Rainfall-induced carbon dioxide pulses result from sequential resuscitation of phylogenetically clustered microbial groups

Abstract

The pulse of carbon dioxide (CO 2 ) resulting from the first rainfall after the dry summer in Mediterranean ecosystems is so large that it is well documented at the landscape scale, with the CO 2 released in a few days comparable in magnitude to the annual net carbon exchange of many terrestrial ecosystems. Although the origin of this CO 2 is debated, we show that the pulse of CO 2 is produced by a three-step resuscitation of the indigenous microbial community. Specific phylogenetic groups of microorganisms activate and contribute to the CO 2 pulse at different times after a simulation of the first rainfall following the severe summer drought. Differential resuscitation was evident within 1 h of wet-up, with three primary response strategies apparent according to patterns of relative ribosomal quantity. Most bacteria could be classified as rapid responders (within 1 h of wet-up), intermediate responders (between 3 and 24 h after wet-up), or delayed responders (24–72 h after wet-up). Relative ribosomal quantities of rapid responders were as high in the prewet dry soils as at any other time, suggesting that specific groups of organisms may be poised to respond to the wet-up event, in that they preserve their capacity to synthesize proteins rapidly. Microbial response patterns displayed phylogenetic clustering and were primarily conserved at the subphylum level, suggesting that resuscitation strategies after wet-up of dry soil may be a phylogenetically conserved ecological trait.

Responses of soil bacterial and fungal communities to extreme desiccation and rewetting

“…On the basis of the rapid (within 2 h) increase in rRNA in bacteria, archaea and fungi, the members of these soil communities appear to be poised for immediate response to rewetting (Placella et al, 2012); this is consistent with the large pulses of CO 2 that result from wetting of dry soil (Borken and Matzner, 2009;Inglima et al, 2009). The extremely dynamic response of the relative potential activity of the different bacterial phyla and classes to rapid changes in water availability that we found would not have been detectable using DNA-based methods, but the combination of rRNA-based with DNA-based molecular analyses has the potential to further unveil the microbial mechanisms that drive the CO 2 pulse upon rewetting dry soils.…”

“…Numerous members of the Gram-positive, high-G þ C content Actinobacteria phylum are drought resistant and have been shown to be able to grow under challenging dry conditions (Goodfellow and Williams, 1983;Zvyagintsev et al, 2007). Nevertheless, the Rubrobacteridae class, which is abundant at our sites as well as in other waterlimited soils, remains poorly characterised (Holmes et al, 2000;Placella et al, 2012). In contrast with the Actinobacteria phylum, the Acidobacteria and Verrucomicrobia phyla do not appear to invest in ribosome accumulation during desiccation, but to rely on extremely rapid ribosomal synthesis upon rewetting.…”

“…Although microbial communities have sometimes been shown to shift seasonally in water-limited systems (Waldrop and Firestone, 2006b;Clark et al, 2009;Cruz-Martinez et al, 2009), the functional or taxonomic groups that drive the microbial response to dry-down and rewetting, their associated strategies and to what extent these responses may be generalised still remain largely unclear (Placella et al, 2012).…”

“…Both soil bacteria and fungi include heterotrophic microorganisms that are capable of rapid activation upon wet-up, that is, of playing a role in the mineralization burst that is responsible for the soil CO 2 efflux pulse following a rewetting event (Fierer and Schimel, 2003;Placella et al, 2012). Although microbial communities have sometimes been shown to shift seasonally in water-limited systems (Waldrop and Firestone, 2006b;Clark et al, 2009;Cruz-Martinez et al, 2009), the functional or taxonomic groups that drive the microbial response to dry-down and rewetting, their associated strategies and to what extent these responses may be generalised still remain largely unclear (Placella et al, 2012).…”

The effect of environmental stressors on respiration activity of afforested mine soils

“…For the mine soils, the CO 2 pulses did not compensate the reduced respiration over dry periods, as their magnitude was much lower. Increased CO 2 evolution upon the rewett ing of dried soils is known as the Birch eff ect and may be caused by the rapid mineralization of C released from dead cells killed by drought [22], release of previously unavailable organic compounds [1], and resuscitation of soil microorganisms that survived the drought period in a dormant state [27]. We presume that the lower CO 2 pulses after consecutive dry-rewet cycles in mine soils and the consequential decrease in cumulative CO 2 release resulted mainly from their lower content of organic matt er (and, as a consequence, lower microbial biomass).…”