The free-living microbial biomass in soil is unsupportable by the measured inputs of carbon: How do microbes survive and why should ecologists care

Background/Question/Methods

Background and Questions. Heterotrophic microbes in soil, bacteria and fungi, obtain carbon and energy from hotspots of root processes or the slow breakdown of soil organic carbon.  Analysis of the non-hotspot microbes reveals that microbial biomass is much higher than can be supported by the measured inputs of carbon.  This condition, called excess biomass, is always present and leads to low rates of microbial growth; as calculated from soil respiration rates, the microbial population turns over approximately once per year. In spite of the low growth rates, microbes keep a low level of activity and their respiration responds immediately to added sugars and amino acids.  How can heterotrophic microbes survive and compete for substrate?  Does the condition of excess biomass have implications for our studies of ecological function of these microbes?

Results/Conclusions

Conclusions and Implications. As a community, heterotrophic microbes reduce their activity to semi-starvation levels and yet retain the ability to immediately incorporate any substrate molecules, such as sugars, amino acids, or fatty acids, as soon as they become available.  They keep ATP levels high, and retain transport and respiratory pathways.  Because they use amino acids for energy rather than for protein building, we conclude they are energy- and carbon-limited.  One implication is that labile substrates are taken up as fast as the molecules become available; the actual concentration is likely to be vanishing low, at the nM level.  However, water extracts of dissolved amino acids indicate concentrations of hundreds of µM.  The paradox of high concentrations existing despite rapid microbial removal is difficult to resolve.  We conclude that these high concentrations are not available to microbes but are hidden in soil pores and released when soil is disturbed during sampling.  The rapid microbial uptake of both natural and introduced substrates implies that added, labeled substrates will not mix adequately with natural substrate pools prior to uptake; accordingly, a substrate turnover time cannot be measured.  Finally, the ecological implications are: (1) the levels of microbial biomass are uncoupled from decomposition rates; and (2) distinguishing active from inactive cells and perhaps expressed from non-expressed genes is difficult at the persistent low levels of activity in microbes that can nevertheless respond swiftly to sporadic resource pulses.