Article: Ciminiello et al. (2014) First finding of Ostreopsis cf. ovata toxins in marine aerosols. Environmental Science & Technology. 48: 3532-3540. DOI: 10.1021/es405617d
Harmful algal blooms, or HABs, are growth bursts of either micro- or macroalgae that have negative impacts on the local ecosystem and nearby human populations. In some cases, advantageous weather and nutrient conditions allow for certain species of algae to proliferate rapidly, creating a dense assemblage that consequently blocks sunlight to the water column, smothers other species by clogging their gills, and robs the water of oxygen when the algae dies and sinks, creating hypoxic conditions and fish kills. In other instances, the type of algae that blooms contains potent toxins which can cause illness and death in humans and marine organisms, alike. Such blooms occur repeatedly in certain coastal areas, including the Gulf of Maine, where the dinoflagellate Alexandrium fundyense produces the neurotoxin saxitoxin, and in the Gulf of Mexico, where the dinoflagellate Kerenia brevis creates a “red tide” and produces a neurotoxin called brevetoxin. Both toxins are associated with shellfish poisoning in humans resulting from the consumption of contaminated shellfish.
Since the late 1990s, HABs of the dinoflagellate Ostreopsis spp. have been affecting coastal areas all around the Mediterranean Sea (Figure 1). While two Ostreopsis species bloom in the region, it is O. cf. ovata that is known to contain analogues of palytoxin, one of the most potent marine toxins. Accompanying these blooms, there have been outbreaks of respiratory syndromes in humans exposed to marine air. People affected showed symptoms including fever, runny nose, coughing, headaches, nausea/vomiting, bronchoconstriction, and wheezing. The first toxic outbreak occurred along the Tuscan coastline in 1998, where ~100 people developed symptoms, and it has since been observed that human symptoms peak with the climax of the O. cf. ovata bloom, and end when the bloom dissipates. However, inhalation exposure to palytoxins has not been fully established and the presence of these toxins in aerosols has not been confirmed. Previous studies of brevetoxins from red tides revealed uptake of the toxin by aerosols and subsequent respiratory problems in exposed humans. Marine aerosols are produced when wind and wave conditions are right for “bubble bursting.” Bubbles of trapped air rise to the water surface, burst, and form film droplets, ejecting with them algal cells, bacteria, and waterborne toxins present in the surface water. It is possible that O. cf. ovata cells, or the palytoxins they produce, are being transported to the atmosphere as aerosols, where they are subsequently breathed in by unsuspecting beach goers.
To verify the potential toxicity of marine aerosols and to study this mechanism of exposure, a research group in Italy monitored two sites along the Tuscan coastline: Marina di Massa, where Ostreopsis-related illness was first recorded in humans, and Marina di Pisa, 60 kilometers away. Both sites tend to be infested by O. cf. ovata every summer due to their pebble beaches which are favorable for the hard-substrate-loving species, and their relatively protected waters thanks to submerged breakwaters built to prevent coastal erosion. Water and macroalgae samples were collected daily during the summer bloom event, from mid-July to late August 2009 and 2010. Aerosols were collected using portable air samplers a few hours every day. Ostreopsis species were identified using PCR-based DNA extraction, and toxins were determined using liquid chromatography-high resolution mass spectrometry (LC-HRMS).
Italian health guidelines say seawater concentrations of O. cf. ovata exceeding 10,000 cells per liter is an emergency situation. In 2009, cell counts reached 5,000-24,000 cells per liter in analyzed aerosols, however, no respiratory symptoms were reported at the local hospital during the sampling period. In 2010, O. cf. ovata counts were much higher, reaching a peak of ~280,000 cells per liter in early August at Marina di Massa and ~180,000 cells per liter in late July at Marina di Pisa. The bloom created a rusty brown mucilaginous film which covered the macroalgae community and created suspended lumps in the water column (Figure 2). Despite being present at concentrations well above the designated emergency level, no human respiratory illnesses were recorded during the 2010 sampling period, either. One explanation offered by the research team is that meteomarine conditions were not ideal for aerosol transport. Weather conditions were generally mild, and, although it is clear that O. cf. ovata was present in aerosols, those aerosols were collected 10 meters offshore and may not have been significantly transported to populated areas. Additionally, wind and wave turbulence may not have been great enough to fragment the mucilaginous sheath of O. cf. ovata and generate massive aerosols. In general, concentrations measured in 2009 and 2010 were significantly lower than those of the 2005 Ligurian outbreak, when the O. cf. ovata count exceeded 1,800,000 cells per liter, perhaps suggesting that the sampled bloom simply was not great enough to pose a human health risk.
In addition to the O. cf. ovata cells, this study represents the first time ovatoxins (analogues of palytoxin) have been detected in marine aerosols, providing a missing link between O. cf. ovata blooms and human respiratory syndrome. Toxins were detected in aerosols collected at Marina di Pisa at the end of the bloom, when cell counts were starting to drop. It is likely that, during senescence, the cells are breaking, releasing higher amounts of toxins into the seawater, ready for aerosol formation. However, it is not clear whether human symptoms are due to the toxins themselves or an allergic-like reaction to inhaled O. cf. ovata cell fragments, or even a combination of the two. Since Ostreopsis HABs are repeat events across the Mediterranean, it is important to understand which mechanism is causing human illness and the pathway by which palytoxins enter the human body. Although this study sets an important precedent, continued monitoring must be conducted in order to measure conditions during hazardous outbreaks and to determine trends in frequency, duration, and severity of such HABs.