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Proc Natl Acad Sci U S A. Jul 3, 2012; 109(27): 10931–10936.
Published online Jun 19, 2012. doi:  10.1073/pnas.1204306109
PMCID: PMC3390866
Ecology, Environmental Sciences

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

Abstract

The pulse of carbon dioxide (CO2) 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 CO2 released in a few days comparable in magnitude to the annual net carbon exchange of many terrestrial ecosystems. Although the origin of this CO2 is debated, we show that the pulse of CO2 is produced by a three-step resuscitation of the indigenous microbial community. Specific phylogenetic groups of microorganisms activate and contribute to the CO2 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.

Keywords: niche partitioning, 16S ribosomal RNA, dormancy, pulsed-activity event, Birch effect

The first rainfalls after dry periods in arid and semiarid ecosystems cause very large and rapidly initiated CO2 pulses (1); rainfall also causes acute water potential changes that are both a severe physiological stress and a defined stimulus for the revival of soil microbial communities rendered inactive by low-water conditions. The source of the CO2 pulse is a hotly debated topic, with proposed contributions from displacement of soil porespace CO2 (2) or microbial metabolism of soil organic carbon originating from photodegradation of plant material over the summer (35), dead microbial biomass (6), microbial intracellular osmolytes (7, 8), or previously inaccessible soil carbon made available for mineralization by soil wet-up (9). No matter what the origin of the organic carbon, the substrate must be decomposed to CO2 by a microbial community emerging from stasis. Here we demonstrate that this CO2 pulse is related to the sequential resuscitation of microorganisms after the severe summer drought.

Extreme summer droughts, with soil water potentials commonly below −20 MPa (6), represent a significant stress to soil microorganisms (10) and are associated with minimal activity (11). The sudden increase in water availability after the first rainfall after a prolonged drought creates an osmotic shock but alleviates the drought-induced stasis. Wet-up–induced changes in microbial processes have been explored over time scales of days to weeks, with prior work focusing on carbon (12, 13) and nitrogen mineralization (1416). The flush of available carbon at wet-up (6) represents a significant nutrient pulse in an environment where microorganisms are often considered to be carbon-limited (17). Thus, wet-up represents both a physiological stress and a defined stimulus for microorganisms recovering from the severe drought of the summer with renewed water and resource availability.

Microorganisms feature a variety of states that permit survival of harsh conditions such as those they experience in the soil environment during a dry Mediterranean summer. Many microbes produce cyst-like cells that are smaller and restructured from vegetative cells (18), whereas Firmicutes and some Actinobacteria produce spores. Although cysts and spores are generally considered dormant states, other physiological responses may also provide a degree of protection from some types of stress. Exopolysaccharide production has been suggested to be a potentially widespread mechanism of protection against desiccation (19) that requires less cell differentiation; meanwhile, the importation or production of compatible solutes allows cellular activity to persist as water potential declines. Although these mechanisms may be important for surviving an extended drought, organisms that have physiologically transitioned into a dormant state must return to an active state at wet-up to compete for resources. The resuscitation process can be responsible for extremely large increases in respiration, as shown during spore germination in Bacillus megaterium (20) and many species of fungi (21). A high degree of gene coordination may be necessary for survival of water potential shock, as well as for entry into and resuscitation from dormant states.

The importance of these CO2 pulses and our general lack of understanding of their origins highlight the following questions. Are particular microorganisms capable of rapid response, and does that allow them to take advantage of the nutrient pulse, thus increasing their abundances? Are there recognizable temporal response strategies of the indigenous bacterial and archaeal communities? Do the response patterns of the soil microbial communities frame the characteristics of the CO2 pulses resulting from wet-up?

To investigate changes in activity of soil bacterial and archaeal communities in response to wet-up, we quantified the relative ribosomal content of taxa over time through extraction of rRNA and analysis using a high-density phylogenetic microarray [PhyloChip (22)]. In all living cells, ribosomes are essential for protein synthesis, may be produced rapidly to increase cellular activity, and can be rapidly recycled when resources are depleted (23, 24). RNA concentration, the bulk of which is rRNA, has been correlated with cell growth rate (25, 26) and with protein synthesis (26) in actively growing cells. Here we explore the patterns of rRNA dynamics within complex soil bacterial and archaeal communities as they emerge from stasis and resume metabolic activity. In this study we investigated the wet-up responses of soil microbial communities from two Mediterranean-type annual grasslands 600 km apart in California. Soil samples were taken at the end of the dry season, when annual plants had been dead for months. These communities both experience severe annual drought, suggesting that the indigenous microorganisms may be adapted to survive and compete during these pulsed-activity events (6). We measured the relative abundances of 16S rRNA molecules from more than 1,700 taxa over eight time points, immediately before and up to 72 h after wet-up. We demonstrate distinct resuscitation strategies that are shared by phylogenetically related microorganisms.

Results

Rapid Environmental Change.

Addition of water to dry soils from a northern California annual grassland (NCA) and a southern California annual grassland (SCA) caused soil water potential to increase rapidly and sharply in both soils, from −38 MPa in NCA and −33 MPa in SCA to −0.006 MPa and −0.03 MPa, respectively (Fig. 1). Site information is given in Table 1. The rate of carbon dioxide production also increased rapidly and sharply in both soils, peaking at approximately 1 h and declining gradually over time (Fig. 1). Although the rates of CO2 production were similar in NCA and SCA at prewet (0.4 and 0.2 μg CO2-C g−1 d−1, respectively) and at 72 h after wet-up (33 and 37 μg CO2-C g−1 d−1, respectively), rates at intermediate time points were higher in NCA than in SCA. The total quantity of bacterial 16S rRNA did not change significantly over time in either soil (Fig. S1); we detected significantly more 16S rRNA in NCA than in SCA.

Fig. 1.
Water potential and rate of carbon dioxide production before and after wet-up in NCA and SCA (n = 5). Open circles, water potential values; bold x’s, rates of CO2 production; P, prewet. Points represented by different letters are significantly ...
Table 1.
Soil characteristics for NCA (Hopland Field Station) and SCA (Sedgwick Reserve)

Detected Taxa.

The communities present as DNA in the two soils were assessed before wet-up and at 72 h by PhyloChip analysis. Before wet-up, the indigenous taxa showed minimal metabolic activity, according to CO2 production rates (Fig. 1). Although the microbial community structure was significantly different between the soils (Fig. S2), there was substantial overlap in their composition, with 95% of the taxa detected in NCA also detected in SCA (Fig. S2).

Most (97%) of the taxa detected by analysis of rRNA (ribosomal community) were also detected by DNA analysis. Although taxa detected in the ribosomal community varied significantly with time, the change over time was primarily driven by taxa dropping below detection [i.e., Preston’s veil line (27)] within 1 h and reemerging at 3 h (Figs. S1 and S3). Although soil origin had a significant impact on the ribosomal community structure, the detected taxa were primarily the same in both soils (97% of detected taxa shared; Fig. S2). Differences in community structure between soils were driven by differences in the relative intensities of the detected taxa; this was the case for both the ribosomal and the DNA communities.

Microbial Response Trajectory.

To evaluate microbial response as a function of time, we filtered taxa to include only those that had a significant change in relative intensity between any two time points after wet-up. Because we monitored relative ribosomal abundance of individual taxa over a short time frame, we refer to changes in relative ribosomal abundance as changes in relative activity (25, 26, 28). Taxa exhibited distinct response trajectories, and hierarchical clustering based on correlations of trajectories (relative intensity patterns) revealed three primary response strategies after wet-up (Fig. 2A). Some taxa displayed their highest relative activity at the outset (between 15 min and 1 h after wet-up), which we refer to as rapid responders; some displayed intermediate temporal response (between 3 h and 24 h), referred to as intermediate responders; still others responded either 24 h or more after wet-up; these we refer to as delayed responders. These taxa and their assigned strategies are represented on a phylogenetically rooted tree (Fig. 2B).

Fig. 2.
(A) Heatmaps and dendrograms displaying the clustering of taxa based on response pattern over time after wetting of dry soil in NCA and SCA. Heatmaps show the trends in average relative activity over time (n = 5) by taxon. Each dendrogram clusters the ...

Significant phylogenetic clustering (net relatedness index; NRI) was found for all strategies in NCA and for intermediate and delayed responders in SCA (Fig. 2B). NRI assesses the phylogenetic clustering of taxa with a given strategy compared with a null model of random distribution over all taxa that were detected by cDNA PhyloChip for a given soil. NRI values represent SDs from the mean (random distribution); hence nonrandom patterns, overdispersion or clustering, are significant when NRI < −1.96 or NRI > 1.96, respectively. Taxa that were detected but not assigned a strategy (strategy = none in Fig. 2B) did not display any discernable patterns. In both soils, Firmicutes were primarily classified as intermediate responders and Spirochaetes as rapid responders. Verrucomicrobia and Actinobacteria were clearly rapid responders in NCA. Strategies were remarkably consistent at the class and order level, except within the Proteobacteria, which varied by class. Deltaproteobacteria and Epsilonproteobacteria were primarily rapid responders. On the other hand, Alphaproteobacteria were consistently delayed responders in both soils. In NCA Betaproteobacteria and Gammaproteobacteria were also delayed responders, but in SCA more taxa from these classes were intermediate responders. A simplified conceptual model of these response strategies is shown in Fig. 3. Not all taxa fit well into our three-strategy model; for instance, many Acidobacteria displayed high relative activity within 1 h of water addition and then again at 72 h. Thus, Acidobacteria were assigned multiple strategies in our groupings, even though they exhibited consistent response trajectories. The numbers of taxa by phylum in the three strategy groups are given in Table S1.

Fig. 3.
Conceptual model showing the trend in relative activity of broad phylogenetic groups over time after wet-up and their relation to water potential and the rate of CO2 production over time. *All taxa had minimal activity prewet as indicated by the rate ...

Ribosomes at Prewet Relate to Strategy.

To evaluate whether relative ribosomal content of taxa before wet-up was related to their subsequent response strategies, we compared the rank order distributions of all taxa deemed present in any replicate (by site) with taxa belonging to each of three strategy groups (rapid, intermediate, and delayed) (Fig. 4). In both soils, rapid responders had significantly more ribosomes relative to the other taxa at prewet than at the post wet-up time points (P < 0.05). Intermediate responders in both soils and delayed responders in SCA, on the other hand, had significantly less relative ribosomal abundance at prewet than at the other time points. Our examination of the number of rRNA operons of taxa in each strategy group showed that in both soils representatives of the intermediate responders had more rRNA operons than the other strategy groups (Fig. S4).

Fig. 4.
Box plots showing the average rank over time of taxa in different strategy groups in NCA and SCA. Higher rank means a higher proportion of cDNA. Strategy groups include always detectable in the ribosomal (cDNA) community (present in at least three out ...

Changes in Abundance.

We detected significant changes in relative abundance (by DNA PhyloChip analysis) in 18% and 14% of taxa in NCA and SCA, respectively, from prewet to 72 h after water addition. Declines in relative abundance were common among taxa of the Acidobacteria, Actinobacteria, Chloroflexi, Planctomycetes, and Verrucomicrobia in both soils (Table S2). On the other hand, taxa of the Betaproteobacteria and Gammaproteobacteria generally increased in relative abundance after wet-up in both soils. However, unlike ribosomal response trajectories, changes in relative abundance varied within many phyla, with responses varying by order and taxon in some cases. For instance, Alphaproteobacteria of the order Sphingomonadales increased in relative abundance, whereas Alphaproteobacteria of the order Bradyrhizobiales declined. Taxa that declined in relative abundance (DNA) were least likely to have been detected in the community detected by rRNA analysis (Table S3).

Discussion

In both soils, water potentials at the end of the summer (−33 and −38 MPa) were below the hydration point for nucleic acids and proteins (10). The rapid water potential change that occurs with wet-up may induce microbial cell lysis or the active efflux of intracellular solutes to avoid cell lysis (6). This flush of microbial biomass carbon has been suggested to be a significant carbon source driving the CO2 pulse observed here and elsewhere after wetting of dry soil (7). After our laboratory wet-up, both soils returned immediately to conditions favorable for microbial metabolism (10). Our identification of three primary resuscitation strategies—rapid, intermediate, and delayed—indicates that taxa within these groups play distinct roles, physiologically, metabolically, and/or ecologically. Although these roles were evidenced during wet-up, they may reflect distinct niches in the ecosystem more generally.

The ability of rapid responders to resuscitate almost immediately after 5 mo of severe desiccation and survive the shock of wet-up may reflect a strategy of preparedness. Rapid responders had relatively more ribosomes at prewet than either intermediate or delayed responders, but rather than increase, they maintained their relative ribosomal abundance soon after wet-up. Actinobacteria, Spirochaetes, and Verrucomicrobia, members of which were generally rapid responders, had relatively more ribosomes per cell than other phyla at prewet (Table S4). A high abundance of ribosomes before and soon after wet-up could allow specific populations to respond to the wet-up event with rapid protein synthesis. On the other hand, one of the main phyla of rapid responders, Actinobacteria, are known for another resuscitation mechanism, resuscitation promoting factors, that allow cells to self-trigger (29). Although these resuscitation-promoting factors seem to be abundant in soils (30), we were unable to detect them using primers that amplify a region of rpf in Micrococcus luteus (29) or rpfD in Mycobacterium tuberculosis (31). In fact several different mechanisms could result in the same general time frame of response; some taxa may achieve rapid response by storing ribosomes, others may invest in cells that are especially resistant to the physiological stress of wet-up, and still others may use resuscitation-promoting factors, all resulting in a rapid response strategy.

Intermediate responders were generally Firmicutes, a phylum well known for their ability to produce a highly resistant endospore. Although the Firmicutes’ strategy of sporulation is well studied, exactly how endospore outgrowth translates into recovery in soil is not well understood. In pure cultures of Bacillus, RNA is synthesized within minutes of spore transfer to favorable conditions (32). We found increased activity of Bacilli from 3 to 24 h after wet-up, a timeframe that would have been sufficient for spore outgrowth. The higher number of rRNA operons of taxa such as Bacilli that were classified as intermediate responders (Fig. S4) may allow them to more rapidly produce ribosomes (33). Conversely, rapid responders, by virtue of their relatively higher ribosomal content before wet-up seem to resuscitate almost immediately. Many of the taxa that increased their relative abundance (as DNA) within the 72-h experiment were classified as delayed responders, among them members of the Sphingomonadales and Xanthamonadales, representatives of which were recently shown to incorporate 18O water into their DNA within 48 h of wet-up (34). It is possible, however, that other taxa may have grown earlier and then been displaced, in a pattern that we did not detect. Thus, slow growers can be rapid responders, whereas fast growers may require more time to recover their metabolic function, potentially reflecting a tradeoff between ability to respond rapidly and ability to grow rapidly.

Resuscitation strategies may reflect niche partitioning based on the types of carbon available over the course of wet-up. The rapidity of the CO2 pulse indicates that the flush of dissolved organic carbon resulting from wet-up is composed primarily of biologically labile organic compounds (6, 12), with some contribution from macromolecular carbon (35). For instance, many Actinobacteria are rapid responders. Although members of the Actinobacteria can consume and compete effectively for simple carbon substrates (36), many Actinobacteria are known to produce extracellular enzymes capable of hydrolyzing complex polymers (37). Extracellular enzymes produced before or early during drought and stabilized by interactions with clay particles and soil organic matter have been suggested to become functional with electrostatic changes (38) that rewetting can provide. As a result, Actinobacteria could access substrate within minutes of wet-up without producing new enzymes. Bacilli resuscitate next; members of the Bacilli are known to produce hydrolytic enzymes (39) that break intermediate-sized polymers into monomers. Thus, timing of recovery may reflect resource use.

The importance of resource pulses to microbial ecology may be especially pronounced in ecosystems that experience regular, extended drought (40). Our results suggest that the speed of resuscitation and dynamism of grassland soil microbial communities after wet-up is greater than those of other microbial communities in response to favorable conditions. For example, in a study of seawater, the addition of peptone (a nutrient-rich protein derivative) to starved communities in water stimulated half of the inactive bacterioplankton cells to become active in 6 h (41). We report that large shifts in active taxa were evident within 1 h of wet-up. Many taxa showed increases in relative ribosomal abundance just 3 h after wet-up, including intermediate and delayed responders; however, intermediate responders ramped up their activity very quickly, peaking approximately 9 h after wet-up, whereas delayed responders required more time to reach peak activity. The fast response observed in our study could be a result of history; soil microorganisms from Mediterranean climates may be adapted to respond rapidly to favorable water conditions to compete for resources and survive in this water pulse-driven ecosystem. Survival of extreme water potential fluctuations, in general, may be more characteristic of soil bacteria than microorganisms from other environments that experience less water potential fluctuation (42).

Changes in relative abundance of rRNA are ultimately a function of regulation, starvation, death, and growth. Because we were unable to detect any significant changes in the total quantity of 16S rRNA, changes in relative abundances were likely caused by increases in the rRNA of some taxa and declines among other taxa. Large early changes (from prewet to 1 h after wet-up) may have been the result of progressive degradation of RNA from cells that lysed as a result of the water potential upshock or that were dead before wet-up and had their RNA preserved by the severely dry soil conditions; this RNA would have been degraded relatively rapidly upon wet-up as water increased the mobility of ribonucleases. Carbon made available by the wet-up could trigger increases in activity or rapid regrowth of some taxa. Because we were unable to detect changes in bacterial abundance by 16S rRNA or microbial biomass (Fig. S5), we conclude that although some taxa died, others grew, resulting in reallocation of resources between microbial response groups rather than an absolute increase in microbial biomass.

Resuscitation of microorganisms after wet-up is responsible for an environmentally important CO2 pulse (43). Our data indicate that different groups of microorganisms likely contributed to the CO2 pulse over time. A simple correlation between total 16S rRNA and rate of CO2 production after wet-up could not be detected, although between sites higher CO2 production was related to higher numbers of 16S rRNA. The relationship between rRNA and activity varies by organism, and some taxa have orders of magnitude more rRNA than others (44, 45); because the active taxa shifted over time, the lack of a simple correlation is not surprising. The CO2 pulse that occurs with wet-up is produced during a progression of microbial resuscitation; the subsets of taxa constituting each resuscitation strategy group represent clades of related organisms. Microorganisms are very diverse, and organisms closely related phylogenetically (as evidenced by 16S rRNA) often have very different ecological traits, ranging from habitat preference to metabolism (46, 47). A range of phylogenetic conservatism, however, does exist for particular ecological traits, such as habitat preference (47). We found phylogenetic clustering of taxa assigned to intermediate and delayed strategies in both soils. Response strategy was generally conserved at the phylum level except among Proteobacteria, which clustered at the class level. Thus, our data demonstrate phylogenetic coherence of ecological strategy by microorganisms in response to soil wet-up.

Although phylogenetic coherence has previously been demonstrated for habitat preference at the class level (48, 49) and genome size at the order level (50), we show that there are phylogenetically coherent pulse–response niches among cohabiting microorganisms. The high degree of phylogenetic coherence may reflect the complexity of survival of and resuscitation from desiccation. Microbial strategies for tolerating desiccation and responding to rapid wet-up likely require coordinated functioning of multiple physiological traits. Such strategies may be the result of long-term evolutionary adaptation. The phylogenetic roots of strategies for desiccation tolerance and resuscitation from desiccation suggest that understanding the controls of a few common pathways might enable more informed prediction of resuscitation response trajectories and help improve estimates of CO2 flux during these significant pulsed events.

Materials and Methods

Experiment.

Soils were collected from a northern and a southern California annual grassland after the summer dry season and shortly before the first rain of the wet season (details in Table 1). Wet-up was initiated within 1 wk of soil collection by adding 10 mL of double-distilled water to 40 g of field-dry soil, approximately equivalent to a 17-mm rainfall event being distributed through the top 5 cm. Soils were destructively sampled at the respective times after water addition. Rates of CO2 production were determined on parallel but identical jars that were sealed. More details are available in SI Materials and Methods.

Analysis.

Nucleic acids were extracted as described in SI Material and Methods. Subsamples of the extracted RNA were reverse-transcribed to single-stranded cDNA for analysis of bacterial 16S rRNA quantification, whereas double-stranded cDNA was synthesized from extracted 16S rRNA transcripts (51) for analysis of relative ribosomal abundance using a high-density 16S rRNA microarray (Affymetrix), known as the G2 PhyloChip (22). Double-stranded cDNA PhyloChips were prepared and filtered as in Brodie et al. (52), with 200 ng of cDNA applied (except for three samples that had less material) and the modifications of DeAngelis et al. (51). We hybridized PCR-amplified DNA to other PhyloChips to assess relative abundance at prewet and 72 h after wet-up. Details are available in SI Materials and Methods.

Supplementary Material

Supporting Information:

Acknowledgments

We thank Donald J. Herman, Dara Goodheart, Steven Blazewicz, Catherine Osborne, Santiago Utsumi, Jeny Lim, and Yvette Piceno for providing expert technical assistance; Perry de Valpine, Dennis Baldocchi, Margaret Torn, Joshua Schimel, and David Ackerly for providing support and valued advice; and two anonymous reviewers whose comments improved the manuscript. Part of this work was completed at Lawrence Berkeley National Laboratory under Contract DE-AC02-05CH11231 with funding from the US Department of Energy (DOE) Program for Ecosystem Research and the Terrestrial Ecosystem Sciences program. Other funding was provided by the Berkeley Atmospheric Sciences Center. S.A.P. was supported in part by a DOE Global Change Education Program Graduate Research Environmental Fellowship and by a James Bennett Fellowship from the Department of Environmental Science, Policy and Management at University of California, Berkeley.

Footnotes

The authors declare no conflict of interest.

This article is a PNAS Direct Submission.

This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1204306109/-/DCSupplemental.

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