Guyanagaster necrorhizus T.W. Henkel, Aime & M.E. Sm. in Henkel et al., American Journal of Botany. 97(9): 1477 (2010)
Etymology: Nekros = death, corpse; rhiza = root (Greek), referring to the root wood decaying, putatively parasitic habit of the fungus.
Basidiomata gasteroid, subepigeous to erumpent, scattered or in linear troops, attached directly to woody roots of Dicymbe trees; 22−52 mm broad, 11−35 mm tall, globose to subglobose to ovoid and irregularly broadly lobate, dense, base with smooth, sterile concolorous stipe, 7−10 × 3−6 mm, attached directly to substratum. Peridium black during all stages of development, moist, tough, covered in blunt, 4–5 sided polygonal nondeciduous warts, these 0.75−1.5 mm broad, 0.3−0.5 mm tall, more acuminate with age, sharply differentiated from endoperidium; endoperidium white to light pink, tough, 0.8−1.5 mm thick, of matted hyphae transitioning evenly to sterile, white hyphal veins between the glebal locules; gleba composed of well‐defined locules and intervening veins; locules globose to ovate to subangular, 0.5−4 mm broad, initially pinkish white (5A2−5A3), maturing in stages to flesh pink (6A3−6A4, to 6B6) and eventually a rich brick red (8B8−8C8−8D8) evenly throughout, unchanging; hyphae separating locules initially white, light pink (7A3) in older specimens, darkening slightly with exposure; columella well‐defined, base continuous with stipe, 9−22 × 7−15 mm, initially light pink (∼7A3), orange‐red (7B7−8B7) with age, dense, waterlogged, of longitudinally arranged hyphae under hand lens, sharply demarcated from gleba at apex. With advanced age, entire basidioma permeated with invertebrate excavation channels; tissues between excavation channels remaining firm; without evidence of vertebrate consumption (Fig. 5). Odor mild, somewhat musty, clay‐like in older specimens, taste mildly “chemical” or soapy, texture brittle when chewed. Macrochemical spot tests: KOH reddening endoperidium, columella, and gleba, darkening exoperidium; NH4OH reaction lacking on all surfaces.
Hyphal cords proliferating along exterior of long axis of individual Dicymbe roots from 0.5−3 cm diameter, white, 2−4 mm diameter, roundish to subflattened, tuberculate under lens, in cross section exterior rind undifferentiated, of loosely packed, white hyphae, with gelatinous, gray core 0.5−0.75 mm diameter, occasionally bridging adjacent roots; forming dense yellowish mycelial fans proliferating along root cambial region, from which feeder hyphae ingress via sapwood rays; wood decay reddish when incipient, advancing to a water‐saturated, stringy white rot that eventually gelatinizes.
Exoperidium composed of agglutinated masses of anticlinal hyphae forming conical to rounded warts, in mass 168−336 × 160−168 µm; individual hyphae of outer layer dark brown in H2O, inamyloid, curved to tortuously curved, nongelatinous, 30−42 × 5−6 µm, swollen at septa, apically coalescing into protruding clumps, giving warts a hairy appearance under low magnification, hyphal walls rapidly staining deep red in KOH, with red pigment leaching into mounting medium; outer peridial hyphae subtended by a layer of subisodiametric cells, 14−22 × 12−22 µm, walls in H2O yellow to light brown, 2–3 µm wide, intergrading below with hyphae of endoperidium. Endoperidium 700−760 µm thick, well‐differentiated from exoperidium and glebal locules, composed centrally of highly interwoven, branching, anastomosing hyphae that are irregularly inflated, 2−5 µm wide, hyaline in water and KOH, inamyloid, thin‐walled, moderately gelatinizing to yield an irregularly “honeycombed” appearance in mass; near extreme distal transition with exoperidium cells becoming more inflated and subanticlinal, toward the locules hyphae becoming thinner, more tightly interwoven. Sterile hyphae separating locules similar to endoperidial hyphae, parallel‐interwoven, weakly gelatinous. Glebal locules in thin section globose to subglobose, 163−1020 × 255−1500 µm, tissues densely gelatinous such that locules are difficult to flatten on a microscope slide, preventing permeation of stains; locule tissue primarily of tightly packed basidiospores encased in a gel matrix, at maturity mostly lacking intact hyphae, when present hyphae 1–2 µm wide; well‐organized hymenium lacking. Basidia apparently 2‐sterigmate, difficult to observe even in microtome sections, more or less cylindrical and undifferentiated from subtending hyphae, occasionally inflated near apex and tapering evenly toward base, basal septum usually inevident, hyaline in water, thin‐walled, originating as side branches from locular hyphae in immature locules; sterigmata difficult to observe, apparently long, arising at angles from sides of basidium apex. Basidiospores globose; in H2O and KOH light tannish brown with faint pinkish overtones, in Melzer's rich burgundy brown and therefore darkly dextrinoid, main body thick‐walled, outer spore wall 1−2.4 µm wide, inner wall 0.75−1 µm wide, with regularly globose lumen, covered in entirety with straight to slightly recurved, narrow, cylindrical, apically acuminate spines, which are tightly packed and equidistant throughout, 1.7−2.2 µm tall, apical recurvations sometimes unidirectional and giving the spore ornaments a “combed” appearance, spines apparently immersed in a gelatinous matrix; without spines (10.8–)12.1−15.8 × 12−15.5(–16.1) µm (mean = 13.5 ± 0.3 × 13.5 ± 0.3 um, Q r = 0.93−1.06, Q m = 1.0 ± 0.01); with spines included 15.5−18.5 × 15.6−18.8(–19.4) µm (mean = 17.0 ± 0.2 × 16.8 ± 0.3 µm, Q r = 0.95−1.05, Q m = 1.0 ± 0.01), (N = 20 basidiospores); in side view with robust, symmetrically positioned pedicel, 2.9−4.7 × 2.1−2.5 µm; immature basidiospores hyaline to light pink, wall thinner and spines longer relative to overall diameter, this situation reversing with maturity apparently due to progressive outward thickening of wall and resulting increase in basidiospore diameter, without attendant increase in spine length. Columella tissue composed of moderately interwoven, tightly packed, nongelatinous hyphae; hyphae thin‐walled, hyaline in water and KOH, of variable widths, (2.5–)5−10(–18) µm. Clamp connections absent in all tissues.
Habit, habitat, and distribution: Rare, scattered to abundant between leaf litter and mineral soil attached to decaying woody roots of Dicymbe corymbosa and D. altsonii in tropical rainforest, known only from the Upper Potaro Basin of Guyana.
Index Fungorum number: IF565142
Notes: Guyanagaster necrorhiza is easily recognized in the field by its black, verrucose, subglobose to broadly lobate, firm basidiomata, which emerge slightly from the leaf litter in the vicinity of standing dead trees or recent treefalls. A longitudinal section reveals a firm, pinkish‐flesh to brick red, loculate gleba, and distinct columella. Excavations of basidiomata reveal a black, smooth stipe directly attached to decaying woody roots, with associated white, exterior hyphal cords, mycelia fans in the root cambium, and wet, stringy, white rot of root wood. With advanced age, basidiomata maintain their firmness and moisture content, but are heavily excavated by arthropods.
Phylogenetic analyses fully support the placement of Guyanagaster within the Physalacriaceae in the Agaricales and that the closest related genus within the family is the lamellate Armillaria. However, the exact relationship between Armillaria and Guyanagaster could not be definitively resolved. The five‐gene ML analysis and the EF1 α ML and MP analyses, suggest that Guyanagaster represents a sister taxon to Armillaria , whereas the five‐gene Bayesian and parsimony analyses as well the 28S rDNA ML and PP analyses suggest that Guyanagaster may be derived from within Armillaria , rendering Armillaria paraphyletic. With due consideration to these molecular results, we have chosen to erect Guyanagaster as a new genus for the following reasons: (1) the highly divergent basidioma morphology of Guyanagaster relative to all known species of Armillaria worldwide, including the sequestrate subhypogeous fruiting habit, strongly reduced stipe, gelatinized locules, bright‐red glebal and black peridial colors, spinose basidiospores, inconspicuous basidia, and disorganized fertile tissues; (2) the radically different basidiospore dispersal in Guyanagaster relative to Armillaria ; and (3) the differences in vegetative organs (e.g., the invasive hyphal cords of Guyanagaster are loosely organized, nonsclerotized, and white, whereas the rhizomorphs of all known Armillaria spp. are highly organized with a dense, melanized rind; Pegler 2000). For basidiomata, hyphal cords, and mycelial fans, the ITS rDNA sequences were identical, confirming the root decay habit of Guyanagaster.
Figure 1. Basidiomata of Guyanagaster necrorhiza . (A) Holotype; Henkel 9065 . (B) Longitudinal section of basidioma showing immature gleba and well‐developed peridium, columella, and stipe. (C) Mature gleba; note strong reddening of all internal tissues. Scale bars = 10 mm.