Elevated Atmospheric Carbon Dioxide Concentrations Amplify Alternaria Alternata Sporulation and Total Antigen Production
Wolf, Julie, O'Neill, Nichole R., Rogers, Christine A., Muilenberg, Michael L., Ziska, Lewis H., Environmental Health Perspectives
BACKGROUND: Although the effect of elevated carbon dioxide ([CO.sub.2]) concentration on pollen production has been established in some plant species, impacts on fungal sporulation and antigen production have not been elucidated.
OBJECTIVE: Our purpose was to examine the effects of rising atmospheric [CO.sub.2] concentrations on the quantity and quality of fungal spores produced on timothy (Phleum pratense) leaves. METHODS: Timothy plants were grown at four [CO.sub.2] concentrations (300,400,500, and 600 [micro]mol/mol). Leaves were used as growth substrate for Alternaria alternata and Cladosporium phlei. The spore abundance produced by both fungi, as well as the size (microscopy) and antigenic protein content (ELISA) of A. alternata, were quantified.
RESULTS: Leaf carbon-to-nitrogen ratio was greater at 500 and 600 [micro]mol/mol, and leaf biomass was greater at 600 [micro]mol/mol than at the lower [CO.sub.2] concentrations. Leaf carbon-to-nitrogen ratio was positively correlated with A. alternata spore production per gram of leaf but negatively correlated with antigenic protein content per spore. At 500 and 600 [micro]mol/mol [CO.sub.2] concentrations, A. alternata produced nearly three times the number of spores and more than twice the total antigenic protein per plant than at lower concentrations. C. phlei spore production was positively correlated with leaf carbon-to-nitrogen ratio, but overall spore production was much lower than in A. alternata, and total per-plant production did not vary among [CO.sub.2] concentrations.
CONCLUSIONS: Elevated [CO.sub.2] concentrations often increase plant leaf biomass and carbon-to-nitrogen ratio. Here we demonstrate for the first time that these leaf changes are associated with increased spore production by A. alternata, a ubiquitous allergenic fungus. "This response may contribute to the increasing prevalence of allergies and asthma.
KEY WORDS: allergic rhinitis, Alternaria alternata, asthma, Cladosporium phlei, elevated atmospheric carbon dioxide ([CO.sub.2]), fungal antigenic protein, fungal sporulation, global climate change, plant carbon-to-nitrogen ratio (C:N), timothy grass (Phleum pratense). Environ Health Perspect 118:1223-1228 (2010). doi:10.1289/ehp.0901867 [Online 13 May 2010]
Anthropogenic increases in global atmospheric carbon dioxide ([CO.sub.2]) concentration have been shown to stimulate earlier and greater production of allergenic pollen (LaDeau and Clark 2006; Rogers et al. 2006; Ziska et al. 2003), as have warming temperatures (Wan et al. 2002; Yli-Panula et al. 2009). The effects of anthropogenic climate change on the production of airborne fungal spores are not as well documented, but the implications for allergic disease are no less important. As with pollen, exposure to fungal spores is associated with allergy and asthma symptoms [Institute of Medicine (IOM) 2000, 2004; Salo et al. 2006], although the specifics of the relationship are not completely understood (Portnoy et al. 2008). Among patients with asthma from six regions of the world, 11.9%, on average, were sensitized to Alternaria alternata, with the proportion as high as 28.2% in Portland, Oregon; in addition, sensitivity to A. alternata was more prevalent among patients with more severe asthma (Zureik et al. 2002). Allergenic fungal spores may be increasingly abundant in some areas of the globe as well. In Derby, United Kingdom, mean seasonal airborne spore concentrations of the genus Alternaria have increased over the years 1970-1998, as have the number of days with spore counts > 50 per cubic meter of air, and the start of the Alternaria spore season has advanced from the end to the beginning of June (Corden and Millington 2001).
Rising atmospheric [CO.sub.2] concentration is well documented [Intergovernmental Panel on Climate Change (IPCC) 2007]. Large increases in atmospheric [CO.sub.2] concentration (e.g., doubled or greater increases in concentration) have been shown to alter both plant biomass and chemistry in many plant species (Ainsworth and Long 2005; Taub et al. …