Bryophytes harbour microbiomes, including diverse communities of fungi. The molecular mechanisms by which perennial mosses interact with these fungal partners along their senescence gradients are unknown, yet this is an ideal system to study variation in gene expression associated with trophic state transitions. We investigated differentially expressed genes of fungal communities and their host Dicranum scoparium across its naturally occurring senescence gradient using a metatranscriptomic approach. Higher activity of fungal nutrient-related (carbon, nitrogen, phosphorus and sulfur) transporters and Carbohydrate-Active enZyme (CAZy) genes was detected toward the bottom, partially decomposed, layer of the moss. The most prominent variation in the expression levels of fungal nutrient transporters was from inorganic nitrogen-related transporters, whereas the breakdown of organonitrogens was detected as the most enriched gene ontology term for the host D. scoparium, for those transcripts having higher expression in the partially decomposed layer. The abundance of bacterial rRNA transcripts suggested that more living members of Cyanobacteria are associated with the photosynthetic layer of D. scoparium, while members of Rhizobiales are detected throughout the gametophytes. Plant genes for specific fungal-plant communication, including defense responses, were differentially expressed, suggesting that different genetic pathways are involved in plant-microbe crosstalk in photosynthetic tissues compared to partially decomposed tissues.