| Dissolved inorganic phosphate(DIP)limitation has been shown to constrain primary production and nitrogen fixation in the marine ecosystem.Dissolved organic phosphorus(DOP)could be a potential source of P when DIP is limited.Phosphonates are an important kind of DOP characterized by the stable C-P bond,however,its utilization has only been reported in heterotrophic bacteria and cyanobacteria.It has remained unexplored whether eukaryotic phytoplankton are able to utilize phosphonates as a sole source of P or not.Excess light energy can potentially cause photo-oxidative damage and thus is another important challenge faced by phytoplankton living in the surface ocean.Moreover,intensified water column stratification due to global warming has the potential to decrease nutrient availability for the photosynthesis of phytoplankton and also subject phytoplankton to increased excess light in the euphoric zone.Non-photochemical quenching(NPQ)could dissipate the excess light as heat,and thus is an important photoprotective strategy in phytoplankton.However,studies related to NPQ regulation under P deprivation in marine phytoplankton are still very limited.Dinoflagellates constitute one of the most important eukaryotic phytoplankton groups in the marine ecosystem,and contribute significantly to marine primary production,coral reef growth(by the genus of Symbiodinium),harmful algal blooms(HABs),and marine biotoxins.Karlodinium veneficum is a cosmopolitan HAB-forming dinoflagellate species responsible for mass fish kills in many coastal areas of the world due to the production of karlotoxins which demonstrate hemolytic,cytotoxic,and ichthyotoxic properties.In this study,by using K.veneficum and several other dinoflagellate species,we conducted the following work:1.We detected the genes encoding the C-P hydrolase pathway enzymes PhnW and PhnX in K.veneficum and other dinoflagellates through transcriptomic analysis.Furthermore,the genes related to phosphonate biosynthesis were also widely distributed in dinoflagellates.The culture experiments showed that 2-aminoethylphosphonic acid(2-AEP),the presumably dominant type of phosphonate in the ocean,could facilitate the growth of dinoflagellates in normal cultures without antibiotics addition.However,these dinoflagellates are unable to utilize 2-AEP as a sole source of P under the antibiotic-treated condition.In accordance,our RT-qPCR and proteomic analyses of K.veneficum grown on 2-AEP showed no up-regulation of PhnW and PhnX at both transcriptional and translational levels.Taken together,our results suggest that the PhnW-PhnX pathway in dinoflagellates may serve for intracellular phosphonate metabolism instead of scavenging environmental phosphonates.Nevertheless,the study also indicated that phosphonates could be utilized by dinoflagellates through the mediation of bacteria,which bears important significance in the marine ecosystem.2.We investigated whether NPQ is enhanced and how it is regulated molecularly under phosphorus(P)deprivation in the dinoflagellate K.veneficum.We grew K.veneficum under P-replete and P-depleted conditions,monitored their growth rates and chlorophyll fluorescence,and conducted comparative proteomic analysis and gene expression analyses.The results indicated that NPQ in K.veneficum was elevated significantly under P deficiency.Accordingly,the abundances of many pigment proteins including three light-harvesting complex stress-related proteins LI818(named LHCX or LHCSR)increased under P-depleted condition.Besides,many enzymes related to genetic information flow were down-regulated while many enzymes related to energy production and conversion were up-regulated under P deprivation.Taken together,this study indicates that K.veneficum cells respond to P deficiency by reconfiguring the metabolic landscape and up-tuning NPQ to increase the capacity to dissipate excess light energy,which provides a new perspective about what adaptive strategy dinoflagellates have evolved to cope with P deprivation. |
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