Lipid remodelling is a widespread strategy in marine heterotrophic bacteria upon phosphorus deficiency.

Marta Sebastián,Michal Koblížek,Josep M Gasol,Anthony D Postle,José M González,Grielof Koster,Yin Chen,David J Scanlan,Behzad Mostajir,Paraskevi Pitta,Mireia Mestre,Alastair F Smith,Benjamin Van Mooy,Pablo Sánchez,Helen F Fredricks,Joost Brandsma

doi:10.1038/ismej.2015.172

Abstract

Upon phosphorus (P) deficiency, marine phytoplankton reduce their requirements for P by replacing membrane phospholipids with alternative non-phosphorus lipids. It was very recently demonstrated that a SAR11 isolate also shares this capability when phosphate starved in culture. Yet, the extent to which this process occurs in other marine heterotrophic bacteria and in the natural environment is unknown. Here, we demonstrate that the substitution of membrane phospholipids for a variety of non-phosphorus lipids is a conserved response to P deficiency among phylogenetically diverse marine heterotrophic bacteria, including members of the Alphaproteobacteria and Flavobacteria. By deletion mutagenesis and complementation in the model marine bacterium Phaeobacter sp. MED193 and heterologous expression in recombinant Escherichia coli, we confirm the roles of a phospholipase C (PlcP) and a glycosyltransferase in lipid remodelling. Analyses of the Global Ocean Sampling and Tara Oceans metagenome data sets demonstrate that PlcP is particularly abundant in areas characterized by low phosphate concentrations. Furthermore, we show that lipid remodelling occurs seasonally and responds to changing nutrient conditions in natural microbial communities from the Mediterranean Sea. Together, our results point to the key role of lipid substitution as an adaptive strategy enabling heterotrophic bacteria to thrive in the vast P-depleted areas of the ocean.

Highlights

Phosphorus (P) is required by all living organisms (Karl, 2014)
Lipid remodelling is a widespread strategy in marine heterotrophic bacteria under low P conditions The ability to synthesize non-P lipids seems to be widespread among marine heterotrophic bacteria adapted to low P environments
We found that in P-depleted regions, such as the North Atlantic Subtropical Gyre and the Mediterranean Sea, PlcP may be present in the majority of bacterial cells (Supplementary Figure S1)

Summary

Introduction

2009) and the view that non-P lipids are primarily PlcP homologue sequences were retrieved from derived from phytoplankton has influenced the marine bacterial isolates using the Integrated Microinterpretation of some studies (Close et al, 2014; bial Genomes database and marine metagenomes of Gašparović et al, 2014) This view has since been the GOS (Rusch et al, 2007) and the Tara challenged by the observation of glycolipids in the Oceans (Sunagawa et al, 2015) data sets, using membranes of heterotrophic bacteria from the PlcP (MED193_17359) of strain MED193 as a query P-depleted Sargasso Sea (Popendorf et al, 2011) as (e-valueo − ). We demonstrate for the first time that Samples from the LAMP2011 mesocosm experilipid remodelling occurs in nature in P-starved ment in the Eastern Mediterranean Sea (see heterotrophic bacterial communities, which synthe- Supplementary Material and Methods for details) size a wide array of non-P lipids, some of which were were size-fractionated through 0.8-μm pore size previously ascribed to phytoplankton. Growth conditions for marine heterotrophic bacteria tion of the identification and characterization of under P-replete and deplete media are detailed in the glucuronic acid diacylglycerol (GADG) (see below)

Discussion

Findings

Global Ocean Sampling expedition: northwest