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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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Effects of social regulation on microbial organic matter decomposition.(a) Without social regulation (all microbes produce enzymes), turnover rates are high due to a direct positive feedback of enzyme production on microbial growth. The accumulation of microbial remains is limited by a relatively high ratio of enzymes to microbial biomass. The consequently large DOM pool features losses of labile C and N. (b) When cheaters are present, only a (self-regulated) fraction of microbes produces enzymes, resulting not only in a lower total amount of enzymes, but also in a lower amount of enzymes per microbial biomass, leading to a lower amount of enzymes per dead microbial biomass (microbial remains). While the lower total amount of enzymes slows down decay rates, resulting in a smaller DOM pool and less loss over time of C and N by leaching, the lower ratio of enzymes to microbial remains increases the pool of N-rich microbial remains in relation to N-poor plant material, which in turn lowers DOM C:N ratio and alleviates microbial N limitation.
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f4: Effects of social regulation on microbial organic matter decomposition.(a) Without social regulation (all microbes produce enzymes), turnover rates are high due to a direct positive feedback of enzyme production on microbial growth. The accumulation of microbial remains is limited by a relatively high ratio of enzymes to microbial biomass. The consequently large DOM pool features losses of labile C and N. (b) When cheaters are present, only a (self-regulated) fraction of microbes produces enzymes, resulting not only in a lower total amount of enzymes, but also in a lower amount of enzymes per microbial biomass, leading to a lower amount of enzymes per dead microbial biomass (microbial remains). While the lower total amount of enzymes slows down decay rates, resulting in a smaller DOM pool and less loss over time of C and N by leaching, the lower ratio of enzymes to microbial remains increases the pool of N-rich microbial remains in relation to N-poor plant material, which in turn lowers DOM C:N ratio and alleviates microbial N limitation.

Mentions: Closer investigation of C and N flows in our model reveals that the accumulation of microbial remains is closely linked to the ratio between microbial biomass and extracellular enzymes responsible for degrading dead microbial biomass. If that ratio is high, a small number of enzymes face a large amount of dead biomass, resulting in a slow degradation of the latter. Conversely, if that ratio is low, a high number of enzymes more quickly degrade a smaller amount of microbial remains (Fig. 4, Supplementary Fig. 2). In traditional decomposition models, which represent microbial biomass as one pool, as well as in our model without cheaters, the fraction of enzymes produced per total microbial biomass can be controlled by a parameter. Manipulating this parameter (Efr), that is, reducing the amount of C that microbes allocate to enzyme production, indeed increases the accumulation of microbial remains when cheaters are absent (Fig. 3, EP 0.12 and EP 0.10 at ‘Regulation by microbial physiology'). This shows the general sensitivity of the accumulation of microbial remains to the amount of enzymes produced per total microbial biomass, which inevitably affects the ratio of active enzymes to dead microbial biomass. The key result of our model analysis is, however, that in a mixed community of enzyme producers and cheaters community-level adaptations emerge: these alter the ratio between enzyme producers and cheaters in a way that downregulates to a minimum the total amount of enzymes produced per total microbial biomass (Fig. 3, ‘Regulation by community dynamics'), leading to the observed increased accumulation of microbial remains.


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)

Effects of social regulation on microbial organic matter decomposition.(a) Without social regulation (all microbes produce enzymes), turnover rates are high due to a direct positive feedback of enzyme production on microbial growth. The accumulation of microbial remains is limited by a relatively high ratio of enzymes to microbial biomass. The consequently large DOM pool features losses of labile C and N. (b) When cheaters are present, only a (self-regulated) fraction of microbes produces enzymes, resulting not only in a lower total amount of enzymes, but also in a lower amount of enzymes per microbial biomass, leading to a lower amount of enzymes per dead microbial biomass (microbial remains). While the lower total amount of enzymes slows down decay rates, resulting in a smaller DOM pool and less loss over time of C and N by leaching, the lower ratio of enzymes to microbial remains increases the pool of N-rich microbial remains in relation to N-poor plant material, which in turn lowers DOM C:N ratio and alleviates microbial N limitation.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

f4: Effects of social regulation on microbial organic matter decomposition.(a) Without social regulation (all microbes produce enzymes), turnover rates are high due to a direct positive feedback of enzyme production on microbial growth. The accumulation of microbial remains is limited by a relatively high ratio of enzymes to microbial biomass. The consequently large DOM pool features losses of labile C and N. (b) When cheaters are present, only a (self-regulated) fraction of microbes produces enzymes, resulting not only in a lower total amount of enzymes, but also in a lower amount of enzymes per microbial biomass, leading to a lower amount of enzymes per dead microbial biomass (microbial remains). While the lower total amount of enzymes slows down decay rates, resulting in a smaller DOM pool and less loss over time of C and N by leaching, the lower ratio of enzymes to microbial remains increases the pool of N-rich microbial remains in relation to N-poor plant material, which in turn lowers DOM C:N ratio and alleviates microbial N limitation.
Mentions: Closer investigation of C and N flows in our model reveals that the accumulation of microbial remains is closely linked to the ratio between microbial biomass and extracellular enzymes responsible for degrading dead microbial biomass. If that ratio is high, a small number of enzymes face a large amount of dead biomass, resulting in a slow degradation of the latter. Conversely, if that ratio is low, a high number of enzymes more quickly degrade a smaller amount of microbial remains (Fig. 4, Supplementary Fig. 2). In traditional decomposition models, which represent microbial biomass as one pool, as well as in our model without cheaters, the fraction of enzymes produced per total microbial biomass can be controlled by a parameter. Manipulating this parameter (Efr), that is, reducing the amount of C that microbes allocate to enzyme production, indeed increases the accumulation of microbial remains when cheaters are absent (Fig. 3, EP 0.12 and EP 0.10 at ‘Regulation by microbial physiology'). This shows the general sensitivity of the accumulation of microbial remains to the amount of enzymes produced per total microbial biomass, which inevitably affects the ratio of active enzymes to dead microbial biomass. The key result of our model analysis is, however, that in a mixed community of enzyme producers and cheaters community-level adaptations emerge: these alter the ratio between enzyme producers and cheaters in a way that downregulates to a minimum the total amount of enzymes produced per total microbial biomass (Fig. 3, ‘Regulation by community dynamics'), leading to the observed increased accumulation of microbial remains.

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