Bacterial carbon use plasticity, phylogenetic diversity and the priming of soil organic matter

Abstract

Microorganisms perform most decomposition on Earth, mediating carbon (C) loss from ecosystems, and thereby influencing climate. Yet, how variation in the identity and composition of microbial communities influences ecosystem C balance is far from clear. Using quantitative stable isotope probing of DNA, we show how individual bacterial taxa influence soil C cycling following the addition of labile C (glucose). Specifically, we show that increased decomposition of soil C in response to added glucose (positive priming) occurs as a phylogenetically diverse group of taxa, accounting for a large proportion of the bacterial community, shift toward additional soil C use for growth. Our findings suggest that many microbial taxa exhibit C use plasticity, as most taxa altered their use of glucose and soil organic matter depending upon environmental conditions. In contrast, bacteria that exhibit other responses to glucose (reduced growth or reliance on glucose for additional growth) clustered strongly by phylogeny. These results suggest that positive priming is likely the prototypical response of bacteria to sustained labile C addition, consistent with the widespread occurrence of the positive priming effect in nature.

Estimating taxon‐specific population dynamics in diverse microbial communities

“…) and that the enigmatic phenomenon of priming—in which pulses of new organic matter enhance the decomposition of older organic matter—is mediated by taxa across the phylogenetic spectrum (Morrissey et al. ).…”

“…Furthermore, the ability to link population dynamics of individual microbial taxa to biogeochemical processes might illuminate whether a handful of hyper-abundant foundation taxa (Ellison et al 2005) drive element fluxes, or whether they are instead regulated by rare keystone taxa (Power et al 1996). Applications of qSIP in this vein have already revealed that microbial activity varies with phylogeny ) and that the enigmatic phenomenon of priming-in which pulses of new organic matter enhance the decomposition of older organic matter-is mediated by taxa across the phylogenetic spectrum (Morrissey et al 2017).…”

Global effects of plant litter alterations on soil CO2 to the atmosphere

“…The increasing priming effect of aboveground litterfall with experimental duration concurs with those from rhizosphere (Huo et al., ). One possible mechanism for this enhancement is that soil microbial community composition changes in concert with its C use (Morrissey et al., ). Microorganisms prefer to use fresh plant litter as a growth substrate at the beginning of fresh C addition, resulting in no or even negative priming effects; however, long‐term C substrate addition would trigger the production of enzymes that are in favour of priming the native soil C (Morrissey et al., ).…”

“…One possible mechanism for this enhancement is that soil microbial community composition changes in concert with its C use (Morrissey et al., ). Microorganisms prefer to use fresh plant litter as a growth substrate at the beginning of fresh C addition, resulting in no or even negative priming effects; however, long‐term C substrate addition would trigger the production of enzymes that are in favour of priming the native soil C (Morrissey et al., ). Alternatively, the initial weak response in priming effect could result from the disturbance of experimental establishment.…”

“…Despite these efforts, it remains a challenge to predict the magnitude and direction of changes in Rs and Q 10 to litter alteration due to the high spatiotemporal variability in Rs responses to litter alteration (Sayer, ; Xu, Liu et al., ). The impact of litter inputs on Rs may be time‐dependent because the priming effect associated with repeated litter addition increased with time due to temporal changes in microbial C use (Morrissey et al., ; Qiao et al., ). The secondary effects of litter removal on Rs, such as soil nutrient depletion for soil microbial activity, may also increase over time as litterfall is the primary pathway for soil nutrient and energy cycling (Sayer, ; Sayer & Tanner, ).…”