Carbon Use Efficiency and Its Temperature Sensitivity Covary in Soil Bacteria

Abstract

The strategy that microbial decomposers take with respect to using substrate for growth versus maintenance is one essential biological determinant of the propensity of carbon to remain in soil. To quantify the environmental sensitivity of this key physiological trade-off, we characterized the carbon use efficiency (CUE) of 23 soil bacterial isolates across seven phyla at three temperatures and with up to four substrates. Temperature altered CUE in both an isolate-specific manner and a substrate-specific manner. We searched for genes correlated with the temperature sensitivity of CUE on glucose and deemed those functional genes which were similarly correlated with CUE on other substrates to be validated as markers of CUE. Ultimately, we did not identify any such robust functional gene markers of CUE or its temperature sensitivity. However, we found a positive correlation between rRNA operon copy number and CUE, opposite what was expected. We also found that inefficient taxa increased their CUE with temperature, while those with high CUE showed a decrease in CUE with temperature. Together, our results indicate that CUE is a flexible parameter within bacterial taxa and that the temperature sensitivity of CUE is better explained by observed physiology than by genomic composition across diverse taxa. We conclude that the bacterial CUE response to temperature and substrate is more variable than previously thought. IMPORTANCE Soil microbes respond to environmental change by altering how they allocate carbon to growth versus respiration—or carbon use efficiency (CUE). Ecosystem and Earth System models, used to project how global soil C stocks will continue to respond to the climate crisis, often assume that microbes respond homogeneously to changes in the environment. In this study, we quantified how CUE varies with changes in temperature and substrate quality in soil bacteria and evaluated why CUE characteristics may differ between bacterial isolates and in response to altered growth conditions. We found that bacterial taxa capable of rapid growth were more efficient than those limited to slow growth and that taxa with high CUE were more likely to become less efficient at higher temperatures than those that were less efficient to begin with. Together, our results support the idea that the CUE temperature response is constrained by both growth rate and CUE and that this partly explains how bacteria acclimate to a warming world.

Systematic variation in the temperature dependence of bacterial carbon use efficiency

“…Furthermore, Pold et al 13 show that the Q 10 of CUE is higher for more efficient taxa which is analogous to our result of a negative relationship between E CUE and maximum CUE. We find that this trade-off is well described as a linear relationship, with highly negative E CUE values not being found, suggesting a potential biological limit.…”

Microbial diversity drives carbon use efficiency in a model soil

“…This was confirmed by a break point analysis which showed a threshold at a PD value of 4.48 after which only high CUE values were observed ( t = 4.51, df = 86, R 2 = 0.28, P < 0.001). By contrast, the lower diversity samples showed the full range of CUE values suggesting that other factors such as community composition 22 and environmental factors are important in determining community CUE. While we report a positive relationship between diversity and CUE, other studies have evaluated the relationship between respiration and diversity, and found it to be positive 8 , 44 , neutral 44 , 45 , or negative 46 .…”

“…This decrease in CUE for communities incubated at higher temperature was associated with an increase in estimated rrN copy number (Supplementary Fig. 12 ), a high rrN copy number has been related to a lower growth efficiency 53 , although this has not always been observed 22 . Moisture treatment showed no significant impact on either CUE ( t = −1.81, df = 161, P = 0.070) or rrN (Supplementary Fig.…”

“…Generally, elevated temperatures increase respiration more than growth, and therefore CUE tends to decrease with increasing temperature 18 . However, this decrease in CUE with temperature is not ubiquitous 22 , and has been observed to vary with substrate quality 20 . Our knowledge of the impact of soil water content specifically on CUE is limited to two studies 19 , 23 .…”

“…Moreover, community composition, rather than richness, can have a large impact on C cycling in soils 32 , 36 . CUE is known to differ between bacterial strains grown under identical conditions 22 . This suggests that communities with distinct members could have different community CUE.…”