Integrated omics study delineates the dynamics of lipid droplets in Rhodococcus opacus PD630

Yong Chen ,Xiaowo Wang ,Linhe Huo ,Guiming Liu ,Yan Wang ,Honglei Liu ,Yanda Li ,Toyoshi Fujimoto ,Zenghong Xie ,Guoliang Wang ,Michael Q Zhang ,Congyan Zhang ,Yaxin Zhu ,Huina Zhang ,Fuquan Yang ,Chaoxing Huo ,Shuyan Zhang ,Tong Chuan He ,Yue Zhang ,Li Yang ,Shimeng Xu ,Jun Yu ,Yalan Du ,Xumin Wang ,Jinhai Yu ,Alexander Steinbüchel ,Peng Zhang ,Yunfeng Ding ,Simon Cichello ,Dan Yu ,Hangxiao Zhang ,Lai Song ,Huimin Na ,Zhonghua Fan ,Xuegong Zhang ,Pingsheng Liu

doi:10.1093/nar/gkt932

Abstract

Rhodococcus opacus strain PD630 (R. opacus PD630), is an oleaginous bacterium, and also is one of few prokaryotic organisms that contain lipid droplets (LDs). LD is an important organelle for lipid storage but also intercellular communication regarding energy metabolism, and yet is a poorly understood cellular organelle. To understand the dynamics of LD using a simple model organism, we conducted a series of comprehensive omics studies of R. opacus PD630 including complete genome, transcriptome and proteome analysis. The genome of R. opacus PD630 encodes 8947 genes that are significantly enriched in the lipid transport, synthesis and metabolic, indicating a super ability of carbon source biosynthesis and catabolism. The comparative transcriptome analysis from three culture conditions revealed the landscape of gene-altered expressions responsible for lipid accumulation. The LD proteomes further identified the proteins that mediate lipid synthesis, storage and other biological functions. Integrating these three omics uncovered 177 proteins that may be involved in lipid metabolism and LD dynamics. A LD structure-like protein LPD06283 was further verified to affect the LD morphology. Our omics studies provide not only a first integrated omics study of prokaryotic LD organelle, but also a systematic platform for facilitating further prokaryotic LD research and biofuel development.

Highlights

Lipid droplets (LDs) are cellular organelles widely found in fungal, plant, animal and human cells [1,2,3]
R. opacus PD630 is a useful model for the investigation of LD, since the LD is the only intracellular membranous organelle
We have comprehensively presented the R. opacus PD630 genome, transcriptome and LD proteome, and have systematically investigated the key proteins potentially involved in LD dynamics and functions

Summary

Introduction

Lipid droplets (LDs) are cellular organelles widely found in fungal, plant, animal and human cells [1,2,3]. They are encapsulated by a phospholipid monolayer and are compositionally different from other membrane structures [4]. They differ in that their primary role is lipid storage, but may be pivotal in cellular communication with organelles such as the mitochondria to regulate energy metabolism and substrate utilization. LD is an important organelle related to human metabolic diseases and biofuel productions. Triacylglycerol (TAG) in LD of green algae has been investigated and developed for high oil yields by using targeted metabolic engineering [10,11,12], making it a biological candidate for biofuel production

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