Glyphosate (Roundup) as phosphorus nutrient enhances carbon and nitrogen accumulation and up-regulates phosphorus metabolisms in the haptophyte Isochrysis galbana

Abstract

Inorganic phosphate limitation for phytoplankton may be intensified with water stratification by global warming, and with the increasing nitrogen: phosphorus (N:P) ratio in coastal zones resulting from continuous anthropogenic N overloading. Under these circumstances, phytoplankton's ability to use dissolved organic phosphorus (DOP) will give species a competitive advantage. In our previous study, we have shown that the haptophyte Isochrysis galbana can use glyphosate (Roundup) as a P nutrient source to support growth, but the mechanism of how remains unexplored. Here, we show that three genes encoding PhnC (IgPhnCs), which exhibit up-regulated expression in glyphosate-grown cultures, are probably responsible for glyphosate uptake, while homologs of PhnK and PhnL (IgPhnK and IgPhnL) probably provide auxiliary support for the intracellular degradation of glyphosate. Meanwhile, we found the use efficiency of glyphosate was low compared with phosphate, probably because glyphosate uptake and hydrolysis cost energy and because glyphosate induces oxidative stress in I. galbana. Meanwhile, genes encoding 5-enolpyruvylshikimate 3-phosphate (EPSP) synthase, the target of the herbicide, were up-regulated in glyphosate cultures. Furthermore, our data showed the up-regulation of P metabolisms (transcription) in glyphosate-grown cultures, which further induced the up-regulation of nitrate/nitrite transport and biosynthesis of some amino acids. Meanwhile, glyphosate-grown cells accumulated more C and N, resulting in remarkably high C:N:P ratio, and this, along with the up-regulated P metabolisms, was under transcriptional and epigenetic regulation. This study sheds lights on the mechanism of glyphosate utilization as a source of P nutrient by I. galbana, and these findings have biogeochemical implications.