Australian Dust Storm Associated with Extensive Aspergillus sydowii Fungal “Bloom” in Coastal Waters

Abstract

A massive central Australian dust storm in September 2009 was associated with abundant fungal spores (150,000/m 3 ) and hyphae in coastal waters between Brisbane (27°S) and Sydney (34°S). These spores were successfully germinated from formalinpreserved samples, and using molecular sequencing of three different genes (the large subunit rRNA gene [LSU], internal transcribed spacer [ITS[, and beta-tubulin gene), they were conclusively identified as Aspergillus sydowii, an organism circumstantially associated with gorgonian coral fan disease in the Caribbean. Surprisingly, no human health or marine ecosystem impacts were associated with this Australian dust storm event. Australian fungal cultures were nontoxic to fish gills and caused a minor reduction in the motility of Alexandrium or Chattonella algal cultures but had their greatest impacts on Symbiodinium dinoflagellate coral symbiont motility, with hyphae being more detrimental than spores. While we have not yet seen any soft coral disease outbreaks on the Australian Great Barrier Reef similar to those observed in the Caribbean and while this particular fungal population was non-or weakly pathogenic, our observations raise the possibility of future marine ecosystem pathogen impacts from similar dust storms harboring more pathogenic strains. F ungi are rarely described for marine environments and are mainly considered terrestrial life forms. This may reflect a bias by fungal researchers but more likely relates to fungal cell biology. Fungi thrive in nutritionally rich environments, such as on plant or animal hosts and in soils, sediments, and detritus, where their enzymes break down complex biological polymers, allowing osmotrophic uptake of nutrients (1). During the 3 days following 22 September 2009, after a severe 10-year drought, a massive dust plume originating in the Australian Lake Eyre Basin swept eastward, reaching a width of 500 km and a length of 5,500 km before it traversed the Tasman Sea to reach New Zealand (Fig. 1A). Airports on the east coast of Australia were temporarily closed, and visibility was limited in some areas to Ͻ50 m. About 16 Tg of dust was stripped from central Australia, with 75,000 tons/h estimated to have crossed the New South Wales coast (2). Dust that originates in deserts is well known to be a vehicle for the spread of microbial communities and a concern for accidental spread of contaminants and diseases (3). The supply of dust-derived nutrients to the global ocean is also postulated to be a key control on marine primary production (4). In the wake of this dust event, we screened Continuous Plankton Recorder (CPR) samples for potential impacts on coastal phytoplankton communities. Unexpectedly, we discovered massive concentrations of 4-or 5-mdiameter black spinose fungal spores and hyphae in coastal samples collected between Brisbane and Sydney from 16 to 20 Oct 2009 (up to 150,000 spores per m 3 ). The formalin-preserved plankton recorder silks, which were returned to the lab within 10 days after towing, appeared black, as if ...

Characterisation of the major dust storm that traversed over eastern Australia in September 2009; a multidisciplinary approach

“…Our sampling techniques were not appropriate for the analysis of fungal spores, but a recent study by Hallegraeff et al (2014), who analysed samples of the Red Dawn dust storm collected at sea between Brisbane and Sydney (Fig. 1), found high concentrations of Aspergillus sydowii fungal spores, similar to those found to be responsible for outbreaks of sea fan disease in the Caribbean Griffin and Kellogg, 2001).…”

The roles of endolithic fungi in bioerosion and disease in marine ecosystems. II. Potential facultatively parasitic anamorphic ascomycetes can cause disease in corals and molluscs

“…The possible role of secondary metabolites in disease caused by A. sydowii and some of the other fungi isolated by Hallegraeff et al (2014) have been studied further by Hayashi et al (2016). They exposed small numbers of cells from cultures of three clades of Symbiodinium to extracts and purified compounds from culture media after growth of A. sydowii .…”

“…The substrates include living and dead plant and animal hosts, body parts and detritus in soils, sands and sediments (Burge et al 2013). When the substrates dry out, fungi characteristically form conidia and release clouds of spores into the air, which can be significant components of dust storms formed in deserts such as in Africa (Weir-Brush et al 2004) and in Australia (Hallegraeff et al 2014). Dust storms can therefore be an important mechanism for dispersal of spores from terrestrial into aquatic environments.…”

“…Spores of these fungi often germinate easily, and the growth patterns of these fungi cause the formation of fungal blooms which can include floating rafts of hyphae in coastal marine ecosystems (Hallegraeff et al 2014), especially with high nutrient content (Zverev and Vysotskaya 2005), i.e. high concentrations of utilisable organic compounds dissolved in water, formed during the process of eutrophication.…”

Aspergillus sydowii and Other Potential Fungal Pathogens in Gorgonian Octocorals of the Ecuadorian Pacific

“…sydowii is globally distributed and occurs in diverse environments where it survives as a soil decomposing saprotroph [17–19]. It is apparently a terrestrial fungus, but it is salt tolerant and capable of growing in the sea [20]. Moreover, A .…”