Bacterial lipid droplets bind to DNA via an intermediary protein that enhances survival under stress

Abstract

Lipid droplets (LDs) are multi-functional organelles consisting of a neutral lipid core surrounded by a phospholipid monolayer, and exist in organisms ranging from bacteria to humans. Here we study the functions of LDs in the oleaginous bacterium Rhodococcus jostii. We show that these LDs bind to genomic DNA through the major LD protein, MLDS, which increases survival rate of the bacterial cells under nutritional and genotoxic stress. MLDS expression is regulated by a transcriptional regulator, MLDSR, that binds to the operator and promoter of the operon encoding both proteins. LDs sequester MLDSR, controlling its availability for transcriptional regulation. Our findings support the idea that bacterial LDs can regulate nucleic acid function and facilitate bacterial survival under stress.

Complementary Approaches to Imaging Subcellular Lipid Architectures in Live Bacteria Using Phosphorescent Iridium Complexes and Raman Spectroscopy

“…The emission of the complexes was detected after only one minute of dosing at room temperature (Supporting Information, Video 1). This extremely fast cellular uptake is remarkable, if one considers that previously reported protocols involve incubation times from 30 minutes up to two hours . All the complexes were excited with a 405 nm laser and the emission collected in the 500–700 nm region (see the Supporting Information), consistent with the emission properties of the complexes in aqueous media (Table S1, Supporting Information).…”

“…The main obstacle to imaging subcellular components in bacteria is represented by their robust cell envelope . Most of the current protocols to image bacteria rely on the use of a relatively limited number of commercial organic dyes or on the genetic manipulation of target proteins . The use of genetically encoded tags, however, can lead to artefacts and it is not applicable to label nonproteinaceous biomolecules such as glycans, nucleic acids and lipids .…”

“…To the best of our knowledge, our protocol is the first to image lipid distributions within prokaryotes using phosphorescent metal complexes. Indeed, imaging of lipid inclusions in bacteria has to date only been achieved with traditional organic dyes . Significantly, an increasing research effort has focused on the study of the lipid metabolism in bacterial cells .…”

Lipid droplet functions beyond energy storage

“…Although the relevance of these findings for adipocyte function remains to be determined, they raise the possibility that Fsp27 can regulate NFAT5's transcriptional activity by controlling its entry into the nucleus. Finally, in the bacterium Rhodococcus jostii , LDs sequester a transcriptional repressor and thus promote expression of a major LD protein [169]. …”

“…Their physiological role remains to be characterized, but it has been speculated that they may modulate transcriptional regulation mediated by lipidic signals, control nuclear membrane composition, or act as nucleus-specific protein storage sites [200]. Recent work in the oleaginous bacterium Rhodococcus jostii even raises the possibility that nuclear LDs might directly modulate DNA-based processes, since here LDs bind to genomic DNA via a major LD protein, possibly protecting the DNA from damage under stressful conditions [169]. A functional analysis of nuclear LDs is within reach because components of a pathway controlling the frequency of nuclear LDs has been identified [197].…”