Community-Level Analysis of psbA Gene Sequences and Irgarol Tolerance in Marine Periphyton

Abstract

This study analyzes psbA gene sequences, predicted D1 protein sequences, species relative abundance, and pollution-induced community tolerance in marine periphyton communities exposed to the antifouling compound Irgarol 1051. The mechanism of action of Irgarol is the inhibition of photosynthetic electron transport at photosystem II by binding to the D1 protein. The metagenome of the communities was used to produce clone libraries containing fragments of the psbA gene encoding the D1 protein. Community tolerance was quantified with a short-term test for the inhibition of photosynthesis. The communities were established in a continuous flow of natural seawater through microcosms with or without added Irgarol. The selection pressure from Irgarol resulted in an altered species composition and an inducted community tolerance to Irgarol. Moreover, there was a very high diversity in the psbA gene sequences in the periphyton, and the composition of psbA and D1 fragments within the communities was dramatically altered by increased Irgarol exposure. Even though tolerance to this type of compound in land plants often depends on a single amino acid substitution (Ser 264 3Gly) in the D1 protein, this was not the case for marine periphyton species. Instead, the tolerance mechanism likely involves increased degradation of D1. When we compared sequences from low and high Irgarol exposure, differences in nonconserved amino acids were found only in the so-called PEST region of D1, which is involved in regulating its degradation. Our results suggest that environmental contamination with Irgarol has led to selection for high-turnover D1 proteins in marine periphyton communities at the west coast of Sweden.Development of tolerance, or resistance, to anthropogenic toxicants released into the environment is an issue of increasing importance. Reports of tolerant organisms are increasing, and tolerance toward a variety of compounds has been found (22,44,46,100). This is essentially evolution in action and shows that toxicants can act as selective pressures in the environment. Even though high concentrations of toxicants can be released in episodes or pulses, the overall environmental concentrations of toxicants are often quite low, which implies that adaptation and nonlethal selection are more common than acute and/or lethal effects.Since sensitivities to a given toxicant differ within species and even more so between species (12), a toxicant-induced succession (TIS) will occur in toxicant-exposed communities, where sensitive species, individuals, or genotypes are replaced by more tolerant ones, giving an increase in average tolerance in the community. This chain of events is fundamental for the pollution-induced community tolerance (PICT) concept (14). PICT studies can be performed in natural or model ecosystems and have the important advantage of a causal link between exposure and effect. The concept has been used to demonstrate long-term selection pressure from toxicants on several types of communities, as reviewed by Blanck (10) and...

Microalgal sensitivity varies between a diuron-resistant strain and two wild strains when exposed to diuron and irgarol, alone and in mixtures

“…It was demonstrated that PSII inhibitor resistance was mainly due to a mutation in the gene sequence coding for the D1 protein (Erickson et al, 1989;Oettmeier, 1999). However, according to the literature available, such mutations were not involved in resistance to irgarol (Eriksson et al, 2009). Cells resistant to contaminants arise randomly by rare spontaneous pre-selective mutation during replication L opez-Rodas et al, 2001).…”

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