Transcriptional responses to phosphorus stress in the marine diatom, Chaetoceros affinis, reveal characteristic genes and expression patterns in phosphorus uptake and intracellular recycling

Abstract

Chaetoceros spp. are ecologically important ocean diatoms, and it is hypothesized that their genetic adaptations to phosphorus (P) stress may be different from the adaptations of model species with fully sequenced genomes. To investigate how phosphorus availability affects gene expression at the mRNA level, next-generation sequencing (NGS) was used to construct transcriptomes for Chaetoceros affinis (CCMP 160) cultures grown under low-phosphate and nutrient-replete conditions. This operation generated 29,285 scaffolds, and subsequent sequence comparisons resulted in the identification of 10,972 expressed genes, of which 503 were up-regulated and 553 were down-regulated by P stress. The differential expression patterns of 41 of these genes were confirmed by performing quantitative reverse-transcription polymerase chain reactions. These results demonstrated that genes related to nutrient acquisition are up-regulated in C. affinis under P deficiency. Moreover, C. affinis is unique in that it possesses a “classical” alkaline phosphatase and two type II Na+/Pi cotransporters. Three genes homologous to the ones involved in the higher plant regulatory circuit for P uptake were also identified. P deficiency resulted in enhanced intracellular recycling of P in C. affinis via the upregulation of several ribonuclease genes. However, the expression of a gene involved in sulfolipid production was unaffected. Regarding photochemical reactions, the high transcription levels of light-harvesting complex genes, but low maximum quantum efficiency (Fv/Fm), implied that excess energy was dissipated under P deficiency. Furthermore, the NAD-malic enzyme was up-regulated to generate pyruvate via an alternative pathway that is less dependent on P. In low-P cultures, decreased rates of cell proliferation were found during the early stationary phase, consistent with the significant decrease in transcription of genes encoding cell division control protein 45 and ribonucleoside-diphosphate reductase.