Expression of nuclear-encoded, haptophyte-derived ftsH genes support extremely rapid PSII repair and high-light photoacclimation in Karenia brevis (Dinophyceae)

Abstract

Karenia brevis, a neurotoxic dinoflagellate that produces brevetoxins, is endemic to the Gulf of Mexico and can grow at high irradiances typical of surface waters found there. To build upon a growing number of studies addressing high-light tolerance in K. brevis, specific photobiology and molecular mechanisms underlying this capacity were evaluated in culture. Since photosystem II (PSII) repair cycle activity can be crucial to high light tolerance in plants and algae, the present study assessed this capacity in K. brevis and characterized the ftsH-like genes which are fundamental to this process. Compared with cultures grown in low-light, cultures grown in high-light showed a 65-fold increase in PSII photoinactivation, a ∼50-fold increase in PSII repair, enhanced nonphotochemical quenching (NPQ), and depressed Fv/Fm. Repair rates were among the fastest reported in phytoplankton. Publicly available K. brevis transcriptomes (MMETSP) were queried for ftsH-like sequences and refined with additional sequencing from two K. brevis strains. The genes were phylogenetically related to haptophyte orthologs, implicating acquisition during tertiary endosymbiosis. RT-qPCR of three of the four ftsH-like homologs revealed that poly-A tails predominated in all homologs, and that the most highly expressed homolog had a 5′ splice leader and amino-acid motifs characteristic of chloroplast targeting, indicating nuclear encoding for this plastid-targeted gene. High-light cultures showed a ∼1.5-fold upregulation in mRNA expression of the thylakoid-associated genes. Overall, in conjunction with NPQ mechanisms, rapid PSII repair mediated by a haptophyte-derived ftsH prevents chronic photoinhibition in K. brevis. Our findings continue to build the case that high-light photobiology—supported by the acquisition and maintenance of tertiary endosymbiotic genes—is critical to the success of K. brevis in the Gulf of Mexico.