The development of biological soil crust along the time series is mediated by archaeal communities

• The biological soil crusts (BSCs) were compared across a time series spanning over 60 years. • Metagenome analysis revealed increasing community integration and complexity over time. • Archaea played a disproportionate role in community structure and stability. • Several key archaeal families could be related to BSC enzyme activities. Biological soil crusts (BSCs) play an essential role in soil stabilization and nutrient cycling in arid environments, being a hotspot of microbial activity including soil enzyme production. However, the changes in microbial communities of the BSCs from different age are poorly understood. In over a 60-year dune revegetation chronosequence (2021, 2016, 1973, and 1962) in the southeastern Tengger Desert, China, we compared the development of BSCs and underlying sands using metagenome sequencing and enzyme assays. In both BSCs and the underlying sand substrate, enzyme activity increased along the time series but was always greater for BSCs than the substrate, emphasizing the potential for nutrient cycling activity. A clear trend in community composition and co-occurrence network complexity was observed in the BSCs: the family-level taxonomic network of BSCs became more connected in the older age BSCs, while in the substrate, there was no such trend. Unexpectedly, considering their low relative abundance and diversity, archaea emerged as major keystones in establishing community networks, being key to network stability. In the underlying substrate, by contrast, archaea did not play this key role. During the time series of BSCs, the dominant archaeal groups were Nitrososphaeria, Methanomicrobia, Halobacteria, and an unclassified Thaumarchaeota, mainly linked to functional genes related to carbon and nitrogen, such as CHB2, xylA, amyA, amoB, nxrA, nxrB, and nirB. This suggests that in BSCs, the key role of archaea relates to their role in nitrogen cycling. This perspective adds to the emerging view that archaea play an important role in community structure and function in dryland environments.