Breaking the enzymatic latch: impacts of reducing conditions on hydrolytic enzyme activity in tropical forest soils

Abstract

The enzymatic latch hypothesis proposes that oxygen (O 2 ) limitation promotes wetland carbon (C) storage by indirectly decreasing the activities of hydrolytic enzymes that decompose organic matter. Humid tropical forest soils are often characterized by low and fluctuating redox conditions and harbor a large pool of organic matter, yet they also have the fastest decomposition rates globally. We tested the enzymatic latch hypothesis across a soil O 2 gradient in the Luquillo Experimental Forest, Puerto Rico, USA. Enzyme activities expressed on a soil mass basis did not systematically decline across a landscape O 2 gradient, nor did phenolics accumulate, the proposed mechanism of the enzymatic latch. Normalizing enzyme activities by C concentrations did suggest a decline in several enzymes as mean soil O 2 decreased. However, relationships between hydrolytic enzymes and reducing conditions were scale-dependent: enzymes displayed neutral to strongly positive relationships with reducing conditions and phenolics when comparing samples within sites, and enzyme activities in 18-d anaerobic incubations generally exceeded those in aerobic soils despite a fourfold increase in phenolics. In summary, although O 2 availability and the activities of some enzymes appeared to be related at landscape scales after accounting for differences in organic matter, reducing conditions and phenolic compounds did not appear to constrain soil hydrolytic enzyme activity at the scale of soil microsites, challenging the enzymatic latch hypothesis. Hydrolytic enzymes can be resilient to periodic anaerobiosis and may actually stimulate O 2 consumption at the microsite scale. We suggest a critical re-examination of mechanisms and the scale dependence of couplings between O 2 and decomposition in terrestrial soils.

Iron-mediated soil carbon response to water-table decline in an alpine wetland

“…It is noteworthy that phenol oxidative and β-glucosidase activities are positively correlated with Fe(II) concentrations in our experiment ( P <0.05; Fig. 4a), which is consistent with several previous reports17181920 and may be attributed to the following mechanisms. First, it is known that Fe(II) may enhance phenol oxidative activity by catalysing the production of hydroxyl radicals171819.…”

“…Several studies have observed that the presence of ferrous iron [Fe(II)] in hypoxic peatland soils may enhance phenol oxidative activity171819. Recently, Hall et al 20. also demonstrated that the activities of hydrolytic enzymes increased with Fe(II) under anaerobic conditions, in contrast to the ‘enzyme latch’ hypothesis.…”

Reducing conditions, reactive metals, and their interactions can explain spatial patterns of surface soil carbon in a humid tropical forest

“…Recent studies have also showed the importance of periodic anaerobiosis in promoting C mobilization and degradation (Thompson et al 2006;Hall et al 2014;Buettner et al 2014;Hall et al 2015b), although our present data suggest that inhibitory effects of anaerobiosis on organic matter decomposition may predominate at the landscape scale. Recent studies have also showed the importance of periodic anaerobiosis in promoting C mobilization and degradation (Thompson et al 2006;Hall et al 2014;Buettner et al 2014;Hall et al 2015b), although our present data suggest that inhibitory effects of anaerobiosis on organic matter decomposition may predominate at the landscape scale.…”

Lignin decomposition is sustained under fluctuating redox conditions in humid tropical forest soils

“…A broad spectrum of heterotrophic bacteria can couple anaerobic C oxidation directly or indirectly to Fe oxides via organic electron shuttles, generating Fe(II). Across a gradient of representative humid tropical soils (Oxisols, Ultisols, and Inceptisols), in situ Fe(II) concentrations remained at high and ecologically relevant concentrations (hundreds–thousands of μ g Fe(II) g soil −1 ) despite high rainfall, likely due to the high cation exchange capacity of these soils and the predominance of macropore flow, which typically preclude complete moisture saturation (Hall et al ., , ).…”

“…A broad spectrum of soils exhibits O 2 limitation (hypoxia or anaerobiosis) over varying spatial scales, ranging from microsites in soil aggregates (mm-cm) to entire soil profiles (tens of cm) (Sexstone et al, 1985;Silver et al, 1999;Fimmen et al, 2008;Liptzin et al, 2011). Variation in O 2 availability can affect a wide range of biogeochemical process rates (Ponnamperuma, 1972;Silver et al, 1999;Davidson et al, 2012;Hall et al, 2014), and importantly, hypoxia is widely thought to retard lignin decomposition in soils and limit the growth of lignin-degrading fungi (Kirk & Farrell, 1987;Haider, 1992;Ekschmitt et al, 2008). Humid tropical forests provide an important example where a combination of warm temperatures, high rainfall, clay-rich soils, bioturbation, high biological O 2 demand, and large inputs of organic matter generates large spatial and temporal variation in surface soil O 2 availability.…”