth in a warming world could result in greater carbon storage. As temperatures increase, greater microbial activity may help reduce the soil carbon feedback loop. Our results provide insight on how atmospheric carbon cycling and soil health may respond in a warming world.

Quantifying thermal adaptation of soil microbial respiration.

Quantifying the rate of thermal adaptation of soil microbial respiration is essential in determining potential for carbon cycle feedbacks under a warming climate. Uncertainty surrounding this topic stems in part from persistent methodological issues and difficulties isolating the interacting effects of changes in microbial community responses from changes in soil carbon availability. Here, we constructed a series of temperature response curves of microbial respiration (given unlimited substrate) using soils sampled from around New Zealand, including from a natural geothermal gradient, as a proxy for global warming. We estimated the temperature optima ([Formula: see text]) and inflection point ([Formula: see text]) of each curve and found that adaptation of microbial respiration occurred at a rate of 0.29 °C ± 0.04 1SE for [Formula: see text] and 0.27 °C ± 0.05 1SE for [Formula: see text] per degree of warming. Our results bolster previous findings indicating thermal adaptation is demonstrably offset from warming, and may help quantifying the potential for both limitation and acceleration of soil C losses depending on specific soil temperatures.

Exploring Trait Trade-Offs for Fungal Decomposers in a Southern California Grassland.

Fungi are important decomposers in terrestrial ecosystems, so their responses to climate change might influence carbon (C) and nitrogen (N) dynamics. We investigated whether growth and activity of fungi under drought conditions were structured by trade-offs among traits in 15 fungal isolates from a Mediterranean Southern California grassland. We inoculated fungi onto sterilized litter that was incubated at three moisture levels (4, 27, and 50% water holding capacity, WHC). For each isolate, we characterized traits that described three potential lifestyles within the newly proposed "YAS" framework: growth yield, resource acquisition, and stress tolerance. Specifically, we measured fungal hyphal length per unit litter decomposition for growth yield; the potential activities of the extracellular enzymes cellobiohydrolase (CBH), ß -glucosidase (BG), ß -xylosidase (BX), and N-acetyl- ß - D -glucosaminidase (NAG) for resource acquisition; and ability to grow in drought vs. higher moisture levels for drought stress tolerance. Although, we had hypothesized that evolutionary and physiological trade-offs would elicit negative relationships among traits, we found no supporting evidence for this hypothesis. Across isolates, growth yield, drought stress tolerance, and extracellular enzyme activities were not significantly related to each other. Thus, it is possible that drought-induced shifts in fungal community composition may not necessarily lead to changes in fungal biomass or decomposer ability in this arid grassland.

Phenotypic plasticity of fungal traits in response to moisture and temperature.

Phenotypic plasticity of traits is commonly measured in plants to improve understanding of organismal and ecosystem responses to climate change but is far less studied for microbes. Specifically, decomposer fungi are thought to display high levels of phenotypic plasticity and their functions have important implications for ecosystem dynamics. Assessing the phenotypic plasticity of fungal traits may therefore be important for predicting fungal community response to climate change. Here, we assess the phenotypic plasticity of 15 fungal isolates (12 species) from a Southern California grassland. Fungi were incubated on litter at five moisture levels (ranging from 4-50% water holding capacity) and at five temperatures (ranging from 4-36 °C). After incubation, fungal biomass and activities of four extracellular enzymes (cellobiohydrolase (CBH), ß-glucosidase (BG), ß-xylosidase (BX), and N-acetyl-ß-D-glucosaminidase (NAG)) were measured. We used response surface methodology to determine how fungal phenotypic plasticity differs across the moisture-temperature gradient. We hypothesized that fungal biomass and extracellular enzyme activities would vary with moisture and temperature and that the shape of the response surface would vary between fungal isolates. We further hypothesized that more closely related fungi would show more similar response surfaces across the moisture-temperature gradient. In support of our hypotheses, we found that plasticity differed between fungi along the temperature gradient for fungal biomass and for all the extracellular enzyme activities. Plasticity also differed between fungi along the moisture gradient for BG activity. These differences appear to be caused by variation mainly at the moisture and temperature extremes. We also found that more closely related fungi had more similar extracellular enzymes activities at the highest temperature. Altogether, this evidence suggests that with global warming, fungal biodiversity may become increasingly important as functional traits tend to diverge along phylogenetic lines at higher temperatures.

Embracing a new paradigm for temperature sensitivity of soil microbes.

The temperature sensitivity of soil processes is of major interest, especially in light of climate change. Originally formulated to explain the temperature dependence of chemical reactions, the Arrhenius equation, and related Q10 temperature coefficient, has a long history of application to soil biological processes. However, empirical data indicate that Q10 and Arrhenius model are often poor metrics of temperature sensitivity in soils. In this opinion piece, we aim to (a) review alternative approaches for characterizing temperature sensitivity, focusing on macromolecular rate theory (MMRT); (b) provide strategies and tools for implementing a new temperature sensitivity framework; (c) develop thermal adaptation hypotheses for the MMRT framework; and (d) explore new questions and opportunities stemming from this paradigm shift. Microbial ecologists should consider developing and adopting MMRT as the basis for predicting biological rates as a function of temperature. Improved understanding of temperature sensitivity in soils is particularly pertinent as microbial response to temperature has a large impact on global climate feedbacks.

A meta-analysis of temperature sensitivity as a microbial trait.

Traits-based approaches in microbial ecology provide a valuable way to abstract organismal interaction with the environment and to generate hypotheses about community function. Using macromolecular rate theory (MMRT), we recently identified that temperature sensitivity can be characterized as a distinct microbial trait. As temperature is fundamental in controlling biological reactions, variation in temperature sensitivity across communities, organisms, and processes has the potential to vastly improve understanding of microbial response to climate change. These microbial temperature sensitivity traits include the heat capacity ( ΔCP‡ ), temperature optimum (Topt ), and point of maximum temperature sensitivity (TSmax ), each of which provide unique insights about organismal response to changes in temperature. In this meta-analysis, we analyzed the distribution of these temperature sensitivity traits from bacteria, fungi, and mixed communities across a variety of biological systems (e.g., soils, oceans, foods, wastewater treatment plants) in order to identify commonalities in temperature responses across these diverse organisms and reaction rates. Our analysis of temperature sensitivity traits from over 350 temperature response curves reveals a wide distribution of temperature sensitivity traits, with Topt and TSmax well within biological relevant temperatures. We find that traits vary significantly depending on organism type, microbial diversity, source environment, and biological process, with higher temperature sensitivity found in fungi than bacteria and in less diverse systems. Carbon dioxide production was found to be less temperature sensitive than denitrification, suggesting that changes in temperature will have a potentially larger impact on nitrogen-related processes. As climate changes, these results have important implications for basic understanding of the temperature sensitivity of biological reactions and for ecological understanding of species' trait distributions, as well as for improved treatment of temperature sensitivity in models.

Temperature Sensitivity as a Microbial Trait Using Parameters from Macromolecular Rate Theory.

The activity of soil microbial extracellular enzymes is strongly controlled by temperature, yet the degree to which temperature sensitivity varies by microbe and enzyme type is unclear. Such information would allow soil microbial enzymes to be incorporated in a traits-based framework to improve prediction of ecosystem response to global change. If temperature sensitivity varies for specific soil enzymes, then determining the underlying causes of variation in temperature sensitivity of these enzymes will provide fundamental insights for predicting nutrient dynamics belowground. In this study, we characterized how both microbial taxonomic variation as well as substrate type affects temperature sensitivity. We measured ß-glucosidase, leucine aminopeptidase, and phosphatase activities at six temperatures: 4, 11, 25, 35, 45, and 60°C, for seven different soil microbial isolates. To calculate temperature sensitivity, we employed two models, Arrhenius, which predicts an exponential increase in reaction rate with temperature, and Macromolecular Rate Theory (MMRT), which predicts rate to peak and then decline as temperature increases. We found MMRT provided a more accurate fit and allowed for more nuanced interpretation of temperature sensitivity in all of the enzyme × isolate combinations tested. Our results revealed that both the enzyme type and soil isolate type explain variation in parameters associated with temperature sensitivity. Because we found temperature sensitivity to be an inherent and variable property of an enzyme, we argue that it can be incorporated as a microbial functional trait, but only when using the MMRT definition of temperature sensitivity. We show that the Arrhenius metrics of temperature sensitivity are overly sensitive to test conditions, with activation energy changing depending on the temperature range it was calculated within. Thus, we propose the use of the MMRT definition of temperature sensitivity for accurate interpretation of temperature sensitivity of soil microbial enzymes.