Isotopic evidence of biotrophy and unusual nitrogen nutrition in soil‐dwelling Hygrophoraceae

Abstract

Several lines of evidence suggest that the agaricoid, non-ectomycorrhizal members of the family Hygrophoraceae (waxcaps) are biotrophic with unusual nitrogen nutrition. However, methods for the axenic culture and lab-based study of these organisms remain to be developed, so our current knowledge is limited to field-based investigations. Addition of nitrogen, lime or organophosphate pesticide at an experimental field site (Sourhope) suppressed fruiting of waxcap basidiocarps. Furthermore, stable isotope natural abundance in basidiocarps were unusually high in N and low in C, the latter consistent with mycorrhizal nutritional status. Similar patterns were found in waxcap basidiocarps from diverse habitats across four continents. Additional data from C analysis of basidiocarps and C pulse label experiments suggest that these fungi are not saprotrophs but rather biotrophic endophytes and possibly mycorrhizal. The consistently high but variable δ N values (10-20‰) of basidiocarps further indicate that N acquisition or processing differ from other fungi; we suggest that N may be derived from acquisition of N via soil fauna high in the food chain.

Soil microbial communities associated with giant sequoia: How does the world's largest tree affect some of the world's smallest organisms?

“…Hygrocybe are widespread and can be found in a variety of habitats worldwide (Halbwachs, Karasch, & Griffith, 2013), including forests of the Sequoiadendron sister genus Sequoia (Glassman, personal observation). These fungi are frequently considered to be saprotrophic; however, recent work has implicated some Hygrocybe species, such as H. virginea, as being endophytic (Halbwachs et al, 2013;Tello et al, 2014), and highly elevated δ 15 N values of Hygrophoraceae basidiocarps suggest that Hygrocybe may acquire their N from unusual sources like soil invertebrates (Halbwachs et al, 2018). In our study, Hygrocybe were rarely recovered from beneath sugar pine, corroborating previous assertions that species in this genus avoid EMF-dominated habitats (Halbwachs et al, 2013).…”

Soil stabilisation for DNA metabarcoding of plants and fungi. Implications for sampling at remote locations or via third-parties

“…The CHEGD fungi (barring Entolomataceae) also showed substantial decline in relative abundance in freeze-thaw treatments. Like AMF, these fungi are obligate root-associated biotrophs (Halbwachs et al 2013;Halbwachs et al 2018) and are negatively affected by the killing of host vegetation (Griffith et al 2014). The fact that Entolomataceae were differently affected, compared to other CHEGD fungi, suggests that they are nutritionally more flexible, potentially with some saprotrophic ability.…”

“…This guild of grassland macrofungi fungi (comprising members of the families Clavariaceae, Hygrophoraceae, Entolomataceae, Geoglossaceae and Dermoloma spp.) are dominant components of undisturbed grassland habitats and suspected to be mycorrhizal or with intricate biotrophic association with higher plants (Detheridge et al 2018;Halbwachs et al 2018).…”

New species and reports of Cuphophyllus from northern North America compared with related Eurasian species

“…Species of Cuphophyllus have a biotrophic mode of nutrition, but the nature of the fungus-plant association is largely unknown (Seitzman et al 2011;Halbwachs et al 2018). Cuphophyllus virgineus (Wulfen) Kovalenko was shown to be a root endophyte of Plantago lanceolata and vertically transmitted via seeds (Tello et al 2014).…”

“…Cuphophyllus virgineus (Wulfen) Kovalenko was shown to be a root endophyte of Plantago lanceolata and vertically transmitted via seeds (Tello et al 2014). Other plant associates have not been identified conclusively (Halbwachs et al 2018).…”