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Review Article | Open Access | Eur. J. Med. Health Sci., 4(2), 64-69 | doi: 10.34104/ejmhs.022.064069

Ustilaginales (Smut Fungi) and their Role in Causing Human Infections, an Update

Harish C Gugnani* Mail Img

Abstract

Ustilaginales is also known as smut fungi are a vast and diverse group of fungi that cause disease in crops causing huge losses worldwide. They belong to the class Ustilaginomycetes. Several members of this group serve as valuable models for unraveling the fundamental mechanisms controlling important biological processes. Several plant pathogenic species of ustilaginales are known to cause human infections. A brief description is given of the genera that contain species pathogenic to humans. The life cycle of Mycosarcoma (Ustilago) maydis is briefly described. The phenomenon of dimorphism in Mycosarcoma maydis is discussed in comparison to a plant pathogenic fungus, Taphrina deformans. Mycosarcoma maydis was the first plant pathogenic fungus known to cause human infection in a 31-years old corn farmer. There are over twenty species of ustilaginales implicated in human infections. This paper reviews the infections caused by Mycosarcoma (Ustilago) maydis, Psudozyma species, viz. Psuedozyma aphidis, P. antartica, P. parantarctica, and P. thialandica, and Dirkmeia churashimaensis

INTRODUCTION

True fungi are a very diverse group of organisms with 1, 4800 described species, and the estimated number is 2.2-3.8 million species with diverse ecological niches and immense economic importance (Hawksworth & Lücking, 2017). The fungi comprise seven phyla: Chytridiomycota, Blastocladiomycota,   Neocallimast-igomycota, Microsporidia, Glomeromycota, Asco-mycota, and Basidiomycota. Ustilaginales belong to the Phylum Basidiomycota, Subphylum Ustilagino-mycotina, Class Ustilaginomycetes, subclass Ustila-ginomycetidae, Ustilaginales comprise 8 families, 49 genera, and 851 species (Kirk et al., 2008). They mostly infect angiosperms, often causing diseases of economic importance, especially in cereals, and form masses of dark, powdery spores in the leaves, stems, flowers, or fruits of the host plants (Allaby, 2013). Ustilaginales cause smut of many cereal grains, in-cluding wheat, barley, corn, and rice; masses of spores (sori) are usually black and dusty; basidial apparatus consisting of thick-walled teleutospore (probasidium), which upon germination gives rise to a septate or non-septate tube (metabasidium) bearing teliospores also known as chlamydospores (Martinez-Espinoza et al., 2002) Several species of this group serve as excellent models for studying mating, morphogenesis, sign, DNA signal transduction, nycoviruses, DNA recom-bination, pathogenicity, and genomics (Martinez-Espinoza et al., 2002; Wang et al., 2015; Kruse et al., 2017). 

Important plant pathogenic species include Ustilago nuda causing smut of barley (Hordeum vulgare). Ustilago maydis, causal agent of corn smut is now classified with a new generic name as Myosarcoma maydis (Taggart et al., 2016). Human infection caused by a novel pathogen Dirkmeia churrashimaensis has been very recently described (Hu et al., 2021). This species was formerly identified as a novel Pseudozyma species on the basis of morphological and physiologic aspects and by molecular analysis of the D1/D2 domains and internal transcribed spacer (ITS) regions (Hu et al., 2021). This species formerly known as Pseudozyma churashimaensis is known to produce glycolipid biosurfactants, mannosylerythritol lipids but it has so far not been known to cause a plant disease (Morita et al., 2011). Two new species of Pseudo-zyma, viz. P. parantarctica and P. thailandica have also been described (Sugita et al., 2003).

During the past six decades, numerous cases of human infections with a varying clinical spectrum caused by a great variety of plant pathogenic fungi belonging to several taxonomic groups have been reported world-wide (Nucci & Anaissie, 2007; Pastor & Guarro, 2008; Gauther and Keller, 2013; Revankar & Sutton, 2010, de Hoog et al., 2019). There has been an earlier review of human infections caused by plant patho-genic fungi including ustilaginales (Gugnani et al., 2021).

Brief descriptions of genera that have species patho-genic for humans - Ustilago: It is basidiomycetous yeast that inhabits the soil and plant material. It is a pathogen of seeds and flowers of cereals, wheat, corn, and grasses. There are only a few reports of human infections caused by Ustilago. Species of Ustilago grow slowly on agar media as moist, cream to yellow-colored and yeast-like colonies becoming wrinkled and membrane-like with profuse budding in the medium within 20 days (Martinez-Espinoza et al., 2002). Microscopically spindle-shaped, elongate, and irregular blastoconidia consisting of spindle-shaped cells are observed. Pseudohyphae and short true hyphae with clamp connections may occasionally be present (Martinez-Espinoza et al., 2002). Ustilago maydis is a host-specific pathogen, being the causal agent of common smut or "huitlacoche" in maize (Zea mays), and its possible ancestor, teozintle (Zea mays ssp. parviglumis and ssp. mexicana). Nevertheless, in contrast to other Ustilaginales that are responsible for severe epiphytics in important harvests, U. maydis infections are sparse infecting a low number of corn plants (Martinez-Espinoza et al., 2002; Wang et al., 2015). Curiously infected ears are edible, and extre-mely appreciated as a delicacy in México, and in modern international cuisine (León-Ramírez et al., 2014). The first three records of human infection caused by Ustilagomyadis (now called Mycosarcoma maydis) were from Hungary (Randhawa et al., 1959), U.S.A. (Moore et al., 1946), and India (Randhawa et al., 1959), Mycosarcoma (Ustilago) maydis is also known to cause respiratory allergy and mycotoxicois (Wołczańska & Szysz, 2018), cases of these diseases will not be described in this review as it deals with infections. Dirkmeia (Pseudozyma) churashimaensis has been used as a leaf colonizing agent for systemic defense of pepper against bacterial and viral pathogens (Lee et al., 2017). Human pathogenic species of ustilaginales include Myosarcoma (Ustilago) maydis, Psueudozyma phidis, P. antartica, P. parantarctica, P. thialandica and Dirkmeia churashimaensis. Very re-cently, a cluster of 12 cases of fungemia in pre-term neonates caused by D. churshimaensis among NICU patients in a multispecialty hospital in Delhi, India has been described (Chowdhary et al., 2020). The authors used whole-genome sequencing (WGS) and amplified fragment-length polymorphism typing and matrix-as¬sisted laser de-sorption/ionization time-of-flight mass spectrometry by using Biotyper 3.1 to understand the genetic relatedness of the isolates and to identify them as Dirkmeia churanshimaensis

The present study describes the details of clinical features of some of the cases not given in this review and provides a further update of human infections caused by different plant pathogenic species of ustilaginales, and human infections caused by Dir-kmeia churashimaensis.

RESULTS

The literature search revealed many reports of human infections caused by several species plant pathogenic ustilaginaceous fungi belonging to the genera Myo-sarcoma, Psudozyma, Moesziomyces, and Dirkmeia in different countries. A noteworthy observation was the report of a case of human infection due to Moeszio-myces bullatus (formerly called Pseudozyma bullatus) from Nigeria (Okolo et al., 2015), constituting the first world record of human infection caused by this species. Two new species of Pseudozyma, viz. Pseu-dozyma antarctica and P. thailandica were found to have been discovered in 2003 (Sugita et al., 2003), Sequencing of the internal transcribed spacer 1 (ITS1)-5.8S-ITS2 region of the rRNA gene was used in the identification of some fungi in some of the publications covered in this review (Wang et al., 2015; Kruse et al., 2017; McTaggart et al., 2016; Chow-dhary et al., 2020; Okolo et al., 2015).

DISCUSSION

The literature search revealed data on human cases of infections caused by different species of ustilaginales in India, Pakistan, China, Japan, the US, Hungary, and Nigeria. The Nigerian case caused M. bullatus cons-tituted the first world record of human infection caused by this species This species is also reclassified as A. thaliana (The yeast form of M. bullatus is known to infect grasses and leaves flowers and fruits of other plants (Eitzen et al., 2021) It may be relevant to mention that the case of brain tumor due to Myco-sarcoma maydis reported by Randhawa et al in 1959 from Delhi, India was the first world record of human infection caused by a plant pathogenic fungus.

Table 1: Demographic and salient clinical features of human infection caused by different species of Ustilaginales.

Meaning of medical terms and abbreviations

Dermatomycosis: Fungal infection of the skin; Lep-tomeningitis: Inflammation of the pia mater and the arachnoid membrane of the brain; Cystic arach-noiditis: Fluid-filled sacs that occur on the arachnoid membrane that covers the brain and the spinal cord, Ependymitis: Inflammation of the cerebral ventricular system; Cerebral craniotocasesmy: a surgical proce-dure in which a part of the skull is temporarily re-moved to perform an intracranial procedure 

CONCLUSION

A noteworthy finding in our review was the report of a cluster of 12 cases of fungemia in pre-term neonates caused by D. churashimaensis among NICU patients in a multispe¬cialty hospital in Delhi (Chowdhary et al., 2020), constituting the first known record of human infection due to this fungus; Another noteworthy observation in our literature search was a case of mycetoma in 51 yrs-old male in China caused by coinfection of Pzeudozyma aphdis and Nocardia oititidiscaviarum (Chen et al., 2011). Cereal crops likely maize, wheat, barley, pearl millet are often infected with smut fungi, which may cause infection in persons encountering these plants. Thus, there is a need for surveillance of the occurrence of infections in supervisory staff and workers engaged in the culti-vation of these crops.

ACKNOWLEDGEMENT

We thank our colleagues for their moral support and guidance.

CONFLICTS OF INTEREST

I have no conflict of interest with any individual or organization 

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Article Info:

Academic Editor 

Dr. Abduleziz Jemal Hamido, Deputy Managing Editor (Health Sciences), Universe Publishing Group (UniversePG), Haramaya, Ethiopia.

Received

February 27, 2022

Accepted

April 4, 2022

Published

April 11, 2022

Article DOI: 10.34104/ejmhs.022.064069

Corresponding author

Harish C Gugnani*

Professor, Department of Microbiology (Retired), Vallab-hbhai Patel Chest Institute, University of Delhi, Delhi-110007, India.

Cite this article

Gugnani HC. (2022). Ustilaginales (Smut fungi) and their role in causing human infections, an update. Eur. J. Med. Health Sci., 4(2), 64-69. https://doi.org/10.34104/ejmhs.022.064069 

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