The Development of Biocrust Along the Successional Time Series is Mediated by Archaeal Communities

Abstract

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 that BSCs undergo during ecological succession and dune stabilization 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 during succession but was 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 during succession, 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 BSC succession, 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 a key role in community structure and function in such environments.

Keywords: Biological soil crusts, Microbial community, enzyme, Network, keystone family