Dysregulation of photosynthetic genes in oceanic Prochlorococcus populations exposed to organic pollutants

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.

Microbial responses to anthropogenic dissolved organic carbon in the Arctic and Antarctic coastal seawaters

“…These concentrations were analysed from the same bottles where metagenomes and metatranscriptomes were sequenced, using the filtrate after collecting biomass for DNA/RNA material. Still, field experiments performed in tropical seawaters have been able to detect a decrease in concentrations for n-alkanes after 24 h of incubation (Fernández-Pinos et al, 2017). We did not observe a significant decrease of concentrations of total PAHs, n-alkanes and OPEs larger than the accuracy of the concentration measurements after 24 h of incubation (Table 1; t-test, P > 0.05).…”

“…Operationally defined ADOC was obtained following the standard protocols for sampling and extraction of hydrophobic and non-polar OPs and hydrocarbons from seawater (Galbán-Malagón et al, 2012;Galbán-Malagón et al, 2013a;González-Gaya et al, 2016;Fernández-Pinos et al, 2017). Operationally defined ADOC was obtained following the standard protocols for sampling and extraction of hydrophobic and non-polar OPs and hydrocarbons from seawater (Galbán-Malagón et al, 2012;Galbán-Malagón et al, 2013a;González-Gaya et al, 2016;Fernández-Pinos et al, 2017).…”

“…Briefly, 200 l of surface water (4 m depth) was collected during the ATOS-I and ATOS-II sampling cruises in the Arctic (Galbán-Malagón et al, 2012) and Southern Oceans (Galbán-Malagón et al, 2013b). This is analogous to the mixture used previously for assessing the influence of ADOC to phytoplankton (Echeveste et al, 2016;Fernández-Pinos et al, 2017). The XAD-2 adsorbent was eluted with methanol followed by dichloromethane.…”

“…Recent studies have shown that hydrophobic OPs have toxicological effects on temperate and polar phytoplankton. Minimal variation of the aliphatic and aromatic fractions of ADOC inhibited gene expression of photosynthetic genes of Prochlorococcus without inducing mortality (Fernández-Pinos et al, 2017). Minimal variation of the aliphatic and aromatic fractions of ADOC inhibited gene expression of photosynthetic genes of Prochlorococcus without inducing mortality (Fernández-Pinos et al, 2017).…”

“…The smallest cells, Synechococcus and Prochlorococcus, were the most sensitive in the subtropical oligotrophic oceans, but diatoms and flagellates also decreased in abundance in the Arctic and Southern oceans (Echeveste et al, 2016). Minimal variation of the aliphatic and aromatic fractions of ADOC inhibited gene expression of photosynthetic genes of Prochlorococcus without inducing mortality (Fernández-Pinos et al, 2017). Analysis of community gene expression, metatranscriptomics, has been successfully used to describe the effects of oil spills on microbial communities .…”