Conservation of biotrophy in Hygrophoraceae inferred from combined stable isotope and phylogenetic analyses

Abstract

The nutritional modes of genera in Hygrophoraceae (Basidiomycota: Agaricales), apart from the ectomycorrhizal Hygrophorus and lichen-forming taxa, are uncertain. New δ(15)N and δ(13)C values were obtained from 15 taxa under Hygrophoraceae collected in central Massachusetts and combined with isotopic datasets from five prior studies including a further 12 species using a data standardization method to allow cross-site comparison. Based on these data, we inferred the probable nutritional modes for species of Hygrophorus, Hygrocybe, Humidicutis, Cuphophyllus and Gliophorus. A phylogeny of Hygrophoraceae was constructed by maximum likelihood analysis of nuclear ribosomal 28S and 5.8S sequences and standardized δ(15)N and δ(13)C values were used for parsimony optimization on this phylogeny. Our results supported a mode of biotrophy in Hygrocybe, Humidicutis, Cuphophyllus and Gliophorus quantitatively unlike that in more than 450 other fungal taxa sampled in the present and prior studies. Parsimony optimization of stable isotope data suggests moderate conservation of nutritional strategies in Hygrophoraceae and a single switch to a predominantly ectomycorrhizal life strategy in the lineage leading to Hygrophorus. We conclude that Hygrophoraceae of previously unknown nutritional status are unlikely to be saprotrophs and are probably in symbiosis with bryophytes or other understory plants.

Molecular phylogeny, morphology, pigment chemistry and ecology in Hygrophoraceae (Agaricales)

“…Moncalvo et al (2002) identified many phylogenetic clades that were later supported as belonging to the Hygrophoraceae by Lodge et al (2006), Matheny et al (2006), Lawrey et al (2009) and Binder et al (2010). Neither Binder et al (2010) nor Seitzman et al (2011) found support for a monophyletic family, but Matheny et al (2006) found Bayesian support for a monophyletic Hygrophoraceae s.l. if Camarophyllopsis and Neohygrophorus were excluded.…”

“…Matheny et al (2006) were first to show strong support for a monophyletic Hygrophoraceae. The Hygrophoraceae appears to be mostly biotrophic based on stable carbon and nitrogen isotope signatures, though only the type genus, Hygrophorus, forms ectomycorrhizal associations with tree roots (Seitzman et al 2011;Tedersoo et al 2010). Acantholichen, Cora, Corella, Cyphellostereum, Dictyonema, Lichenomphalia and Semiomphalina species form lichens with green algae or cyanobacteria Matheny et al 2006;Redhead et al 2002), Eonema is associated with live ferns and grasses , and Arrhenia and Cantharellula are generally associated with bryophytes ).…”

“…Acantholichen, Cora, Corella, Cyphellostereum, Dictyonema, Lichenomphalia and Semiomphalina species form lichens with green algae or cyanobacteria Matheny et al 2006;Redhead et al 2002), Eonema is associated with live ferns and grasses , and Arrhenia and Cantharellula are generally associated with bryophytes ). Biotic relationships for the remaining genera of Hygrophoraceae are enigmatic (Seitzman et al 2011). Currently, Hygrophoraceae comprises over 600 species (not all described) in 25 named genera and one new genus (Tables 1 and 2), and is thus one of the larger families in the Agaricales.…”

DNA barcoding and morphological studies reveal two new species of waxcap mushrooms (Hygrophoraceae) in Britain

“…However, their belowground ecology, in particular their nutritional mode(s), remains unclear despite recent attention by several researchers. Indirect evidence from carbon and nitrogen stable isotope ratios suggests that at least some taxa are biotrophic (Seitzman et al 2011), and further evidence of a mycorrhiza-like association with plants has been demonstrated recently (Halbwachs et al unpublished data).…”

The phylogenetic position ofHaasiella(Basidiomycota, Agaricomycetes) and the relationships betweenH. venustissimaandH. splendidissima

“…Based on BLASTN results, sequences were selected according to the outcomes of recent phylogenetic studies on Agaricales Underw. (Matheny et al 2006;Binder et al 2010;Ovrebo et al 2011;Seitzman et al 2011). A combined analysis of ITS and LSU sequences was carried out with sequences from the same strain or specimen.…”