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Coordination in the transcriptome and proteome of the diatom Thalassiosira pseudonana reveals a diverse phosphorus stress response

ABSTRACT: Phosphorus (P) is a critical driver of phytoplankton growth and ecosystem structure and function in the ocean. Diatoms are an abundant and widespread functional group of phytoplankton that are responsible for significant amounts of primary production in the ocean, however there has not been a comprehensive study of diatom physiological responses to P deficiency. Here, we coupled deep sequencing of transcript tags and quantitative proteomic analysis from the diatom Thalassiosira pseudonana grown under P-replete and P-deficient conditions. The reads (tags) were mapped to the T. pseudonana genome sequence, confirming expression of 91% of the modeled gene set. A total of 318 genes were differentially regulated with a false discovery rate of p<0.05. A total of 1264 proteins were detected, and of those 136 were differentially expressed with a false discovery rate of p<0.05. Significant changes in the abundance of transcripts and proteins were observed and these changes were coordinated for glycolysis, translation, and multiple biochemical responses to P deficiency. These data demonstrate that diatom P deficiency results in changes in cellular P allocation through polyphosphate production, increased P transport, a switch to utilization of dissolved organic P (DOP) through increased production of alkaline phosphatase metalloenzymes and a diesterase, and a remodeling of the cell surface through production of sulfolipids. Together, these findings reveal that T. pseudonana has evolved a sophisticated response to P deficiency involving multiple biochemical strategies that are likely critical to its ability to rapidly respond to variations in environmental P availability.

ORGANISM(S): Thalassiosira pseudonana CCMP1335

PROVIDER: GSE28134 | GEO | 2013/08/03

SECONDARY ACCESSION(S): PRJNA139821

REPOSITORIES: GEO

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Project description:Phosphorus (P) is a critical driver of phytoplankton growth and ecosystem structure and function in the ocean. Diatoms are an abundant and widespread functional group of phytoplankton that are responsible for significant amounts of primary production in the ocean, however there has not been a comprehensive study of diatom physiological responses to P deficiency. Here, we coupled deep sequencing of transcript tags and quantitative proteomic analysis from the diatom Thalassiosira pseudonana grown under P-replete and P-deficient conditions. The reads (tags) were mapped to the T. pseudonana genome sequence, confirming expression of 91% of the modeled gene set. A total of 318 genes were differentially regulated with a false discovery rate of p<0.05. A total of 1264 proteins were detected, and of those 136 were differentially expressed with a false discovery rate of p<0.05. Significant changes in the abundance of transcripts and proteins were observed and these changes were coordinated for glycolysis, translation, and multiple biochemical responses to P deficiency. These data demonstrate that diatom P deficiency results in changes in cellular P allocation through polyphosphate production, increased P transport, a switch to utilization of dissolved organic P (DOP) through increased production of alkaline phosphatase metalloenzymes and a diesterase, and a remodeling of the cell surface through production of sulfolipids. Together, these findings reveal that T. pseudonana has evolved a sophisticated response to P deficiency involving multiple biochemical strategies that are likely critical to its ability to rapidly respond to variations in environmental P availability. T. pseudonana (Strain 1335 from the Provosoli-Guillard National Center for the Culture of Marine Phytoplankton (CCMP)) was grown in a modified f/2 medium made from Sargasso Sea water. Macronutrients and vitamin B12, biotin, and thiamine solutions were treated with prepared Chelex-100 resin to remove trace metal contaminants followed by trace-metal clean syringe sterilization to yield final nutrient concentrations of 882 μM NaNO3 and 106 μM Na2SiO3, and vitamin concentrations of 75 pM, 400 pM, and 60 nM, respectively. The Fe concentration was also modified from f/2 to 400 nM. All conditions were run in triplicate at 14 ºC, in constant light (120 µmol photons m-2 s-1). Cells were grown with f/2 phosphorus concentrations (P-replete; 36 µM PO4) and with low phosphorus concentrations (P-deficient; 0.4 µM PO4). Growth was monitored daily with cell counts. Duplicate P-replete treatments were pooled and harvested in mid log phase, and triplicate P-deficient treatments were pooled, and also quickly harvested onto 2 µm filters at the onset of P depletion. All RNA samples were snap frozen in liquid nitrogen. Replicate P-deficient cultures were refed to 36 µM phosphate at the onset of P depletion, and subsequently resumed growth. Additional growth studies were performed as described above substituting glycerolphosphate and adenosine monophosphate at 36 µM, for the phosphate in the medium.

Project description:Diatoms perform about 20% of photosynthesis on earth, play a crucial role in forming the base of the marine food web, and sequester anthropogenic carbon into the deep ocean through the biological pump. In some areas of the ocean, diatom growth is limited by the organic micronutrient cobalamin (vitamin B12). Cobalamin affects phytoplankton growth rate and biomass yield, though the consequences of cobalamin limitation are not well understood on the biochemical level. In a controlled laboratory setting, we grew two diatoms, Thalassiosira pseudonana and Navicula pelliculosa, under cobalamin limited and replete conditions to elucidate changes in metabolite pools under cobalamin limitation. Using targeted and untargeted metabolomics, we show that the cobalamin-dependent T. pseudonana experienced a metabolic cascade under cobalamin limitation that a ects the central methionine cycle, the transsulfuration pathway, and the composition of its osmolyte pools. N. pelliculosa, a cobalamin-independent diatom, also showed evidence for changes in the methionine cycle when grown without cobalamin, though to a lesser extent than what we observed in T. pseudonana. In both diatoms the concentration of 5'-methylthioadenosine decreased when limited for cobalamin, suggesting a disruption in the diatoms' polyamine biosynthesis. Furthermore, two acylcarnitines and adenosyl cobalamin accumulated in T. pseudonana under cobalamin limitation, suggesting the use of an adenosylcobalamin-dependent enzyme, methylmalonyl CoA mutase. Overall, these changes in metabolite pools yield insight into the metabolic consequences of cobalamin limitation in diatoms and suggest that cobalamin starvation may have consequences for microbial interactions that are based on metabolite production by phytoplankton. Thalassiosira pseudonana protocols and data are reported in the current study <a href='https://www.ebi.ac.uk/metabolights/MTBLS703' rel='noopener noreferrer' target='_blank'>MTBLS703</a>. Navicula pelliculosa protocols and data are reported in <a href='https://www.ebi.ac.uk/metabolights/MTBLS708' rel='noopener noreferrer' target='_blank'>MTBLS708</a>.

Project description:Diatoms perform about 20% of photosynthesis on earth, play a crucial role in forming the base of the marine food web, and sequester anthropogenic carbon into the deep ocean through the biological pump. In some areas of the ocean, diatom growth is limited by the organic micronutrient cobalamin (vitamin B12). Cobalamin affects phytoplankton growth rate and biomass yield, though the consequences of cobalamin limitation are not well understood on the biochemical level. In a controlled laboratory setting, we grew two diatoms, Thalassiosira pseudonana and Navicula pelliculosa, under cobalamin limited and replete conditions to elucidate changes in metabolite pools under cobalamin limitation. Using targeted and untargeted metabolomics, we show that the cobalamin-dependent T. pseudonana experienced a metabolic cascade under cobalamin limitation that a ects the central methionine cycle, the transsulfuration pathway, and the composition of its osmolyte pools. N. pelliculosa, a cobalamin-independent diatom, also showed evidence for changes in the methionine cycle when grown without cobalamin, though to a lesser extent than what we observed in T. pseudonana. In both diatoms the concentration of 5'-methylthioadenosine decreased when limited for cobalamin, suggesting a disruption in the diatoms' polyamine biosynthesis. Furthermore, two acylcarnitines and adenosyl cobalamin accumulated in T. pseudonana under cobalamin limitation, suggesting the use of an adenosylcobalamin-dependent enzyme, methylmalonyl CoA mutase. Overall, these changes in metabolite pools yield insight into the metabolic consequences of cobalamin limitation in diatoms and suggest that cobalamin starvation may have consequences for microbial interactions that are based on metabolite production by phytoplankton. Navicula pelliculosa protocols and data are reported in the current study <a href='https://www.ebi.ac.uk/metabolights/MTBLS708' rel='noopener noreferrer' target='_blank'>MTBLS708</a>. Thalassiosira pseudonana protocols and data are reported in <a href='https://www.ebi.ac.uk/metabolights/MTBLS703' rel='noopener noreferrer' target='_blank'>MTBLS703</a>.

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Coordination in the transcriptome and proteome of the diatom Thalassiosira pseudonana reveals a diverse phosphorus stress response

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