SPX-related genes regulate phosphorus homeostasis in the marine phytoplankton, Phaeodactylum tricornutum

Kaidian Zhang,Jiashun Li,Senjie Lin,Jingtian Wang,Liying Yu,Zhi Zhou

doi:10.1038/s42003-021-02284-x

Abstract

Phosphorus (P) is an essential nutrient for marine phytoplankton. Maintaining intracellular P homeostasis against environmental P variability is critical for phytoplankton, but how they achieve this is poorly understood. Here we identify a SPX gene and investigate its role in Phaeodactylum tricornutum. SPX knockout led to significant increases in the expression of phosphate transporters, alkaline phosphatases (the P acquisition machinery) and phospholipid hydrolases (a mechanism to reduce P demand). These demonstrate that SPX is a negative regulator of both P uptake and P-stress responses. Furthermore, we show that SPX regulation of P uptake and metabolism involves a phosphate starvation response regulator (PHR) as an intermediate. Additionally, we find the SPX related genes exist and operate across the phytoplankton phylogenetic spectrum and in the global oceans, indicating its universal importance in marine phytoplankton. This study lays a foundation for better understanding phytoplankton adaptation to P variability in the future changing oceans.

Highlights

Phosphorus (P) is an essential nutrient for marine phytoplankton
We mined a collection of reference transcriptomes derived from cultured marine eukaryotic microorganisms (MMETSP)[24], a catalog of genes derived from the Tara Oceans expedition (MATOU)[25], and a collection of metagenomics-based transcriptomes derived from the MATOU catalog (MGTs)[26] to examine the distribution and expression of the SPX genes across phytoplankton species and in the global oceans
Using the SPX domain as a query to search in the P. tricornutum genome, we found a total of six genes that harbor an SPX domain

Summary

Introduction

Phosphorus (P) is an essential nutrient for marine phytoplankton. Maintaining intracellular P homeostasis against environmental P variability is critical for phytoplankton, but how they achieve this is poorly understood. SPX knockout led to significant increases in the expression of phosphate transporters, alkaline phosphatases (the P acquisition machinery) and phospholipid hydrolases (a mechanism to reduce P demand). These demonstrate that SPX is a negative regulator of both P uptake and P-stress responses. Whether a regulatory cascade similar to plants’ SPX-PHR23 operates in P. tricornutum remains unclear We searched this species’ genome and found that it possesses six SPX domaincontaining genes, three of which (one SPX gene and two SPX domain-containing genes) were significantly induced by P deficiency. We mined a collection of reference transcriptomes derived from cultured marine eukaryotic microorganisms (MMETSP)[24], a catalog of genes derived from the Tara Oceans expedition (MATOU)[25], and a collection of metagenomics-based transcriptomes derived from the MATOU catalog (MGTs)[26] to examine the distribution and expression of the SPX genes across phytoplankton species and in the global oceans

Methods

Results

Conclusion