Research Article: From Dandruff to Deep-Sea Vents: Malassezia-like Fungi Are Ecologically Hyper-diverse

Date Published: August 21, 2014

Publisher: Public Library of Science

Author(s): Anthony Amend, Joseph Heitman.


Partial Text

As the dominant component of the mycobiota on human skin [1] —both healthy and diseased [2] —the genus Malassezia has received a fair amount of attention. Since the middle of the 19th century, researchers have linked these fungi with skin maladies such as dandruff and eczema [3], but their difficulty to culture axenically long hampered studies of their systematics and diversity [4]. Malassezia is the sole genus within the fungal order Malasseziales, contained within the proposed subphylum Malasseziomycetes (anonymous reviewer; personal communication). Although Malassezia is sister to the so-called “smut” plant pathogens, they are markedly divergent in ecological terms. A hallmark of Malassezia species is their incomplete fatty acids synthesis metabolic pathway, and reliance, instead, on a suite of extracellular lipases, phospholipases, and acid sphingomyelinases [5]. In fact, only a single species, M. pachydermatis, is able to survive in axenic culture lacking lipid amendment [6].

Despite being difficult to cultivate, putative Malassezia are readily detected in environmental DNA samples using standard fungal “barcoding” approaches. Scanning GenBank and the scientific literature, therefore, is useful for approximating occurrence patterns. DNA sequences identical to M. globosa and M. restricta, which are both well characterized as human skin associates, appear to be cosmopolitan. M. restricta may be particularly widespread, and DNA sequences similar to these species have been detected in habitats as diverse as deep-sea sediments [7], hydrothermal vents [8], stony corals [9], lobster larval guts [10], Japanese Eel (Anguilla japonica) gut and muscle tissue [11], Antarctic soils [12], [13], on the exoskeleton of soil nematodes [14], and various plant roots including mycoheterotrophic species such as orchids (e.g., [15]). Remarkably, the ribosomal DNA sequences of Malassezia in these studies are nearly identical to those of human associates, suggesting either a very recent divergence in habitat or else that these organisms are highly tolerant to some of the planet’s most extreme environments. Unsurprisingly, Malassezia sequences are not uncommon in studies of human dwellings [16], where human skin contributes substantially to house dust.

The evolutionary origins of marine Malassezia and their relatedness to better- characterized terrestrial species is a matter of speculation. A phylogeny compiled from environmental samples and sequenced isolates (Figure 1) demonstrates a tremendous amount of phylogenetic novelty contained within and adjacent to the Malassezia lineage. Evidence from both large and small subunit loci of the ribosomal cistron demonstrate well-supported clades from various environments, including a large monophyletic group of marine water column mycoplankton, sequences from separate studies of marine anoxic environments, and combinations of host-associated (coral and coralline algae) Malassezia that group with presumably free-living taxa in various marine and terrestrial habitats. The relatively long branch lengths separating some of these isolates from their sister taxa suggest either a particularly rapid diversification, or, alternatively, that intermediate taxa remain to be sampled and sequenced.

The tremendous diversity of habitats in which Malassezia-like organisms are found suggests that marine species of this group may incorporate a spectrum of trophic strategies ranging from saprotrophy to biotrophy. Resident Malassezia-like organisms on seemingly healthy coral and sponge hosts may be commensals, latent pathogens awaiting host immunosuppression, or both, depending on host and environmental context. A study of crustose coralline algae around Palmyra Atoll found that a Malassezia phylotype was abundant in banding disease lesions [20]. Incidence of the disease increased by an order of magnitude following an el Niño event. A laboratory manipulation study showed that disease virulence correlated with an interaction between increases in CO2 and temperature. Despite efforts, the authors were unable to cultivate the fungus, and it remains to be tested if Malassezia is the cause or merely a symptom of the banding disease. Nevertheless, the study presents the possibility that a putative Malassezia may act as a pathogen in nonmammal hosts under certain environmental contexts. The high incidence and virulence of the disease raises the possibility that when combined with environmental perturbations, marine Malassezia may even exert bottom-up control on reef community structure.

Given the high incidence of Malassezia species on human skin [1], [2], a healthy skepticism is warranted since mammalian skin cells from terrestrial sources could potentially accumulate in marine samples, or contamination by lab personnel could result in false positives. Potential for contamination is particularly high when environmental DNA sequences are generated using sensitive, high-throughput methods. Nevertheless, multiple lines of evidence support the position of Malassezia-like organisms as true marine residents. Edgcomb and colleagues [21] reported a high proportion of Malassezia-like sequences in deep-sea sediments detected by sequencing environmental RNA. Because single stranded RNA degrades quickly in situ, its presence supports the notion of active growth as opposed to DNA “contamination” in this habitat. Furthermore, the RNA sequences were distinct from those of any organism known to associate with mammalian hosts, excluding the possibility of lab contamination. A follow-up study using even more stringent protocols and negative controls to exclude exogenous nucleic acids detected Malassezia-like sequences in samples located at depths of 1.6 and 45.1 meters below the sea floor [22]. Fungal community composition overall was highly correlated with site geochemistry, suggesting the environmental selection of a metabolically active assemblage. Similarly, an analysis of actively transcribed genes (mRNA) from a coral habitat identified components of multiple metabolic pathways allied with sequenced Malassezia genomes [9] —further evidence that these fungi are alive and metabolically active underwater. The fact that Malassezia-like organisms are frequently found in remote marine locations far from humans (e.g., [7], [8], [21], [23]–[27], and many others) also renders the terrestrial input hypothesis less likely.

The remarkable environmental plasticity of M. restricta lends itself to population-level studies of adaptation and acclimatization among the Earth’s most extreme environments. How do differences in gene content and transcription correlate with residence in arctic soils versus deep-sea vents? What traits mark the transition from saprobic to pathogenic lifestyles? How many times has a marine (or terrestrial) lifestyle evolved independently?

Analysis of environmental sequences demonstrates that putative members of the Malassezia lineage likely rank among the most widespread fungi on the planet. They are found in a startling diversity of habitats and locations, from polar regions to deep-sea vents. Malassezia-like species appear to dominate certain marine habitats, which should most certainly be the focus of future research into the diversity and distribution of this enigmatic group. Clearly, considering Malassezia a mere epidermis-commensal is a definition that is only skin deep.