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Stable Isotope Analyses Reveal Previously Unknown Trophic Mode Diversity in the Hymenochaetales

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Stable Isotope Analyses Reveal Previously Unknown Trophic Mode Diversity in the Hymenochaetales RESEARCH ARTICLE Stable isotope analyses reveal previously unknown trophic mode diversity in the Hymenochaetales Hailee B. Korotkin1, Rachel A. Swenie1, Otto Miettinen2, Jessica M. Budke1, Ko-Hsuan Chen3, François Lutzoni3, Matthew E. Smith4, and P. Brandon Matheny1,5 Manuscript received 24 February 2018; revision accepted 2 August PREMISE OF THE STUDY: The Hymenochaetales are dominated by lignicolous saprotrophic 2018. fungi involved in wood decay. However, the group also includes bryophilous and 1 Department of Ecology and Evolutionary Biology, University of terricolous taxa, but their modes of nutrition are not clear. Here, we investigate patterns Tennessee, 1416 Circle Drive, Knoxville, Tennessee 37996, USA of carbon and nitrogen utilization in numerous non- lignicolous Hymenochaetales and 2 Botanical Museum, Finnish Museum of Natural History, University provide a phylogenetic context in which these non- canonical ecological guilds arose. of Helsinki, PO Box 7, FI-00014, Finland 3 Department of Biology, Duke University, Box 90338, Durham, North METHODS: We combined stable isotope analyses of δ13C and δ15N and phylogenetic analyses Carolina 27708, USA to explore assignment and evolution of nutritional modes. Clustering procedures and 4 Institute of Food and Agricultural Sciences, Plant statistical tests were performed to assign trophic modes to Hymenochaetales and test for Pathology, University of Florida, 2550 Hull Road, Gainesville, Florida differences between varying ecologies. Genomes of Hymenochaetales were mined for 32611, USA presence of enzymes involved in plant cell wall and lignin degradation and sucrolytic activity. 5 Author for correspondence (e-mail: [email protected]) Citation: Korotkin, H. B., R. A. Swenie, O. Miettinen, J. M. Budke, KEY RESULTS: Three different trophic clusters were detected – biotrophic, saprotrophic, K.-H. Chen, F. Lutzoni, M. E. Smith, and P. B. Matheny. 2018. Stable and a second biotrophic cluster including many bryophilous Hymenochaetales and isotope analyses reveal previously unknown trophic mode diversity in mosses. Non- lignicolous Hymenochaetales are generally biotrophic. All lignicolous the Hymenochaetales. American Journal of Botany 105(11): 1–19. Hymenochaetales clustered as saprotrophic and most terricolous Hymenochaetales doi:10.1002/ajb2.1183 clustered as ectomycorrhizal. Overall, at least 15 species of Hymenochaetales are inferred as biotrophic. Bryophilous species of Rickenella can degrade plant cell walls and lignin, and cleave sucrose to glucose consistent with a parasitic or endophytic life style. CONCLUSIONS: Most non- lignicolous Hymenochaetales are biotrophic. Stable isotope values of many bryophilous Hymenochaetales cluster as ectomycorrhizal or in a biotrophic cluster indicative of parasitism or an endophytic life style. Overall, trophic mode diversity in the Hymenochaetales is greater than anticipated, and non- lignicolous ecological traits and biotrophic modes of nutrition are evolutionarily derived features. KEY WORDS Agaricomycetes; Basidiomycota; ecology; endophytes; functional diversity; mosses; mycorrhizoids; phylogenetics; stable isotopes. The basidiomycete order Hymenochaetales Oberw. contains some 2006), were previously treated as Agaricales Underw. due to simi- 900 species of mostly polyporoid and corticioid fungi classified larities in basidiome morphology (Redhead et al., 2002) but were re- in 75 genera worldwide (Hibbett et al., 2014). Most are lignicolous covered in the Hymenochaetales by molecular phylogenetic analyses white- rot saprotrophs that decompose wood (Wagner and Fischer, (Moncalvo et al., 2000, 2002; Redhead et al., 2002). Later, the group 2002; Binder et al., 2005; Larsson et al., 2006; Tedersoo et al., 2007). was referred to as the Rickenella clade (Larsson et al., 2006) and classi- The order also includes a few species with diverse mycorrhizal abil- fied in the family Rickenellaceae Vizzini (Vizzini, 2010; Nakasone and ities (Nouhra et al., 2013; Tedersoo and Smith, 2013; Kolařík and Burdsall, 2012), the name of which, unfortunately, is illegitimate due to Vohník, 2018), plant pathogens (Larsson et al., 2006), and several inclusion of the type of the earlier described family Repetobasidiaceae agarics or mushroom- forming fungi that typically occur on or with Jülich (Jülich, 1981). In addition, the diversity of its constituents is bryophytes—particularly mosses or liverworts—or that occur on soil unsettled, the monophyly of the group has been questioned (Larsson, (Redhead et al., 2002) (Fig. 1). These non- lignicolous fungi, particu- 2007; Miettinen and Larsson, 2010), and their nutritional modes are larly the bryophilous agarics (Racovitza, 1959; Davey and Currah, largely unclear (Felix, 1988; Kost, 1988; Bresinsky and Schötz, 2006). American Journal of Botany 105(11): 1–19, 2018; http://www.wileyonlinelibrary.com/journal/AJB © 2018 Botanical Society of America • 1 2 • American Journal of Botany A B 2001; Trudell et al., 2004; Mayor et al., 2009; Seitzman et al., 2011; Hobbie and Högberg, 2012; Tedersoo et al., 2012; Birkebak et al., 2013; Trappe et al., 2015; Sánchez- García and Matheny, 2017). However, analysis of stable isotope data has not been used to ex- plore the trophic status of bryophilous and terricolous Hymenochaetales, and very few Hymenochaetales overall have even been evaluated, probably due to the fact that most Hymenochaetales are lignicolous sapro- trophs (Wagner and Fischer, 2002). Stable isotope data are useful to discriminate be- tween Hymenochaetales that acquire their nutrition from a live associate or from dead C organic matter, thus providing a powerful D means to discern the degree of trophic di- versity in the order without direct observa- tions of trophic interactions in the field or laboratory. Analysis of fungal nutritional modes can also be augmented by an array of approaches that include anatomical studies, pure synthe- ses or in vitro experiments, molecular ecol- ogy (e.g., barcoding ectomycorrhizal (ECM) root tips), and phylogenetic relatedness (Tedersoo et al., 2010). In addition, the pres- ence or absence of unique suites of genes that EF encode enzymes involved in nutrient acqui- sition can also be used to characterize trophic modes in fungi (Parrent et al., 2009; Wolfe et al., 2012). To this end, the U.S. Department of Energy Joint Genome Institute has se- quenced the whole genomes of two species of bryophilous Hymenochaetales, Rickenella fibula (Bull.) Raithelh. and R. mellea (Singer & Clémençon) Lamoure, and five genomes of lignicolous Hymenochaetales as of this writing. Here we carry out a cluster analysis of sta- ble C and N stable isotope data from nearly 1000 samples of Agaricomycetes Doweld, phylogenetic analyses of a multigene data- FIGURE 1. Ecological and trophic diversity of Hymenochaetales. (A) Hymenochaete cinnamomea set, ancestral state reconstruction analyses, (lignicolous saprotroph). (B) Trichaptum abietinum (lignicolous saprotroph). (C) Contumyces and genome searches for key enzymes used rosellus (terricolous and possible biotroph). (D) Coltricia perennis (terricolous ECM biotroph). (E) to degrade plant cell walls and lignin and Rickenella swartzii (bryophilous biotroph). (F) Rickenella minuta (terricolous ECM biotroph). (A–E) sucrolytic activity, in order to determine Photos M. G. Wood. (F) Photo P. B. Matheny. Scale bars = 10 mm. whether bryophilous, lignicolous, and ter- ricolous Hymenochaetales are saprotrophic The phyogenetic placement of the Rickenella clade in the or biotrophic, whether these states are derived or ancestral, and Hymenochaetales raises several questions about its ecology and evo- whether these ecological guilds share similar or dissimilar modes lution: (1) is the non- lignicolous association derived or ancestral in of nutrition. the Hymenochaetales? (2) What are the trophic modes of bryophil- ous and terricolous Hymenochaetales? That is, are they saprotrophs that decay dead organic matter for carbon nutrition, or are they bi- MATERIALS AND METHODS otrophs that acquire carbon nutrition from a live symbiont? Or; (3) can they do both? If biotrophs, do they engage in a nutrient-exchange Stable isotope analyses mutualism with bryophytes, or are they parasites of bryophytes? Analysis of stable isotope signatures of nitrogen (δ15N) and carbon A total of 108 specimens, including 92 samples of Hymenochaetales (δ13C) has been used to infer trophic modes of fungi (Hobbie et al., (Table 1), were analyzed at the University of New Hampshire 2018, Volume 105 • Korotkin et al.—Trophic mode diversity in the Hymenochaetales • 3 TABLE 1. Metadata for 108 collections analyzed by stable isotope mass spectrometry, δ15N and δ13C stable isotope values, and trophic cluster assigned by mclust analysis. liv. = living gametophyte tissue; sen. = senescent gametophyte tissue. Herbarium abbreviations follow Thiers [continuously updated]. Herbarium Specimen- Long./ Date of δ15N δ13C Taxon accession no. voucher no. Location Lat. Ecology collection (‰) (‰) Alloclavaria purpurea TENN071489 HRL0146 Quebec 48.7081 Terricolous On soil 2008- 08- 26 4.92 −24.28 −67.3889 Alloclavaria purpurea H6047394 Korhonenen Finland 66.5039 Terricolous On soil 1991- 08- 18 3.10 −22.18 10305 25.7294 Alloclavaria purpurea H6047434 Korhonen Finland 65.9646 Terricolous On soil 1991- 08- 26 1.41 −24.86 10411 29.1887 Alloclavaria purpurea H6034567 Niskanen Finland 62.5000 Terricolous On soil with Picea, 2001- 08- 20 3.61 −24.46 01- 053 22.7500 Betula Alloclavaria purpurea H6034547 Niskanen Finland 64.8675 Terricolous
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