Origins of sea fan aspergillosis

Infectious disease outbreaks are a major cause of coral loss and reef degradation.  Evidence from paleontological studies and ecological monitoring indicate that coral disease prevalence, variety, and host range have all increased over the last 30 years.  But what is the origin of coral pathogens?  Even in the few cases where the causal pathogen has been identified, we don’t know where it came from, if it is new or newly introduced or whether it was always present on reefs, but only recently became virulent due to a mutation or environmental change.

Identifying the source of coral pathogens is a key goal of coral disease ecology with obvious importance for disease mitigation and reef management.  Coral pathogens could originate in terrestrial habitats and be introduced to the ocean following deforestation and soil runoff.  They could also be added via sewage outfalls, transported from faraway reefs in the ballast water of cargo ships, and might even be spread within and among regions by human travel.

A pair of exciting new studies clarifies the origins of sea fan aspergillosis, a major Caribbean epizootic caused by the pathenogenic fungus Aspergillus sydowii.  In the first paper, Rypien et al. (2008) used molecular markers to determine patterns of relatedness among strains of Aspergillus sydowii collected from a variety of hosts and environments. Specifically, they tested four hypotheses:

1) The Endemic Marine Hypothesis predicts that corals are infected by fungus that is native to marine habitats and therefore phylogenetically distinct from nearby terrestrial isolates.

2) The Terrestrial Runoff Hypothesis predicts that isolates from diseased corals will be most closely related to terrestrial isolates from nearby landmasses.

3) The single-origin African Dust Hypothesis predicts that isolates will have reduced genetic diversity and allelic richness, with evidence of a recent bottleneck in coral disease-causing isolates. This hypothesis also predicts that isolates will be most closely related to terrestrial isolates from Africa.

4) The multiple origins African Dust Hypothesis predicts no evidence of a recent bottleneck, with disease-causing isolates being most closely related to terrestrial isolates from Africa.

Their results essentially refute all four hypotheses and reveal a pattern of global panmixia and multiple origins, suggesting that a single source of Aspergillus sydowii into reefs is unlikely.  The results illustrate the opportunistic nature of the fungal pathogen and suggest that a diversity of isolates can cause aspergillosis.

Despite coming from very different geographic locations (Japan to North America to Europe) and different sources (diseased corals, diseased humans, dried fish), we found that all strains form a single well-connected global population. – lead author Dr. Krystal Rypien, currently a post doc at Scripps Institution of Oceanography

Dr. Rypien added; This has important implications for the management of disease, as it means that any isolate of this fungus has the potential to cause disease in coral, and that we are not dealing with a specialized group of pathogens.  Interestingly, this is similar to a close relative, Aspergillus fumigatus, a common fungal pathogen of immune compromised humans.  Given the global distribution of A. sydowii, and evidence for multiple introductions into marine systems, it seems that this pathogen has always been present in marine systems, and changes in environmental conditions and host immune status are likely to be more important in driving patterns of disease outbreak.

The second study (Rypien 2008) tested the widely-believed hypothesis that African dust plays a role in coral epizootics in general and sea fan aspergillosis in particular.  Each year hundreds of millions of tons of dust is transported from the Sahara desert to the Caribbean.  There are indications that the volume of dust has increased as the Sahara expands and atmospheric conditions and wind patterns change.  The idea is that African dust can cause or exacerbate coral epizootics by depositing nutrients and trace elements that benefit pathogens or by transporting pathogens from terrestrial African habitats to Caribbean coral reefs.  Past studies have indeed found Aspergillus spp. in dust samples collected from the Caribbean, but none have identified the fungi to species, which turns out to be a critical shortcoming.

Dr. Rypien collected dust samples from the Caribbean and Africa, isolated Aspergillus, and identified the isolates to species using standard colony-level and microscopic morphological characteristics.  Despite yielding seven different species of Aspergillus and related taxa, there was no A. sydowii in airborne dust samples from Africa and the Caribbean or in sediment samples from Africa and the Cape Verde Islands.

The lack of A. sydowii in airborne dust and sediment samples suggests that African dust is an unlikely source of the marine pathogen A. sydowii.  Given the high richness of fungi observed, even under selective growth conditions, identification of potential pathogens to the species level is critical.

The study doesn’t entirely refute African dust as a source of Aspergillus sydowii – it is nearly impossible to prove the absence of something – but it does cast doubt on much-heralded theory.

References

Rypien, K. L. 2008. African dust is an unlikely source of Aspergillus sydowii, the causative agent of sea fan disease. Marine Ecology Progress Series 367:125-131.

Rypien, K. L., J. P. Andras, and C. D. Harvell. 2008. Globally panmictic population structure in the opportunistic fungal pathogen Aspergillus sydowii. Molecular Ecology 17:4068-4078.