Multikingdom interactions govern the microbiome in subterranean cultural heritage sites

Microbial biodeterioration is a major concern for the conservation of historical cultural relics worldwide. However, the ecology involving the origin, composition, and establishment of microbiomes on relics, once exposed to external environments, is largely unknown. Here, we combined field surveys with physiological assays and biological interaction experiments to investigate the microbiome in the Dahuting Han Dynasty Tomb, a Chinese tomb with more than 1,800 y of history, and its surrounding environments. Our investigation finds that multikingdom interactions, from mutualism to competition, drive the microbiome in this subterranean tomb. We reveal that Actinobacteria, Pseudonocardiaceae are the dominant organisms on walls in this tomb. These bacteria produce volatile geosmin that attracts springtails (Collembola), forming an interkingdom mutualism, which contributes to their dispersal, as one of the possible sources into the tomb from surrounding environments. Then, intrakingdom competition helps explain why Pseudonocardiaceae thrive in this tomb via the production of a mixture of cellulases, in combination with potential antimicrobial substances. Together, our findings show that multikingdom interactions play an important role in governing the microbiomes that colonize cultural relics. This knowledge is integral to understanding the ecological and physiological features of relic microbiomes and to supporting the relics’ long-term conservation.