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Social dynamics within decomposer communities lead to nitrogen retention and organic matter build-up in soils.

Kaiser C, Franklin O, Richter A, Dieckmann U - Nat Commun (2015)

Bottom Line: The chemical structure of organic matter has been shown to be only marginally important for its decomposability by microorganisms.Moreover, increasing catalytic efficiencies of enzymes are outbalanced by a strong negative feedback on enzyme producers, leading to less enzymes being produced at the community level.Our results thus reveal a possible control mechanism that may buffer soil CO2 emissions in a future climate.

View Article: PubMed Central - PubMed

Affiliation: Evolution and Ecology Program, International Institute for Applied Systems Analysis (IIASA), Schlossplatz 1, A-2361 Laxenburg, Austria.

ABSTRACT
The chemical structure of organic matter has been shown to be only marginally important for its decomposability by microorganisms. The question of why organic matter does accumulate in the face of powerful microbial degraders is thus key for understanding terrestrial carbon and nitrogen cycling. Here we demonstrate, based on an individual-based microbial community model, that social dynamics among microbes producing extracellular enzymes ('decomposers') and microbes exploiting the catalytic activities of others ('cheaters') regulate organic matter turnover. We show that the presence of cheaters increases nitrogen retention and organic matter build-up by downregulating the ratio of extracellular enzymes to total microbial biomass, allowing nitrogen-rich microbial necromass to accumulate. Moreover, increasing catalytic efficiencies of enzymes are outbalanced by a strong negative feedback on enzyme producers, leading to less enzymes being produced at the community level. Our results thus reveal a possible control mechanism that may buffer soil CO2 emissions in a future climate.

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Social dynamics among microbial decomposers affect C and N turnover rates.Effect of microbial cheaters on (a) decay rates, (b) community carbon use efficiency (both time-averaged over model runs until 60% C loss), (c) C in microbial products and (d) N in microbial products (both aggregated over the grid at the point of 60% total C loss). Open circles: no cheaters, that is, all microbes have equal extracellular enzyme production rates of 0.12 (given as fraction of C uptake after deduction of maintenance respiration invested into extracellular enzyme production). Light-red symbols: mixed communities of enzyme producers with production rates of 0.12 and cheaters with enzyme production rates of 0.04 (‘mild', circles), 0.02 (‘strong', squares) or 0 (‘full', triangles), which otherwise have the same traits as enzyme producers. Dark-red triangles: mixed communities of enzyme producers and cheaters with enzyme production rates of 0 with a higher maximum growth rate compared with enzyme producers (Table 1). Error bars indicate model stochasticity by displaying s.d.'s among five independent model runs (error bars smaller than symbol size are not displayed).
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f1: Social dynamics among microbial decomposers affect C and N turnover rates.Effect of microbial cheaters on (a) decay rates, (b) community carbon use efficiency (both time-averaged over model runs until 60% C loss), (c) C in microbial products and (d) N in microbial products (both aggregated over the grid at the point of 60% total C loss). Open circles: no cheaters, that is, all microbes have equal extracellular enzyme production rates of 0.12 (given as fraction of C uptake after deduction of maintenance respiration invested into extracellular enzyme production). Light-red symbols: mixed communities of enzyme producers with production rates of 0.12 and cheaters with enzyme production rates of 0.04 (‘mild', circles), 0.02 (‘strong', squares) or 0 (‘full', triangles), which otherwise have the same traits as enzyme producers. Dark-red triangles: mixed communities of enzyme producers and cheaters with enzyme production rates of 0 with a higher maximum growth rate compared with enzyme producers (Table 1). Error bars indicate model stochasticity by displaying s.d.'s among five independent model runs (error bars smaller than symbol size are not displayed).

Mentions: The presence of cheating microbes in our model has a strong negative effect on overall litter decay rates across all initial litter C:N ratios (Fig. 1a). If cheaters possess the same functional traits as the main enzyme producers (except for enzyme production), the model predicts that decay rates are reduced by around 50%, no matter if the former are only partly or fully cheating (Fig. 1). If cheating microbes have a higher maximum growth rate than the main enzyme producers, as often observed for opportunistic microbes27, the slowing-down effect is magnified due to cheaters being more competitive, with decay rates being reduced by up to 90%. Initial litter N content also influences decay rates in the model: decay rates decrease with increasing initial litter C:N ratios, particularly in the absence of cheaters, due to increasing N limitation (Fig. 1a). The presence or absence of microbial cheaters, however, has a far stronger influence on decay rates than initial litter N content (Fig. 1a). Decay rates slow down specifically at low initial litter C:N ratios when fast-growing cheaters are present, as fast-growing microbes are especially competitive at high N availability28 (Fig. 1a, dark-red triangles). When initial C:N ratios are high, however, fast-growing cheaters are less competitive compared with cheaters that grow at the same (slow) rate as enzyme producers, because slow-growing microbes cope better with N limitation in our model28. The negative influence of fast-growing cheaters on decay rates is thus diminished when C:N ratios are high, which is visible from decreasing microbial products and carbon use efficiency (CUE), both coming closer to the levels seen in the absence of cheaters (Fig. 1c,d).


Social dynamics within decomposer communities lead to nitrogen retention and organic matter build-up in soils.

Kaiser C, Franklin O, Richter A, Dieckmann U - Nat Commun (2015)

Social dynamics among microbial decomposers affect C and N turnover rates.Effect of microbial cheaters on (a) decay rates, (b) community carbon use efficiency (both time-averaged over model runs until 60% C loss), (c) C in microbial products and (d) N in microbial products (both aggregated over the grid at the point of 60% total C loss). Open circles: no cheaters, that is, all microbes have equal extracellular enzyme production rates of 0.12 (given as fraction of C uptake after deduction of maintenance respiration invested into extracellular enzyme production). Light-red symbols: mixed communities of enzyme producers with production rates of 0.12 and cheaters with enzyme production rates of 0.04 (‘mild', circles), 0.02 (‘strong', squares) or 0 (‘full', triangles), which otherwise have the same traits as enzyme producers. Dark-red triangles: mixed communities of enzyme producers and cheaters with enzyme production rates of 0 with a higher maximum growth rate compared with enzyme producers (Table 1). Error bars indicate model stochasticity by displaying s.d.'s among five independent model runs (error bars smaller than symbol size are not displayed).
© Copyright Policy - open-access
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4697322&req=5

f1: Social dynamics among microbial decomposers affect C and N turnover rates.Effect of microbial cheaters on (a) decay rates, (b) community carbon use efficiency (both time-averaged over model runs until 60% C loss), (c) C in microbial products and (d) N in microbial products (both aggregated over the grid at the point of 60% total C loss). Open circles: no cheaters, that is, all microbes have equal extracellular enzyme production rates of 0.12 (given as fraction of C uptake after deduction of maintenance respiration invested into extracellular enzyme production). Light-red symbols: mixed communities of enzyme producers with production rates of 0.12 and cheaters with enzyme production rates of 0.04 (‘mild', circles), 0.02 (‘strong', squares) or 0 (‘full', triangles), which otherwise have the same traits as enzyme producers. Dark-red triangles: mixed communities of enzyme producers and cheaters with enzyme production rates of 0 with a higher maximum growth rate compared with enzyme producers (Table 1). Error bars indicate model stochasticity by displaying s.d.'s among five independent model runs (error bars smaller than symbol size are not displayed).
Mentions: The presence of cheating microbes in our model has a strong negative effect on overall litter decay rates across all initial litter C:N ratios (Fig. 1a). If cheaters possess the same functional traits as the main enzyme producers (except for enzyme production), the model predicts that decay rates are reduced by around 50%, no matter if the former are only partly or fully cheating (Fig. 1). If cheating microbes have a higher maximum growth rate than the main enzyme producers, as often observed for opportunistic microbes27, the slowing-down effect is magnified due to cheaters being more competitive, with decay rates being reduced by up to 90%. Initial litter N content also influences decay rates in the model: decay rates decrease with increasing initial litter C:N ratios, particularly in the absence of cheaters, due to increasing N limitation (Fig. 1a). The presence or absence of microbial cheaters, however, has a far stronger influence on decay rates than initial litter N content (Fig. 1a). Decay rates slow down specifically at low initial litter C:N ratios when fast-growing cheaters are present, as fast-growing microbes are especially competitive at high N availability28 (Fig. 1a, dark-red triangles). When initial C:N ratios are high, however, fast-growing cheaters are less competitive compared with cheaters that grow at the same (slow) rate as enzyme producers, because slow-growing microbes cope better with N limitation in our model28. The negative influence of fast-growing cheaters on decay rates is thus diminished when C:N ratios are high, which is visible from decreasing microbial products and carbon use efficiency (CUE), both coming closer to the levels seen in the absence of cheaters (Fig. 1c,d).

Bottom Line: The chemical structure of organic matter has been shown to be only marginally important for its decomposability by microorganisms.Moreover, increasing catalytic efficiencies of enzymes are outbalanced by a strong negative feedback on enzyme producers, leading to less enzymes being produced at the community level.Our results thus reveal a possible control mechanism that may buffer soil CO2 emissions in a future climate.

View Article: PubMed Central - PubMed

Affiliation: Evolution and Ecology Program, International Institute for Applied Systems Analysis (IIASA), Schlossplatz 1, A-2361 Laxenburg, Austria.

ABSTRACT
The chemical structure of organic matter has been shown to be only marginally important for its decomposability by microorganisms. The question of why organic matter does accumulate in the face of powerful microbial degraders is thus key for understanding terrestrial carbon and nitrogen cycling. Here we demonstrate, based on an individual-based microbial community model, that social dynamics among microbes producing extracellular enzymes ('decomposers') and microbes exploiting the catalytic activities of others ('cheaters') regulate organic matter turnover. We show that the presence of cheaters increases nitrogen retention and organic matter build-up by downregulating the ratio of extracellular enzymes to total microbial biomass, allowing nitrogen-rich microbial necromass to accumulate. Moreover, increasing catalytic efficiencies of enzymes are outbalanced by a strong negative feedback on enzyme producers, leading to less enzymes being produced at the community level. Our results thus reveal a possible control mechanism that may buffer soil CO2 emissions in a future climate.

Show MeSH
Related in: MedlinePlus