Abstract
Organic matter constitutes a key reservoir in global elemental cycles. However, our understanding of the dynamics of organic matter and its accumulation remains incomplete. Seemingly disparate hypotheses have been proposed to explain organic matter accumulation: the slow degradation of intrinsically recalcitrant substrates, the depletion to concentrations that inhibit microbial consumption, and a dependency on the consumption capabilities of nearby microbial populations. Here, using a mechanistic model, we develop a theoretical framework that explains how organic matter predictably accumulates in natural environments due to biochemical, ecological, and environmental factors. Our framework subsumes the previous hypotheses. Changes in the microbial community or the environment can move a class of organic matter from a state of functional recalcitrance to a state of depletion by microbial consumers. The model explains the vertical profile of dissolved organic carbon in the ocean and connects microbial activity at subannual timescales to organic matter turnover at millennial timescales. The threshold behavior of the model implies that organic matter accumulation may respond nonlinearly to changes in temperature and other factors, providing hypotheses for the observed correlations between organic carbon reservoirs and temperature in past earth climates.
Highlights
Organic matter constitutes a key reservoir in global elemental cycles
Though significant progress has been made on integrating organic matter (OM) cycling with microbial community dynamics [12,13,14,15,16,17], we still lack a mechanistic understanding of the ecological controls on OM and its accumulation
Three hypotheses have been invoked to explain DOM accumulation in the ocean: 1) “Recalcitrance”: Compounds may accumulate because they are relatively slowly degraded or resistant to further degradation by microorganisms [8, 9, 18, 19]. This is consistent with observations, theory, and inferences of a wide range of consumption rates and compound ages in the ocean [20,21,22,23,24,25], as well as in sediments and soils [9,10,11, 26, 27]. 2) “Dilution”: The accumulation may represent the sum of low concentrations of many organic compounds, each having been diluted by microbial consumption to a minimum amount [28]
Summary
The majority of pools are depleted to relatively low concentrations (10−4 to 1 μM C), while a subset accumulates to substantially higher concentrations (0.1 to 10 μM C). The latter accumulated pools comprise the bulk of total carbon content (Fig. 2B). We evaluate whether each OM pool equilibrates or accumulates in the model. Equilibration indicates that the pool can sustain a microbial population in the given environment, and we classify that pool as “functionally labile.”. The pool accumulates in the environment, and we classify that pool as “functionally recalcitrant.”. Equilibration indicates that the pool can sustain a microbial population in the given environment, and we classify that pool as “functionally labile.” Otherwise, the pool accumulates in the environment, and we classify that pool as “functionally recalcitrant.” For example, we describe the population dynamics of specialist population j , subsisting solely on OM pool i, as (Materials and Methods):
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