Diversity, taxonomic composition, and functional aspects of fungal communities in living, senesced, and fallen leaves at five sites across North America

Abstract

BackgroundFungal endophytes inhabit symptomless, living tissues of all major plant lineages to form one of earth’s most prevalent groups of symbionts. Many reproduce from senesced and/or decomposing leaves and can produce extracellular leaf-degrading enzymes, blurring the line between symbiotrophy and saprotrophy. To better understand the endophyte–saprotroph continuum we compared fungal communities and functional traits of focal strains isolated from living leaves to those isolated from leaves after senescence and decomposition, with a focus on foliage of woody plants in five biogeographic provinces ranging from tundra to subtropical scrub forest.MethodsWe cultured fungi from the interior of surface-sterilized leaves that were living at the time of sampling (i.e., endophytes), leaves that were dead and were retained in plant canopies (dead leaf fungi, DLF), and fallen leaves (leaf litter fungi, LLF) from 3–4 species of woody plants in each of five sites in North America. Our sampling encompassed 18 plant species representing two families of Pinophyta and five families of Angiospermae. Diversity and composition of fungal communities within and among leaf life stages, hosts, and sites were compared using ITS-partial LSU rDNA data. We evaluated substrate use and enzyme activity by a subset of fungi isolated only from living tissues vs. fungi isolated only from non-living leaves.ResultsAcross the diverse biomes and plant taxa surveyed here, culturable fungi from living leaves were isolated less frequently and were less diverse than those isolated from non-living leaves. Fungal communities in living leaves also differed detectably in composition from communities in dead leaves and leaf litter within focal sites and host taxa, regardless of differential weighting of rare and abundant fungi. All focal isolates grew on cellulose, lignin, and pectin as sole carbon sources, but none displayed ligninolytic or pectinolytic activity in vitro. Cellulolytic activity differed among fungal classes. Within Dothideomycetes, activity differed significantly between fungi from living vs. non-living leaves, but such differences were not observed in Sordariomycetes.DiscussionAlthough some fungi with endophytic life stages clearly persist for periods of time in leaves after senescence and incorporation into leaf litter, our sampling across diverse biomes and host lineages detected consistent differences between fungal assemblages in living vs. non-living leaves, reflecting incursion by fungi from the leaf exterior after leaf death and as leaves begin to decompose. However, fungi found only in living leaves do not differ consistently in cellulolytic activity from those fungi detected thus far only in dead leaves. Future analyses should consider Basidiomycota in addition to the Ascomycota fungi evaluated here, and should explore more dimensions of functional traits and persistence to further define the endophytism-to-saprotrophy continuum.

RNA‐based analyses reveal fungal communities structured by a senescence gradient in the moss Dicranum scoparium and the presence of putative multi‐trophic fungi

“…Because no surface sterilization was conducted for the RNA‐based approach, it is possible that some fungi detected using this method are epiphytes. Our finding that few active fungi were differentially more abundant in the top layer vs lower layers suggests that a small proportion of fungal endophytes are obligate biotrophs (Table S8), and that many are multi‐trophic (see also U'Ren & Arnold, ). Whether this pattern results from directional turnover of communities (endophytes transitioning to saprotrophy from top to bottom, saprotrophs switching to endophytism from bottom to top, or individual mycelia spanning multiple layers but having different functional activity in each) requires further investigation.…”

“…Our results demonstrate that several of these fungi are active across the three gametophytic layers, evidence that these fungi might be multi‐trophic even within the same moss gametophyte. These results support the observation that many endophytes have saprotrophic lifestyles in addition to being symbiotrophic (Carroll & Petrini, ; Saikkonen et al ., ; Osono & Hirose, ; Zuccaro et al ., ; U'Ren & Arnold, ; Song et al ., ). Because no surface sterilization was conducted for the RNA‐based approach, it is possible that some fungi detected using this method are epiphytes.…”

“…Understanding the ecological and evolutionary dynamics of such fungi requires an understanding of both their distributions and activity in various plant tissues. Some fungi have been isolated independently from both dead and living plant tissues, suggesting that they may be able to exploit both living and nonliving plant material (U'Ren et al ., ; Osono & Hirose, ; Yuan & Chen, ; U'Ren & Arnold, ). Lophodermium pinastri is one such fungus: it lives as an endophyte inside symptomless pine needles, produces ascospores on fallen needles and can contribute directly to litter decomposition by degrading dead needles (Osono & Hirose, ).…”

Litter chemistry influences decomposition through activity of specific microbial functional guilds

“…, Treseder et al. , U'Ren and Arnold ) and many studies demonstrate linear relationships between C cycle processes (e.g., decomposition) and the number or type of microbial species involved (Griffiths et al. , Naeem et al.…”

Negative plant‐phyllosphere feedbacks in native Asteraceae hosts – a novel extension of the plant‐soil feedback framework

“…), particularly following seed germination and early plant development. Over longer time periods, decomposing litter can eventually contribute to rhizosphere communities (U'Ren & Arnold ). Several studies have measured direct, conspecific effects induced by phyllosphere microbiota using in vivo inoculation, or have extrapolated the functional consequences of host colonisation using in vitro competition assays for specific taxa (Mejia et al .…”