Differential gene expression associated with fungal trophic shifts along the senescence gradient of the moss Dicranum scoparium

Abstract

Summary 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.

Long‐term warming effects on the microbiome andnifHgene abundance of a common moss species in sub‐Arctic tundra

“…Mosses provide a habitat for a range of microbiota, microfauna and mesofauna (Lindo & Gonzalez, 2010). These moss‐associated microorganisms are involved in the decomposition of dead moss tissue (Kulichevskaya et al ., 2007) and some of them are active diazotrophs (Chen et al ., 2019). Nitrogen fixation by moss‐associated Cyanobacteria, the best studied of these diazotrophs, was shown to directly increase moss growth rates (Berg et al ., 2013) and thereby controls C sequestration in moss tissues.…”

Long-term warming effects on the microbiome and nitrogen fixation of a common moss species in sub-Arctic tundra

“…Mosses provide a habitat for a range of microbiota, microfauna and mesofauna (Lindo & Gonzalez, 2010). These moss-associated microorganisms are involved in the decomposition of dead moss tissue (Kulichevskaya et al, 2007) and some of them are active diazotrophs (Chen et al, 2019). N 2 -fixation by moss-associated Cyanobacteria, the best studied of these diazotrophs, was shown to directly increase moss growth rates (Berg et al, 2013) and thereby control C sequestration in moss tissues.…”

Comparative transcriptomics of fungal endophytes in co‐culture with their moss host Dicranum scoparium reveals fungal trophic lability and moss unchanged to slightly increased growth rates

“…The procedure to obtain a reference transcriptome from axenic cultures of D. scoparium was described in Chen et al . (2019). Reference transcriptomes for the targeted fungi were prepared from pure culture growing in liquid malt extract (Table S2).…”

“…By investigating the metabolic activity defined by the relative abundance of transcribed ribosomal RNAs (rRNAs) in metatranscriptomes, fungal communities were shown to be structured by the senescence gradient of D. scoparium (Chen et al, 2018). However, many fungi are able to colonize all three layers, suggesting that these fungi could undergo functional switches associated with occurrence in living vs dead tissue (Chen et al, 2018(Chen et al, , 2019. Dicranum scoparium can be cultivated axenically from spores obtained from unopened capsules (Vuji ci c et al, 2009) and has been studied previously via culture-dependent and culture-free methods with respect to the diverse fungi it harbors (e.g.…”

“…Primarily based on phenotypic features, it has been reported that bryophyte‐associated fungi have various trophic interactions ranging from pathogenic and parasitic to saprotrophic or commensal (Martínez‐Abaigar et al ., 2005; Davey & Currah, 2006; Davey et al ., 2010; Stenroos et al ., 2010; Korotkin et al ., 2018; Raudabaugh et al ., 2021). Though there is rising awareness of the functional importance of the plant microbiome, and the large number of endophytic fungi that inhabit mosses (Kauserud et al ., 2008; U'Ren et al ., 2012, 2019; Davey et al ., 2013a; Yu et al ., 2014; Chen et al ., 2018, 2019), the functions of moss‐associated fungal endophytes are mostly unknown. At the molecular level, moss–fungus interactions have been mostly examined in the model species Physcomitrella patens .…”