Metabolic rates of prokaryotic microbes may inevitably rise with global warming

Abstract

11Understanding how the metabolic rates of prokaryotes respond to temperature is fun-12 damental to our understanding of how ecosystem functioning will be altered by climate 13 change, as these micro-organisms are major contributors to global carbon efflux. Ecological 14 metabolic theory suggests that species living at higher temperatures evolve higher growth 15 rates than those in cooler niches due to thermodynamic constraints. Here, using a global 16 prokaryotic dataset, we find that maximal growth rate at thermal optimum increases with 17 temperature for mesophiles (temperature optima 45 • C), but not thermophiles ( 45 • C). 18 Furthermore, short-term (within-day) thermal responses of prokaryotic metabolic rates are 19 typically more sensitive to warming than those of eukaryotes. Given that climatic warming 20 will mostly impact ecosystems in the mesophilic temperature range, we conclude that as 21 microbial communities adapt to higher temperatures, their metabolic rates and therefore, 22 carbon efflux, will inevitably rise. Using a mathematical model, we illustrate the potential 23 global impacts of these findings. 24 Introduction 25 A general understanding of how individual organisms respond to changing environmental temperature 26 is necessary for predicting how populations, communities and ecosystems will respond to a changing 27 climate 1,2,3,4 . Because fundamental physiological rates of ectotherms are directly affected by environ-28 1 mental temperature 3,5,6 , climatic warming may be expected to lead to ectotherm communities with 29 higher metabolic rates on average 3,7 . How environmental temperature drives metabolic rates of prokary-30 otes (bacteria and archaea) is of particular importance because they are globally ubiquitous, estimated 31 to comprise up to half of the planet's global biomass 8 , and consume (respire) the majority of net primary 32 production 9,10 . Therefore, climate-driven changes in prokaryotic metabolic rates are expected to signif-33 icantly alter ecosystem productivity, nutrient cycling, and carbon flux 9,10,11,12,13,14 . Indeed, increased 34 carbon efflux has been observed in experimental measures of soil CO 2 loss to warming 15,16 , as well as 35 the responses of other microbial metabolic processes to increased temperature such as methanogenesis 17 . 36However, whether the short-term (timescales of minutes to days) thermal responses of prokaryotes can be 37 compensated by acclimation (physiological phenotypic plasticity) or longer-term (timescales of years or 38 months, years or longer) evolutionary adaptation 18,19,20 is currently unclear. The most recent study to 39 investigate this idea concluded that both short-and long-term responses of ecosystem-level heterotrophic 40 respiration were similar 21 . However, this study quantified short-term responses by aggregating day-level 41 carbon fluxes across sites, and did not have data on the direct respiratory contributions of prokaryotyes 42 per se. 43The short term, or "instantaneous" response of metab...

Adaptive evolution shapes the present-day distribution of the thermal sensitivity of population growth rate

“…24 Early MTE studies argued that, because of strong thermodynamic constraints, 25 adaptation will predominantly result in changes in B 0 , whereas E will remain almost 26 constant across traits (e.g., respiration rate, r max ), species, and environments around a 27 range of 0.6-0.7 eV [6][7][8]. The latter assumption is referred to in the literature as the 28 "universal temperature dependence" (UTD). The limited range of values that E can take 29 is due to the average activation energy of respiration (≈ 0.65 eV), which is suggested to 30 determine the shape of the TPCs of ecological traits.…”

“…This difference in phylogenetic heritability most likely reflects the strength of the positive correlation between B pk and T pk in the two groups. More precisely, T pk , which has a phylogenetic heritability of ≈ 1, is more strongly correlated with B pk among prokaryotes [28] than among phytoplankton [27], possibly due to differences in their cellular physiology. As a result, the phylogenetic heritability of ln(B pk ) in prokaryotes is very close to that of T 2 pk .…”

“…We used four TPC datasets: i) r max across 380 phytoplankton species [27], ii) r max 109 across 272 prokaryote species [28], iii) net photosynthesis rates across 221 species of 110…”

“…Finally, the existence of adaptive variation in thermal 408 sensitivity is likely to partly drive ecological patterns at higher scales (e.g., the response 409 of an ecosystem to warming). How differences in thermal sensitivity among species 410 influence ecosystem function is largely unaddressed [28,61] but highly important for 411 accurately predicting the impacts of climate change on diverse ecosystems.…”

Modeling and Exploiting Microbial Temperature Response

“…Microbiologists have noticed a major effect of temperature on the growth rate of microbial populations and described this effect with the Arrhenius equation by simply replacing the rate constant k in Equation (4) with the growth rate (µ), meaning the reciprocal of the generation time. The so-called Arrhenius plot, where ln(µ) is plotted against the reciprocal temperature, was used in the past and is still applied today to describe a relation between the temperature and growth of different bacteria and molds [23][24][25][26]. From this plot, Arrhenius parameters can easily be derived.…”