Microbial community structure and resource availability drive the catalytic efficiency of soil enzymes under land-use change conditions

Abstract

The turnover of nutrients bound to organic matter is largely mediated by extracellular hydrolytic enzymes (EHEs) produced by soil microorganisms. However, little is known about the environmental drivers (e.g., soil pH, C content, C:N ratio) of the catalytic properties of EHEs and their functional link to the structure of soil microbial communities. We linked catalytic properties, Km and Vmax, determined by Michaelis–Menten kinetics, to a set of environmental and microbial properties in the soils of a land-use sequence ranging from undisturbed natural forest to pastures of different ages and to secondary succession in the Andes of southern Ecuador. The sensitivity of the substrate affinity constant (Km) and the maximum rate (Vmax) of six EHEs (β-cellobiohydrolase (CBH), β-glucosidase (BG), N-acetylglucosaminidase (NAG), α-glucosidase (AG), xylanase (XYL), acid phosphomonoesterase (AP)) to changing environmental conditions was tested by fluorogenic substrates. We used the Vmax-to-Km ratio (Ka) as a proxy for the catalytic efficiency and the signature membrane phospholipid fatty acids as a proxy of microbial community structure.Microbial communities adapted to environmental changes, selected for enzymes with higher substrate affinity (Km) and catalytic efficiency (Ka) compared with pure cultures. Along the land-use sequence, catalytic efficiency increased from natural forest to young pasture, while it decreased during long-term pasture use and secondary succession. This is consistent with three to five times faster turnover of tested substrates (estimated based on Michaelis–Menten kinetic parameters) at the young pasture compared with the long-term pasture and secondary succession. Environmental drivers of the Km were enzyme-specific (e.g., the pH for XYL, the C:N ratio for AP, and the C availability for NAG) and differed from those for Vmax. A decoupled response of Vmax and Km to land-use changes observed for AG, BG, CBH, XYL, and AP, implies divers consequences for ecosystem processes mediated by these enzymes. A high abundance of Gram(−) bacteria triggered the catalytic properties (Km and/or Ka) of enzymes decomposing cellulose, hemicellulose, starch, and monophosphoesters. The importance of climatic factors for catalytic properties of EHEs was emphasized by the Ka values extracted from the literature and demonstrated good correspondence of Ka between soils from geographically distinct experimental plots.