Mucor hiemalis Wehmer 1903

Characteristics of the genus are as follows:

“Mucor species produce nonapophysate sporangia that have a wet or dry wall when mature. The sporangia are more or less globose and all of the same type. The sporangiophores are simple or branched and they arise directly from the substrate; stolons and rhizoids are not formed. Zygospores, where known, have more or less equal, opposed, non-appendaged suspensors.”

The complete description, originally defined by Wehmer 1903 and expanded upon by Hoog et al. is as follows:

oColonies (MEA) expanding, greyish-ochraceous.

oSporangiophores hyaline, up to 15 mm high, up to 14 mm wide, erect, unbranched at first, later sparingly branched. Sporangia yellowish at first, becoming dark brown, up to 80 mm in diameter with diffluent membranes; columellae ellipsoidal, spherical when young, up to 38 x 30 mm. Sporangiospores ellipsoidal, sometimes flattened at one side, 5.7-8.7 x 2.7-5.4 mm, smooth-walled. Oidia present in substrate hyphae.

oZygospores up to 100 mm diameter, roughened with long spines, blackish-brown.

oSuspensors equal or nearly equal. Heterothallic.

oMaximum growth temperature 30°C. Nitrate negative. Mostly no thiamin required.

The distinguishing factor for M. hiemalis from the rest of the genus are sporangiophores unbranched or weakly branched and sporangiospores ellipsoidal, 5.7-8.7 x 2.7-5.4 µm (Alvarez 2011).

Mucor hiemalis is primarily a soil-borne fungus associated with decomposing leaf litter but has also been found to be saprotrophic or parasitic on animal and plant materials (Costa et al. 1990). Studies have found this fungus growing on porcupine dung, bear dung, horse dung, woodchuck dung, moldy bones in the woods, sandy wood soil surfaces, and soil in mixed woods (Povah 1917).

It has been found in a wide range of habitats and plant materials including on bog and fen in southern boreal forests in Alberta, Canada (Thormann et al. 2003), in Michigan habitats and throughout Europe (Povah 1917, Budziszewska 2010), and throughout England (Parkinson 1960).

Mucor hiemalis was found to be present in soil samples in a variety of studies. It is noted to impact soil respiration but the direct effect is unknown as it is based upon interactions with other microflora and energy sources (Anderson and Domsch 1973).

M. hiemalis reproduces asexually via sporangiospores 3-5 μm in diameter. Alternatively, the fungus can reproduce vegetative from mycelial fragments. These fragments are more viable at high sucrose concentrations rather than low concentrations, at temperatures of 25-30 C, at neutral pH, and with low concentrations of cadmium ions (Ivanova and Marfenina 2001).

Hoque and Fritscher found a unique anaerobic M. hiemalis strain (EH11) present in a biofilm layer in a pristine spring in Germany under heavily methanic conditions (2017). M. hiemalis has been found to grow by fermenting sugars anaerobically or under anearobiosic condtions in which the fungus ferments substrates in polluted areas with low oxygen. M. hiemalis strain EH11 comprised 10% of the biofilms present on rocks in the spring. Hoque and Fritscher’s report is the first to find unusual morphological characteristics of M. hiemalis including the following:

“Variation in morphology ofM.hiemalisEH11 under strict anaerobic culture conditions (e-donor: cellobiose, e-acceptor: nitrate). (a) Formation of dense material (dc, arrows) in nonseptate hyphae, (b) initialization of septate formation, cell division, cell swelling, thickening of intracellular materials in sporangium-like formations of EH11 (arrows near a jute fiber, J) under strict anaerobic conditions imaged by transmission differential contrast microscopy, (c) strong cell division, cell swelling, initialization of pseudosporangiospores, and detachment of intracellular pseudosporangium (Sp) instead of terminal sporangium release as observed by differential contrast microscopy, (d). Release and ripening of detached cells (S, pseudosporangium) as well as intracellular division into numerous pseudosporangiospores within the pseudosporangia.”

EH11 was shown to change its metabolism under strictly anaerobic conditions to that of chemoautotropic bacteria, utilizing nonfermentive metabolism reducing Fe (III) to Fe (II) (Hoque and Fritscher 2017). It is posited that the fungus also provides structural support for the other microorganisms living within its matrix on rocks in springs.

M. hiemalis may have use as a bioremediant for removing cyanotoxins from contaminated aquatic environments. Pflugmacher demonstrated that in culture, M. hiemalis growth is not deterred by the presence of three cyanobacterial toxins, “MC-LR, BMAA and CYN, for up to seven days at concentrations ranging from 5-1000 μg/L” (2015). The fungus uptakes these toxins and effectively removes them from the environment while possibly using carbon from secondary cyanobacterial metabolites for energy. (Pflugmacher 2015).

M. hiemalis strain EH8 growing anaerobically and aquatically has the capacity to remove mercury from water within 10-48 hours after initial exposure to Hg(II) under low temperatures and sulfur reducing conditions (Hoque and Fritscher 2016). Further studies have also identified M. hiemalis’s potential for use in removing Ni (II) (Shroff and Vaidya 2011) and Cr (VI) from the environment and found that the fungus retains its capacity to remove these heavy metals for several sorption and desorption cycles (Tewari et al. 2005). Additionally, Hoque and Fritscher found that the EH11 strain “fixed more than 80% of the applied ionic metals (Al 98.9%, Cd 80.3%, Co 80.6%, Cr 89.5%, Cu 87.2%, Ni 82.1%, Pb 97.1%, Zn 83.6%) on the spore surfaces” (2017).

M. hiemalis is significant commercially in countries manufacturing fermented soybean products. Recent studies have found Mucor hiemalis to be present in traditional fermented Asian products, including Sufu Pehtze (Chinese molded tofu) and traditional Korean meju used as a starter for soy sauce (Han et al. 2004, Hong et al. 2011).

Uricase is vital to nitrogen metabolism, is used to measure uric acid in blood and other biological fluids, and has been effective in treating hyperuricemia, gout, prophylaxis, and tumor lysis hyperuricemia (Bomalaski and Clark 2004). M. hiemalis has been shown to produce a significant amount intracellular uricase over 24 h in a simple medium of pH 6.0, illustrating potential for use in clinical settings. (Yazdi et al. 2006).

M. hiemalis is found to produce ethylene in pure culture in the presence of available oxygen (Primrose 1976).

Phylogenetic studies are still uncertain as to the placement of the family Mucoraceae and as a result, also M. hiemalis. O’Donnell et al. constructed a most-parsimonious tree of the 13 families of the order Mucorales and found little support for previously established placement based on sexual morphology, establishing that Mucor is a polyphyletic group (2001).

Phylogenetic placement of this fungus in particular is still under debate. In 1973, Schipper had described four f. sp. within Mucor hiemalis: “M. hiemalis f. hiemalis, M. hiemalis f. silvaticus, M. hiemalis f. corticolus and M. hiemalis f. luteus. M. genevensis is the homothallic counterpart of M. hiemalis.”

More recently, in 2010, Budziszewska et al. have posited that M. hiemalis f. luteus should be delineated as its own species separate from M. hiemalis based upon noted differences phylogenetically and morphologically. Additionally, they advocate transferring the M. hiemalis group from the Mucor genus entirely, as M. hiemalis does not form a monophyletic clade with the type species of the genus, M. mucedo (Budziszewska et al. 2010).

Other studies have found Mucor hiemalis and its f. sp. to be phylogenetically distant from other species within Mucor (Han et al. 2004), most particularly Mucor flavus and Mucor hiemalis more distant from other members of the genus. with Mucor hiemalis forming a clade with the type of Rhizomucor variabilis var. variabilis, corroborating other recent findings regarding this placement (Alvarez 2011).

Close relatives of the fungus include Mucor irregularis (=Rhizomucor variabilis) which was reclassified in 2011 due to its close phylogenetic relationship with Mucor hiemalis (Budziszewska et al. 2010, Voigt et al. 1999). Furthermore, Budziszewska et al. suggest placement of Rhizomucor variabilis as a f. sp. of M. hiemalis (Budziszewska et al. 2010). The noted differences between M. irregularis and M. hiemalis are that the former produces rudimentary rhizoids. Further research is required to determine the variances between the two as the presence of rhizoids in M. irregularis is not a consistent taxonomic feature (Alvarez et al. 2009).

Several members of the Mucorales order, most commonly Rhizopus and Mucor, are capable of causing mucormycosis (previously called zygomycosis) in humans (Roden et al. 2005). Mucormycosis is a rare fungal infection that mostly impacts immunocompromised individuals following inhalation of spores. The infection can also be contracted on the skin after entering the epidermal tissue through a cut, scrape, or burn: This is the primary way that the infection impacts non-weakened immune system individuals (Center for Disease Control 2015).

Mucor hiemalis is not commonly attributed as the causal agent of mucormycosis, likely due to its low temperature tolerance of 33 C (Lu X-L et al. 2013). However, there have been three reports of this fungus causing cutaneous mucormycosis, all of which impacted immunocompetent individuals. Additionally, there is one case of the fungus infecting an individual subcutaneously in contrast to prior belief that the fungus only infected cutaneous tissue on healthy individuals (Desai 2013).

Cutaneous mucormycosis accounts for approximately 10% of mucormycosis events while it is posited that previous cases have been underestimated (Oliveira-Neto et al. 2006). General cutaneous symptoms of mucormycosis include “blisters or ulcers, and the infectioned area may turn black. Other symptoms include pain, warmth, excessive redness, or swelling around a wound” (For a list of full symptoms, visit the Center for Disease Control website - https://www.cdc.gov/fungal/diseases/mucormycosis/symptoms.html).

Mucormycosis caused by M. hiemalis is marked by “superficial lesions having only slightly elevated circinate and squamous border resembling tinea corporis” (Paes Oliveira-Neto et al. 2006, Prevoo et al. 1991). In one case, there was no identifying trigger event prior to the development of the lesions over the course of 5 years, and in the Prevoo case, the patient attributed infection possibly to an insect bite and the infection evolved over approximately 10 months. In both cases, the patient was a healthy young female, which is in contrast to most cases of mucormycosis which occur in heavily diabetic or immune-compromised individuals.

Mucor hiemalis is a fungus within the order Mucorales. The genus Mucor contains 39 species of fungi and are typically associated with leaf litter or saprobic activity on animal dung. M. hiemalis was first described by C. Wehmer in 1903, with distribution from the arctic and alpine soils to the tropics, in Europe and the Americas (Domsch 1980).

Mucor hiemalis is known to occasionally cause mucormycosis in humans (Center for Disease Control 2015) and is now being studied for its potential use in bioremediation (Hoque and Fritscher 2016, 2017).

The fungus is also significant to countries manufacturing fermented soybean products (Han et al. 2004, Hong et al. 2011)and is known to produce intracellular uricase which may have applications in clinical settings (Yazdi et al. 2006).

Mucor hiemalis is among the zygosporic fungi found in unspoiled foods. It has different industrial importance as biotransforming agents of pharmacological and chemical compounds.