Fungal Diversity DOI 10.1007/s13225-015-0338-5 Chaetomium-like fungi causing opportunistic infections in humans: a possible role for extremotolerance Sarah A. Ahmed1,2,3 & Ziauddin Khan4 & Xue-wei Wang2,5 & Tarek A. A. Moussa 6,7 & Hassan S. Al-Zahrani6 & Omar A. Almaghrabi6 & Deanna A. Sutton8 & S. Ahmad4 & Johannes Z. Groenewald2 & A. Alastruey-Izquierdo9 & Anne van Diepeningen2 & S. B. J. Menken3 & M. J. Najafzadeh10 & Pedro W. Crous 2 & Oliver Cornely11 & Axel Hamprecht12 & Maria J. G. T. Vehreschild11 & A. J. Kindo13 & G. Sybren de Hoog2,3,6,14,15,16,17 Received: 27 March 2015 /Accepted: 11 June 2015 # The Author(s) 2015. This article is published with open access at Springerlink.com Abstract Members of the family Chaetomiaceae are ubiqui- described; two belong to the genus Subramaniula and one tous ascosporulating fungi commonly, which reside in soil represents a Chaetomium species. Subramaniula asteroides enriched with manure or cellulosic materials. Their role as was isolated from various sources including eye and skin in- human pathogens is largely ignored. However, the ability of fections as well as from the natural environment, and some species to grow at high temperature enables them to play S. obscura was isolated from a toe infection. Chaetomium an important role as opportunistic pathogens. The family con- anamorphosum was isolated from a kidney transplant patient tains several genera and species that have never been reported suffering from fungal peritonitis. All species described were to cause human infection. Hereby, three new species are previously misidentified as Papulaspora spp. due to the Taxonomic novelties: Chaetomium anamorphosum S.A. Ahmed, Z.U. Khan, X. Wang & de Hoog, Subramaniula asteroides S.A. Ahmed, Z.U. Khan, X. Wang & de Hoog, Subramaniula obscura S.A. Ahmed, Z.U. Khan, X. Wang & de Hoog. * Sarah A. Ahmed 9 Mycology Reference Laboratory, National Centre for Microbiology, [email protected] Carlos III Institute of Health (Servicio de Micología, Centro Nacional de Microbiología, Instituto de Salud Carlos III), Madrid, Spain 10 Department of Parasitology and Mycology, Mashhad University of 1 Faculty of Medical Laboratory Sciences, University of Khartoum, Medical Sciences, Mashhad, Iran Khartoum, Sudan 11 German Centre for Infection Research (DZIF) at Cologne/Bonn, First 2 CBS-KNAW Fungal Biodiversity Centre, P.O. Box 85167, 3508 Department of Internal Medicine, University Hospital of Cologne, AD Utrecht, The Netherlands Cologne, Germany 3 Institute for Biodiversity and Ecosystem Dynamics, University of 12 Institute for Medical Microbiology, Immunology and Hygiene, Amsterdam, Amsterdam, The Netherlands University of Cologne, Cologne, Germany 4 Department of Microbiology, Faculty of Medicine, Kuwait 13 Department of Microbiology, Sri Ramachandra University, Porur, University, Kuwait, Kuwait Chennai, India 5 State Key Laboratory of Mycology, Institute of Microbiology, 14 Peking University Health Science Center, Research Center for Chinese Academy of Sciences, Beijing, China Medical Mycology, Beijing, China 6 Biological Sciences Department, Faculty of Science, King Abdulaziz 15 Sun Yat-Sen Memorial Hospital, Sun Yat-Sen University, University, Jeddah, Saudi Arabia Guangzhou, China 7 Botany and Microbiology Department, Faculty of Science, Cairo 16 Shanghai Institute of Medical Mycology, Changzheng Hospital, University, Giza, Egypt Second Military Medical University, Shanghai, China 8 Fungus Testing Laboratory, Department of Pathology, University of 17 Basic Pathology Department, Federal University of Paraná State, Texas Health Science Center at San Antonio, San Antonio, TX, USA Curitiba, Paraná, Brazil Fungal Diversity formation of cellular clumps or bulbil-like structures, which sepedonioides isamemberoftheorderMelanosporales are characteristic of Papulaspora. The isolates failed to form (Davey et al. 2008), but further papulaspora-like asexual sexual fruit bodies and ascospores remained absent, which is morphs have been assigned to Ceratostoma and an unusual feature for the generally ascosporulating genera Chaetomium in the order Sordariales (Bainier 1907; Hotson Chaetomium and Subramaniula; minute conidia from 1917; Weresub and LeClair 1971;Zangetal.2004). Isolates phialides were sometimes observed. previously misidentified as P. sepedonioides are currently listed as non-sporulating Chaetomium species (Vinod Keywords Chaetomium . Desert fungi . Keratitis . Mootha et al. 2012). Papulaspora . Peritonitis . Sterile fungi . Subramaniula Recently, more attention has been paid to the non- sporulating chaetomium-like isolates that cause human infec- tion (Najafzadeh et al. 2014; Vinod Mootha et al. 2012), such Introduction as keratitis or subcutaneous infection after trauma. Despite application of molecular phylogenetic methods, researchers Melanized fungi are important causes of human infection. were unable to identify these isolates down to species level About 70 genera representing hundreds of species have been in the genus Chaetomium because of the present state of mor- implicated in human disease (de Hoog et al. 2013a;Guppy phological confusion and high phylogenetic divergence in the et al. 1998; Revankar and Sutton 2010; Revankar et al. 2002). genus. Chaetomium contains more than 300 described spe- Several main ecological groups can be distinguished. cies, but modern descriptions of most taxa are lacking, and Members of Chaetothyriales exhibit pronounced virulence very few have been circumscribed with DNA data. In the and cause deep and systemic infections in immunocompetent present concept of the genus, species that produce elaborate humans, e.g. chromoblastomycosis or brain infection (Badali sporocarps are accepted, and most species lack asexual et al. 2009; Revankar and Sutton 2010). Members of morphs (von Arx et al. 1986). Species are generally cosmo- Pleosporales are preponderantly found as degraders of plants politan and reside in soil on cellulose-rich materials or on debris or as mild opportunistic pathogens; human infections dung (Bell 2005; Carter and Khan 1982;Doveri2008;von mostly comprise traumatic inoculation of contaminated mate- Arx et al. 1986). A certain prevalence of chaetomium-like rials (Revankar and Sutton 2010). Recently, the significance species was noted in desert soil subjected to conditions of of Sordariales was underlined (Badali et al. 2011; de Hoog dryness and extremely variable temperatures (Rodríguez et al. 2013b), particularly the Chaetomiaceae whose preva- et al. 2004). Members of the madurella-clade phylogenetically lence has been underestimated because of diagnostic located inside the genus Chaetomium are typically confined to problems. areas with arid climates. Madurella species are consistent Phenotypically, the identification of clinical chaetomium- agents of human subcutaneous mycoses, and the arid areas like fungi has been difficult as a large proportion of them fail of northeastern Africa are endemic for human mycetoma to produce typical diagnostic structures in culture (Najafzadeh (Ahmed et al. 2002). Most human infections by et al. 2014; Vinod Mootha et al. 2012). Until recently, fungi chaetomium-like species concern traumatic inoculations into lacking propagation in the form of conidia were treated in the otherwise healthy humans, and rarely occur as deep infections clinical laboratory as unidentifiable ‘mycelia sterilia’ in severely immunocompromised hosts (Al-Aidaroos et al. (Pounder et al. 2007;Santosetal.2013; Vinod Mootha et al. 2007; Guppy et al. 1998; Hubka et al. 2011). 2012). Isolates forming clumps or bulbils were referred to as In the present paper we describe three novel species from Papulaspora, whereas filamentous strains from subcutaneous clinical sources that were earlier provisionally identified as infection were known as Madurella (de Hoog et al. 2013b). Papulaspora or Chaetomium species. One of the species was With the application of molecular phylogenetic multi-gene represented by seven clinical isolates particularly from the DNA sequence analyses, such isolates were found to be of Middle East, while an environmental strain was derived from high diversity being distributed to many genera and families hydrocarbon-polluted desert soil. This raises the question wheth- of ascomycetes. In addition, species proved to comprise sev- er in these fungi there is a connection between growth under arid eral sibling species that were previously thought to represent a conditions and ability to cause opportunistic infections. single taxon. For example, Madurella is now known to har- bour four species (de Hoog et al. 2012). Despite recent progress in the taxonomy of sterile fungi, the Materials and methods phylogenetic position of Papulaspora remains uncertain. The occurrence of bulbils or papulospores is non-specific and Isolates and morphology polyphyletic, as similar compact masses of cells can be pro- duced by a wide range of fungi from different genera and Strains studied were isolated from human patients, or from orders (Hotson 1917). The generic type species Papulaspora hydrocarbon-rich desert soil using enrichment under toluene Fungal Diversity atmosphere according to Zhao et al. (2010). Reference strains The run was conducted for 30,000,000 generations with sam- were obtained from the CBS reference collection (Table 1). pling every 100 generations and the ‘burn in’ was set at 25 % Morphology and colony characteristics were examined on of resulting trees. Convergence was evaluated from the two Malt Extract Agar (MEA, Oxoid, U.K.) and