Abstract
Two distinct nutritional syndromes have been described in temperate green orchids. Most orchids form mycorrhizas with rhizoctonia fungi and are considered autotrophic. Some orchids, however, associate with fungi that simultaneously form ectomycorrhizas with surrounding trees and derive their carbon from these fungi. This evolutionarily derived condition has been called mixotrophy or partial mycoheterotrophy and is characterized by 13C enrichment and high N content. Although it has been suggested that the two major nutritional syndromes are clearly distinct and tightly linked to the composition of mycorrhizal communities, recent studies have challenged this assumption. Here, we investigated whether mycorrhizal communities and nutritional syndromes differed between seven green orchid species that co-occur under similar ecological conditions (coastal dune slacks). Our results showed that mycorrhizal communities differed significantly between orchid species. Rhizoctonia fungi dominated in Dactylorhiza sp., Herminium monorchis, and Epipactis palustris, which were autotrophic based on 13C and N content. Conversely, Liparis loeselii and Epipactis neerlandica associated primarily with ectomycorrhizal fungi but surprisingly, 13C and N content supported mixotrophy only in E. neerlandica. This, together with the finding of some ectomycorrhizal fungi in rhizoctonia-associated orchids, suggests that there exists an ecological continuum between the two syndromes. The presence of a large number of indicator species associating with individual orchid species further confirms previous findings that mycorrhizal fungi may be important factors driving niche-partitioning in terrestrial orchids and therefore contribute to orchid coexistence.
Highlights
Since the early discoveries that orchids significantly rely on mycorrhizal fungi for seed germination and seedling establishment (Bernard, 1899; Burgeff, 1909), it has become increasingly clear that mycorrhizal fungi play an important role in carbon nutrition of orchids and in their population dynamics and spatial distribution (McCormick and Jacquemyn, 2014)
The quality-filtered pyrosequencing data set comprised 556 fungal Operational taxonomic units (OTUs) (89900 sequences), of which 104 (64732 sequences – 72.0%) were assigned to putatively orchid mycorrhizal OTUs according to Dearnaley et al (2012) and information from previous studies that detected mycorrhizal fungi from the roots and protocorms of these and related orchid species (Supplementary Table S1)
The majority of the detected fungi belonged to the Ceratobasidiaceae (8 OTUs, 20671 sequences) and Tulasnellaceae (10 OTUs, 9701 sequences) among rhizoctonia fungi, and ectomycorrhizal fungi from the Thelephoraceae (23 OTUs, 13297 sequences), Sebacinaceae (26 OTUs, 8420 sequences) and Inocybaceae (14 OTUs, 8261 sequences) (Figure 1)
Summary
Since the early discoveries that orchids significantly rely on mycorrhizal fungi for seed germination and seedling establishment (Bernard, 1899; Burgeff, 1909), it has become increasingly clear that mycorrhizal fungi play an important role in carbon nutrition of orchids and in their population dynamics and spatial distribution (McCormick and Jacquemyn, 2014). In some green orchid species, often related to the above-mentioned achlorophyllous species, a partly heterotrophic syndrome has been described, called partial mycoheterotrophy or mixotrophy (Selosse and Roy, 2009; Hynson et al, 2013). Such species often grow in closed forest habitats with limited light-availability and associate with the same fungal guilds as achlorophyllous species, most often fungi that form ectomycorrhizae on surrounding trees (Bidartondo et al, 2004; Selosse et al, 2004). Mixotrophic orchids combine photosynthesis and heterotrophic nutrition on ectomycorrhizal fungi
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