Microbial metal homeostasis of biological soil crusts as a mechanism for promoting soil restoration during desert revegetation

Abstract

The main characteristic of a desert ecosystem is a low content of water and nutrients, which reduces the rate of the biogeochemical cycle. In such a seemingly slow metabolism ecosystem, little attention has been paid to microbial metal homeostasis and its relationship with biogeochemical processes and soil properties. Here, we studied the microbial functional genes associated with metal homeostasis from five measurements (17y, 30y, 44y, 53y and 61y) during a 61-year development of biological soil crusts (BSCs) in the revegetation of the Tengger Desert. The aim was to determine the effect of metal homeostasis on biogeochemical cycle and soil properties in a desert ecosystem. Among the microbial functional genes detected by GeoChip 5.0 in BSC samples of different ages, the total signal intensity of iron (Fe) and nickel (Ni) metabolism genes was the highest in the ranking of the top 17 metals. Moreover, Proteobacteria and Actinobacteria were the major source groups at the phylum level of all metal metabolism genes. Almost all genes involved in metal homeostasis had the potential to function as transporters or redox catalyzers. Fe metabolism genes were the main nodes (ten of the top 50 genes) and the zinc (Zn) transporter gene znuC had the most connections (21) in the correlation network of metal genes. Metal metabolism was the focus (11 of the top 30 nodes) for the biogeochemical cycle and other metabolic processes. It had the closest relationship with stress responses, the carbon (C) cycle, and virulence, in that order, and a relatively weak relationship with the nitrogen (N) cycle. Metal homeostasis showed a close positive relationship with soil physiochemical (48.7% explanation) and biological properties (51.4% explanation) compared with C and N cycling (35.2% and 19.8% explanation, respectively). Due to the promotion of soil nutrient and microbial activity in BSCs, metal homeostasis may be regarded as a potential mechanism for soil restoration during desert revegetation. This study unravels the importance of metal homeostasis in the regulation of soil quality and underscores the need for future studies that take a holistic view on biogeochemical cycles mediated by metal homeostasis in soil ecosystems.