A revision of malbranchea-like fungi from clinical specimens in the United States of America reveals unexpected novelty

Abstract

The fungi of the order Onygenales can cause important human infections; however, their taxonomy and worldwide occurrence is still little known. We have studied and identified a representative number of clinical fungi belonging to that order from a reference laboratory in the USA. A total of 22 strains isolated from respiratory tract (40%) and human skin and nails (27.2%) showed a malbranchea-like morphology. Six genera were phenotypically and molecularly identified, i.e. Auxarthron/Malbranchea (68.2%), Arachnomyces (9.1%), Spiromastigoides (9.1%), and Currahmyces (4.5%), and two newly proposed genera (4.5% each). Based on the results of the phylogenetic study, we synonymized Auxarthron with Malbranchea, and erected two new genera: Pseudoarthropsis and Pseudomalbranchea. New species proposed are: Arachnomyces bostrychodes, A. graciliformis, Currahmyces sparsispora, Malbranchea gymnoascoides, M. multiseptata, M. stricta, Pseudoarthropsis crassispora, Pseudomalbranchea gemmata, and Spiromastigoides geomycoides, along with a new combination for Malbranchea gypsea. The echinocandins showed the highest in vitro antifungal activity against the studied isolates, followed by terbinafine and posaconazole; in contrast, amphotericin B, fluconazole, itraconazole and 5-fluorocytosine were less active or lacked in vitro activity against these fungi.

Keywords: Antifungals; Arachnomycetales; Auxarthron; Clinical fungi; Malbranchea; New taxa; Onygenales.

Fig. 1

Malbranchea pulchella Sacc. & Penzig. Holotype and lectotype. Black ink drawings by A. Malbranche, and pencil drawings by P. A. Saccardo (credits: Rosella Marcucci, erbario micologico di Pier Andrea Saccardo, Università di Padova, Italy)

Fig. 2

ML phylogenetic tree based on the analysis of ITS-LSU nucleotide sequences for the 22 clinical fungi from the USA. Bootstrap support values/Bayesian posterior probability scores of 70/0.95 and higher are indicated on the nodes. ^T = ex type. Fully supported branched (100% BS /1 PP) are indicated in bold. Strains identified by us are in bold. Arachnomyces spp. were chosen as out-group. The sequences used in this analysis are in Table 1

Fig. 3

Arachnomyces bostrychodes CBS 146926 ^T. a Colonies on PYE, PDA and OA after 14 d at 25 °C, from left to right (top row, surface; bottom row, reverse). b Detail of the colony on OA. c, d Sinuous, contorted to coiled fertile hyphae. e Arthroconidia. Scale bar = 10 μm

Fig. 4

Arachnomyces graciliformis CBS 146927 ^T. a Colonies on PYE, PDA and OA after 14 d at 25 °C, from left to right (top row, surface; bottom row, reverse). b Detail of the colony on OA. c–e Contorted, apically coiled fertile hyphae bearing arthroconidia. Scale bar = 10 μm

Fig. 5

Currahmyces sparsispora CBS 146929 ^T. a Colonies on PYE, PDA and OA after 14 d at 25 °C, from left to right (top row, surface; bottom row, reverse). b Detail of the colony on OA. c–d Intercalary arthroconidia along the fertile hyphae. Scale bar = 10 μm

Fig. 6

Malbranchea gymnoascoides CBS 146930 ^T. a Colonies on PYE, PDA and OA after 14 d at 25 °C, from left to right (top row, surface; bottom row, reverse). b Detail of the colony on OA. c–d Young and mature ascomata. e Young ascus on fertile hyphae. f Peridial spine-like appendage. g Intercalary arthroconidia along the fertile hyphae. Scale bar = 10 μm

Fig. 7

Malbranchea multiseptata CBS 146931 ^T. a Colonies on PYE, PDA and OA after 14 d at 25 °C, from left to right (top row, surface; bottom row, reverse). b Detail of the colony on PDA. c–d Highly septate fertile hyphae and arthroconidia. Scale bar = 10 μm

Fig. 8

Malbranchea stricta CBS 146932 ^T. a Colonies on PYE, PDA and OA after 14 d at 25 °C, from left to right (top row, surface; bottom row, reverse). b Detail of the colony on OA. c–e Alternate arthroconidia on primary hyphae and lateral branches. Scale bar = 10 μm

Fig. 9

Pseudoarthropsis crassispora CBS 146928 ^T. a Colonies on PYE, PDA and OA after 14 d at 25 °C, from left to right (top row, surface; bottom row, reverse). b Detail of the colony on OA. c–e Bi- to trichotomously-branched fertile hyphae. f A large chain of holoarthric conidia. Scale bar = 10 μm

Fig. 10

Pseudomalbranchea gemmata CBS 146933 ^T. a Colonies on PYE, PDA and OA after 14 d at 25 °C, from left to right (top row, surface; bottom row, reverse). b Detail of the colony on OA. c–d Large, intercalary, irregularly-shaped arthroconidia disposed singly or in chains along the fertile hyphae. Scale bar = 10 μm

Fig. 11

Spiromastigoides geomycoides CBS 146934 ^T. a Colonies on PYE, PDA and OA after 14 d at 25 °C, from left to right (top row, surface; bottom row, reverse). b Detail of the colony on OA. c Fertile lateral branches mimicking Geomyces spp. conidiophores. d–e Fertile hyphae with intercalary, barrel-shaped arthroconidia. f Morphological diversity of arthroconidia. Scale bar = 10 μm