Research Article: Differences in the Activities of Eight Enzymes from Ten Soil Fungi and Their Possible Influences on the Surface Structure, Functional Groups, and Element Composition of Soil Colloids

Date Published: November 14, 2014

Publisher: Public Library of Science

Author(s): Wenjie Wang, Yanhong Li, Huimei Wang, Yuangang Zu, Andrew C. Singer.


How soil fungi function in soil carbon and nutrient cycling is not well understood by using fungal enzymatic differences and their interactions with soil colloids. Eight extracellular enzymes, EEAs (chitinase, carboxymethyl cellulase, β-glucosidase, protease, acid phosphatase, polyphenol oxidase, laccase, and guaiacol oxidase) secreted by ten fungi were compared, and then the fungi that showed low and high enzymatic activity were co-cultured with soil colloids for the purpose of finding fungi-soil interactions. Some fungi (Gomphidius rutilus, Russula integra, Pholiota adiposa, and Geastrum mammosum) secreted 3–4 enzymes with weak activities, while others (Cyathus striatus, Suillus granulate, Phallus impudicus, Collybia dryophila, Agaricus sylvicola, and Lactarius deliciosus) could secret over 5 enzymes with high activities. The differences in these fungi contributed to the alterations of functional groups (stretching bands of O-H, N-H, C-H, C = O, COO- decreased by 11–60%, while P = O, C-O stretching, O-H bending and Si-O-Si stretching increased 9–22%), surface appearance (disappearance of adhesive organic materials), and elemental compositions (11–49% decreases in C1s) in soil colloids. Moreover, more evident changes were generally in high enzymatic fungi (C. striatus) compared with low enzymatic fungi (G. rutilus). Our findings indicate that inter-fungi differences in EEA types and activities might be responsible for physical and chemical changes in soil colloids (the most active component of soil matrix), highlighting the important roles of soil fungi in soil nutrient cycling and functional maintenance.

Partial Text

The large majority of the 80,000+ fungal species so far named and described are likely to occur in the soil environment at some stage in their life-cycle [1]. Soil fungi are vital in proper functioning of the ecosystem by helping in the degradation of dead matter, releasing vital nutrients and leading to soil carbon sequestration in boreal forests [2]. Fungal activity is greatest in decomposing leaves and wood, and tends to diminish in the later stages of decomposition when bacteria become more dominant. Fungi utilize both simple and complex molecules as foods by the secretion of a variety of extracellular enzymes (EEA), including protease, cellulase, β-glucosidase, and chitinase [3]–[5]. These EEAs degrade plant protein, cellulose, hemicellulose, starch, and animal compounds such as chitin. In soil, phosphatases, extracellularly secreted by plants and microorganisms, play a key role in the phosphorus cycle, allowing the formation of inorganic phosphorus, the only phosphate form taken up by plants and microorganisms [6]–[9]. Laccase and polyphenol oxidase are the ligninolytic enzymes involved in the degradation of lignin as well as various xenobiotic aromatic compounds [10]–[12]. Various EEAs, which can indicate biological equilibrium, fertility, quality, and biological soil status [13], participate in soil nutrient transformation, energy metabolism, and degradation of various compounds [14], [15]. Current knowledge of fungal diversity in soil has been characterized through various next-generation sequencing methods in many papers [16]–[18] or observations of fruiting bodies present in the variable environment [1]. However, relatively few of these studies have examined functional diversity. Differences in soil fungal communities that affect C,N,P cycling may be due to inter-species differences in EEA activities related with C,N and P metabolism [19]. The functional differences that affect soil C and nutrient cycling need investigational support via comparison of inter-species soil enzymes and their effect on soil C, N, and P. As a hotspot for global warming in the northern hemisphere, northeastern China, with its fertile black soil, is also abundant with diverse soil fungi [20], [21]. Identification of inter-species differences of EEAs secretions could define the roles of soil fungi in cycling of C, N, and P substrates in the global warming process [19].

Fungi play an important role in boreal forest ecosystems, both as decomposers of SOM and as root-associated mediators of belowground C transport and nutrient cycling [12], [18], [40]. Ectomycorrhizal fungi and arbuscular mycorrhizal can benefit forest trees by enhancing soil nutrient uptake, particularly for elements with low mobility in the soil such as P and micronutrients [8], [9], [41], [42]. Our result proved that different fungi differed in their enzymatic secretions related to C, N and P metabolism, and these enzymatic differences could possibly affect the surface structure and chemical composition of soil colloids. In the following sections, these findings will be discussed with comparison of previous studies and data in present study.

EEA types and activities secreted by different fungi vary, and such enzymatic differences affect functional groups traits, element composition, and surface images of soil colloids when co-cultured with fungi. Some fungi (R. integra, P. adiposa, G. rutilus, and G. mammosum) can secrete 3–4 types of enzymes, while others (S. granulatus, P. impudicus, C. dryophila, A. sylvicola, C. striatus, and L. deliciosus) can secrete more than 5 types of enzymes, all with relatively higher enzymatic activity, showing their possible divergent function in soil C, N, and P cycling. Most functional groups related with C and N were markedly decreased, while increases in P-related functional groups were observed, which may be a basis for the fungi-induced P increases for plant growth. Both SEM and EDX data showed changes on the colloid surface and elemental compositions of the soil colloids. Investigations of this process via soil fungi enzymatic differences and interaction with soil colloids may promote the understanding of the underlying mechanisms driving soil nutrient cycling.