Abstract
The impact of organic pollutants on oceanic ecosystem functioning is largely unknown. Prochlorococcus, the most abundant known photosynthetic organism on Earth, has been suggested to be especially sensible to exposure to organic pollutants, but the sub-lethal effects of organic pollutants on its photosynthetic function at environmentally relevant concentrations and mixtures remain unexplored. Here we show the modulation of the expression of two photosynthetic genes, rbcL (RuBisCO large subunit) and psbA (PSII D1 protein), of oceanic populations of Prochlorococcus from the Atlantic, Indian and Pacific Oceans when exposed to mixtures of organic pollutants consisting of the non-polar fraction of a seawater extract. This mixture included most persistent organic pollutants, semivolatile aromatic-like compounds, and the unresolved complex mixture of hydrocarbons. Prochlorococcus populations in the controls showed the expected diel cycle variations in expression of photosynthetic genes. However, exposure to a complex mixture at concentrations only 2-fold above the environmental levels resulted in a decrease of expression of both genes, suggesting an effect on the photosynthetic function. While organic pollutant effects on marine phytoplankton have been already demonstrated at the cellular level, this is the first field study showing alterations at the molecular level of the photosynthetic function due to organic pollutants.
Highlights
Semivolatile and hydrophobic organic pollutants (OPs) reach the global oceans by long range atmospheric transport and deposition, can affect ecosystems, and represent a vector of global change[1,2,3,4,5]
Several studies showed that mixtures of organic pollutants, including those known as persistent organic pollutants (POPs), can exert a toxic effect on marine phytoplankton, reducing their abundance and viability at concentrations one to two orders of magnitude higher than those found in oceanic waters[3, 10]
The recent development of a quantitative method to assess the expression of the photosynthetic genes rbcL and psbA (D1 protein) of Prochlorococcus allowed identifying specific perturbations of these genes in Prochlorococcus axenic cultures when exposed to sublethal levels of simple mixtures of polycyclic aromatic hydrocarbons (PAHs) or organochlorine pesticides (OClPs)[18]
Summary
In order to analyze the effects of both simple and complex mixtures of OPs on the photosynthetic capacity of Prochlorococcus at environmentally relevant levels, we quantified the expression of the two photosynthetic genes rbcL and psbA in natural communities of Prochlorococcus from the Atlantic, Pacific and Indian Oceans (Fig. 1) after exposure to OP mixtures. PAH and n-alkanes can be considered tracers (or surrogates) of the whole mixture of hydrocarbons and OPs, as these OPs have similar physical-chemical properties than the other compounds present in the same non-polar fraction of the seawater extract, and chemicals with similar properties behave [19] These results are consistent with those described for lethality effects on oceanic Prochlorococcus[3, 27], and with other studies performed with different toxicity endpoints, in which the toxicity of known compounds is a small fraction of the total toxicity detected in the sample[20, 21], and with other studies reporting the toxicity of the aromatic UCM28, 29. This perturbation may contribute to the decline in phytoplankton abundance and productivity reported during the Anthropocene for some oceanic regions[32, 33]
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