Patterns and drivers of macro- and micro-diversity of mudflat intertidal archaeomes along the Chinese coasts

Archaea are widespread in Earth's ecosystems, contributing to ecosystem multifunctioning and stability. Compared to bacteria, our understanding of the biodiversity and underlying drivers of archaeal communities in representative ecosystems remains much less tapped. In this study, the macro- and micro-diversity of mudflat intertidal archaeomes were comprehensively analyzed at a large geographic scale, aiming to resolve the ecological drivers determining the variations in archaeal biodiversity. The compositions of mudflat intertidal archaeal taxa highly varied, especially the dominant <i>Thaumarcheota</i> and <i>Euryarchaeota</i>, but maintained relatively stable functional potential across space, demonstrating that functional traits were selected by the ecosystem in priority. While archaeal communities carried important functional traits mediating various biogeochemical cycling processes, horizontal gene transfer played critical roles in endowing functional genes for many archaeal lineages, such as the citric acid cycle in <i>Methanosarcinia</i> and various amino acid metabolism genes in <i>Thermoplasmata</i>. Spatial scaling, including latitudinal diversity gradient and distance-decay patterns (DDR), was clearly observed for archaeal taxonomic groups, but only DDR was weakly observed for functional traits. Intra-population genetic variations were significantly and positively associated with community macro-diversity, demonstrating covariations between nucleotide-level micro- and community-level macro-diversity. The compositions of intertidal archaeomes were mainly structured by homogeneous selection, with different phylogenetic bins being shaped by distinct ecological processes and remarkable variations across different sites. The study contributes to a comprehensive insight into the mechanisms shaping archaeal diversity and ecological characteristics within a fluctuating ecosystem.<b>IMPORTANCE</b>The dynamic intertidal mudflat ecosystems host intense biogeochemical activities mediated by microbial communities, among which archaea contribute as an essential component but remain much less understood compared to bacteria. To gain better insights into the diversity, functional potential, and ecological drivers of archaeal communities in intertidal mudflats, archaeal phylogenetic signatures and genomic sequences were recovered via amplicon sequencing of 16S rRNA genes and shotgun metagenomes, targeting both macro- and micro-diversity. The results showed that archaeal taxonomic composition highly varied across space, whereas the functional potential remained relatively stable. Horizontal gene transfer served as an important source of archaeal metabolic diversity, obtaining additional genes linked to key biochemical pathways. The dominance of environmental selection further demonstrated the ecological forces governing archaeal communities in highly variable coastal habitats. This study established a large-scale framework for understanding the microbial ecology of intertidal archaeomes in dynamic coastal ecosystems.