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      Discovery of novel fungal species and pathogens on bat carcasses in a cave in Yunnan Province, China

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          ABSTRACT

          Virulent infectious fungal diseases, in natural and managed landscapes, are increasing. Fungal diseases in humans, animals and plants have caused die-off and extinction events and have become a threat to food security. A caving expedition in Yunnan Province, China, revealed two bat carcasses covered in fungal mycelia. Eleven fungal isolates were obtained from these bat carcasses, and morphological observations and multigene phylogenetic analyses revealed they were Fusarium incarnatum, Mucor hiemalis and Trichoderma harzianum and four new species, Mortierella rhinolophicola, M. multispora, M. yunnanensis and Neocosmospora pallidimors. One of the more alarming findings is that a number of infections related to Neocosmospora, previously associated with human and animal mycotoxicoses, are reported to be increasing, and here we present a new species from this genus, isolated from dead bats. Due to the ecosystem services provided by bats, and the close relationship between bats and humans, future research should focus on the impacts and significance of N. pallidimors to human and animal health, examining its pathogenicity and secondary metabolites. Taxonomic descriptions, color images of the habitat, in situ samples, microstructures and cultures are presented. SEM photographs of microstructures and phylogenetic trees showing the placement of new and known species are also provided.

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          Most cited references40

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          Zygomycetes in human disease.

          The Zygomycetes represent relatively uncommon isolates in the clinical laboratory, reflecting either environmental contaminants or, less commonly, a clinical disease called zygomycosis. There are two orders of Zygomycetes containing organisms that cause human disease, the Mucorales and the Entomophthorales. The majority of human illness is caused by the Mucorales. While disease is most commonly linked to Rhizopus spp., other organisms are also associated with human infection, including Mucor, Rhizomucor, Absidia, Apophysomyces, Saksenaea, Cunninghamella, Cokeromyces, and Syncephalastrum spp. Although Mortierella spp. do cause disease in animals, there is no longer sufficient evidence to suggest that they are true human pathogens. The spores from these molds are transmitted by inhalation, via a variety of percutaneous routes, or by ingestion of spores. Human zygomycosis caused by the Mucorales generally occurs in immunocompromised hosts as opportunistic infections. Host risk factors include diabetes mellitus, neutropenia, sustained immunosuppressive therapy, chronic prednisone use, iron chelation therapy, broad-spectrum antibiotic use, severe malnutrition, and primary breakdown in the integrity of the cutaneous barrier such as trauma, surgical wounds, needle sticks, or burns. Zygomycosis occurs only rarely in immunocompetent hosts. The disease manifestations reflect the mode of transmission, with rhinocerebral and pulmonary diseases being the most common manifestations. Cutaneous, gastrointestinal, and allergic diseases are also seen. The Mucorales are associated with angioinvasive disease, often leading to thrombosis, infarction of involved tissues, and tissue destruction mediated by a number of fungal proteases, lipases, and mycotoxins. If the diagnosis is not made early, dissemination often occurs. Therapy, if it is to be effective, must be started early and requires combinations of antifungal drugs, surgical intervention, and reversal of the underlying risk factors. The Entomophthorales are closely related to the Mucorales on the basis of sexual growth by production of zygospores and by the production of coenocytic hyphae. Despite these similarities, the Entomophthorales and Mucorales have dramatically different gross morphologies, asexual reproductive characteristics, and disease manifestations. In comparison to the floccose aerial mycelium of the Mucorales, the Entomophthorales produce a compact, glabrous mycelium. The asexually produced spores of the Entomophthorales may be passively released or actively expelled into the environment. Human disease with these organisms occurs predominantly in tropical regions, with transmission occurring by implantation of spores via minor trauma such as insect bites or by inhalation of spores into the sinuses. Conidiobolus typically infects mucocutaneous sites to produce sinusitis disease, while Basidiobolus infections occur as subcutaneous mycosis of the trunk and extremities. The Entomophthorales are true pathogens, infecting primarily immunocompetent hosts. They generally do not invade blood vessels and rarely disseminate. Occasional cases of disseminated and angioinvasive disease have recently been described, primarily in immunocompromised patients, suggesting a possible emerging role for this organism as an opportunist.
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            SplitsTree: analyzing and visualizing evolutionary data.

            D Huson (1998)
            Real evolutionary data often contain a number of different and sometimes conflicting phylogenetic signals, and thus do not always clearly support a unique tree. To address this problem, Bandelt and Dress (Adv. Math., 92, 47-05, 1992) developed the method of split decomposition. For ideal data, this method gives rise to a tree, whereas less ideal data are represented by a tree-like network that may indicate evidence for different and conflicting phylogenies. SplitsTree is an interactive program, for analyzing and visualizing evolutionary data, that implements this approach. It also supports a number of distances transformations, the computation of parsimony splits, spectral analysis and bootstrapping.
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              Genealogical concordance between the mating type locus and seven other nuclear genes supports formal recognition of nine phylogenetically distinct species within the Fusarium graminearum clade.

              Species limits were investigated within the Fusarium graminearum clade (Fg clade) through phylogenetic analyses of DNA sequences from portions of 11 nuclear genes including the mating-type (MAT) locus. Nine phylogenetically distinct species were resolved within the Fg clade, and they all possess contiguous MAT1-1 and MAT1-2 idiomorphs consistent with a homothallic reproductive mode. In contrast, only one of the two MAT idiomorphs was found in five other species, four of which were putatively asexual, and the other was heterothallic. Molecular evolutionary analyses indicate the MAT genes are under strong purifying selection and that they are functionally constrained, even in species for which a sexual state is unknown. The phylogeny supports a monophyletic and apomorphic origin of homothallism within this clade. Morphological analyses demonstrate that a combination of conidial characters could be used to differentiate three species and three species pairs. Species rank is formally proposed for the eight unnamed species within the Fg clade using fixed nucleotide characters.
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                Author and article information

                Journal
                Emerg Microbes Infect
                Emerg Microbes Infect
                Emerging Microbes & Infections
                Taylor & Francis
                2222-1751
                9 July 2020
                2020
                : 9
                : 1
                : 1554-1566
                Affiliations
                [a ]CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Science , Kunming, Yunnan, People’s Republic of China
                [b ]State Key Laboratory for Conservation and Utilization of Bio-Resources in Yunnan, Yunnan Agricultural University , Kunming, People’s Republic of China
                [c ]Yunnan Research Institute for Local Plateau Agriculture and Industry , Kunming, People’s Republic of China
                [d ]Key Laboratory for Agro-biodiversity and Pest Control of Ministry of Education, Yunnan Agricultural University , Kunming, People’s Republic of China
                [e ]Energy and Resources Group, University of California , Berkeley, CA, USA
                [f ]World Agroforestry Centre , Kunming, Yunnan, People’s Republic of China
                [g ]Centre for Mountain Futures, Kunming Institute of Botany , Kunming, Yunnan, People’s Republic of China
                [h ]Center of Excellence in Fungal Research, Mae Fah Luang University , Chinag Rai, Thailand
                [i ]Department of Biology, Faculty of Science, Chiang Mai University , Chiang Mai, Thailand
                [j ]Center of Excellence in Microbial Diversity and Sustainable Utilization, Faculty of Science, Chiang Mai University , Chiang Mai, Thailand
                [k ]Academy of Science, The Royal Society of Thailand , Bangkok, Thailand
                Author notes
                [CONTACT ] Peter Edward Mortimer peter@ 123456mail.kib.ac.cn CAS Key Laboratory for Plant Diversity and Biogeography of East Asia, Kunming Institute of Botany, Chinese Academy of Science , Kunming 650201, Yunnan, People’s Republic of China Centre for Mountain Futures, Kunming Institute of Botany, Kunming650201, Yunnan, People’s Republic of China
                [†]

                Equal contribution.

                Article
                1785333
                10.1080/22221751.2020.1785333
                7473127
                32573334
                a6a132f6-3121-4772-8d3c-2b409df2f596
                © 2020 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group, on behalf of Shanghai Shangyixun Cultural Communication Co., Ltd

                This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                History
                Page count
                Figures: 6, Tables: 1, Equations: 8, References: 63, Pages: 13
                Categories
                Research Article
                Articles

                4 new taxa,fusarium incarnatum,mucor hiemalis,mortierella rhinolophicola,mortierella yunnanensis,mortierella multispora,neocosmospora pallidimors,trichoderma harzianum

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