Shifting carbon flow from roots into associated microbial communities in response to elevated atmospheric CO2

Abstract

Rising atmospheric CO(2) levels are predicted to have major consequences on carbon cycling and the functioning of terrestrial ecosystems. Increased photosynthetic activity is expected, especially for C-3 plants, thereby influencing vegetation dynamics; however, little is known about the path of fixed carbon into soil-borne communities and resulting feedbacks on ecosystem function. Here, we examine how arbuscular mycorrhizal fungi (AMF) act as a major conduit in the transfer of carbon between plants and soil and how elevated atmospheric CO(2) modulates the belowground translocation pathway of plant-fixed carbon. Shifts in active AMF species under elevated atmospheric CO(2) conditions are coupled to changes within active rhizosphere bacterial and fungal communities. Thus, as opposed to simply increasing the activity of soil-borne microbes through enhanced rhizodeposition, elevated atmospheric CO(2) clearly evokes the emergence of distinct opportunistic plant-associated microbial communities. Analyses involving RNA-based stable isotope probing, neutral/phosphate lipid fatty acids stable isotope probing, community fingerprinting, and real-time PCR allowed us to trace plant-fixed carbon to the affected soil-borne microorganisms. Based on our data, we present a conceptual model in which plant-assimilated carbon is rapidly transferred to AMF, followed by a slower release from AMF to the bacterial and fungal populations well-adapted to the prevailing (myco-)rhizosphere conditions. This model provides a general framework for reappraising carbon-flow paths in soils, facilitating predictions of future interactions between rising atmospheric CO(2) concentrations and terrestrial ecosystems.

Fig. 1.

¹³C enrichment in the AMF signatures 16:1ω5 determined in F. rubra rhizosphere soil for NFLA (circles; A) and PLFA (triangles; B) at ambient CO₂ (blue) and elevated CO₂ (red). The given AMF families, Acaulosporaceae and Glomeraceae, denote the affiliations of the 18S rRNA gene fragments recovered from the ¹³C-labeled RNA fractions by RNA-SIP at ambient CO₂ and elevated CO₂, respectively. Asterisks designate significant differences (P < 0.001) between CO₂ concentrations. The values given are the average of biological replicates, and errors represent the standard error.

Fig. 2.

(A) ¹³C enrichment in the bacterial PLFAs at ambient CO₂ (blue) and elevated CO₂ (red) in the rhizosphere soil of F. rubra (circles) and C. arenaria (triangles). Asterisks (P < 0.001) designate significant differences between CO₂ concentrations. The values given are the average of the different biological replicates, and errors represent the standard error. (B) Significantly different groups in clone libraries derived from F. rubra ¹³C-labeled 16S rRNA at ambient (blue) and elevated (red) CO₂, harvested 21 days after labeling.

Fig. 3.

¹³C enrichment in the rhizosphere of F. rubra at ambient (blue) and elevated CO₂ (red) in the PLFAs of (A) Pseudomonas- and (B) Burkholderia-specific signatures. For C. arenaria, Pseudomonas and Burkholderia showed the highest ¹³C enrichment on day 1 at elevated CO₂ (Fig. S6). The active Pseudomonas and Burkholderia species identified by RNA-SIP, PCR-DGGE, and cloning are indicated along the time course at ambient and elevated CO₂. The species active only at elevated CO₂ are in red. Asterisks (P < 0.001) designate significant differences between CO₂ concentrations. The values given are the average of the different biological replicates, and errors represent the standard error. Points without error bars mean that the error falls within the size of the symbol designating the point.

Fig. 4.

Conceptual model of C flow in mycorrhizal plant–soil systems summarizing the observed effects of elevated CO₂ atmospheric concentrations on soil communities. Brown arrows indicate increases and decreases in the respective community sizes, as determined by real-time PCR and lipid analyses from this study and ref. , as well as changes in community structure and carbon flow. Absence of an arrow indicates no significant change in the community size or structure. Red arrows indicate no effect of increased C availability because of elevated CO₂ on the Actinomycetes spp. and Bacillus spp. communities. The mechanism and magnitude of the C flow along the soil–food web are indicated by the green arrows. Effects on nematodes are based on ref. .