title: Lipid remodelling is a widespread strategy in marine heterotrophic bacteria upon phosphorus deficiency.
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.
authors.affiliation: Departament de Biologia Marina i Oceanografia, Institut de Ciències del Mar, CSIC, Barcelona, Spain.
authors.forename: Marta
authors.initials: M
authors.lastname: Sebastián
authors.affiliation: School of Life Sciences, University of Warwick, Coventry, UK.
authors.forename: Alastair F
authors.initials: AF
authors.lastname: Smith
authors.affiliation: Department of Microbiology, University of La Laguna, La Laguna, Spain.
authors.forename: José M
authors.initials: JM
authors.lastname: González
authors.affiliation: Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, USA.
authors.forename: Helen F
authors.initials: HF
authors.lastname: Fredricks
authors.affiliation: Department of Marine Chemistry and Geochemistry, Woods Hole Oceanographic Institution, Woods Hole, MA, USA.
authors.forename: Benjamin
authors.initials: B
authors.lastname: Van Mooy
authors.affiliation: Institute of Microbiology, Center Algatech, Třeboň, Czech Republic.
authors.forename: Michal
authors.initials: M
authors.lastname: Koblížek
authors.affiliation: Clinical and Experimental Sciences, Faculty of Medicine, University of Southampton, Southampton, UK.
authors.forename: Joost
authors.initials: J
authors.lastname: Brandsma
authors.affiliation: Clinical and Experimental Sciences, Faculty of Medicine, University of Southampton, Southampton, UK.
authors.forename: Grielof
authors.initials: G
authors.lastname: Koster
authors.affiliation: Departament de Biologia Marina i Oceanografia, Institut de Ciències del Mar, CSIC, Barcelona, Spain.
authors.forename: Mireia
authors.initials: M
authors.lastname: Mestre
authors.affiliation: Center of Marine Biodiversity, Exploitation and Conservation (MARBEC), UMR 9190, CNRS - Université de Montpellier - IRD - IFREMER, Place Eugène Bataillon, Université de Montpellier, Case 93, Montpellier, France.
authors.forename: Behzad
authors.initials: B
authors.lastname: Mostajir
authors.affiliation: Hellenic Centre for Marine Research, Oceanography Institute, Heraklion, Greece.
authors.forename: Paraskevi
authors.initials: P
authors.lastname: Pitta
authors.affiliation: Clinical and Experimental Sciences, Faculty of Medicine, University of Southampton, Southampton, UK.
authors.forename: Anthony D
authors.initials: AD
authors.lastname: Postle
authors.affiliation: Departament de Biologia Marina i Oceanografia, Institut de Ciències del Mar, CSIC, Barcelona, Spain.
authors.forename: Pablo
authors.initials: P
authors.lastname: Sánchez
authors.affiliation: Departament de Biologia Marina i Oceanografia, Institut de Ciències del Mar, CSIC, Barcelona, Spain.
authors.forename: Josep M
authors.initials: JM
authors.lastname: Gasol
authors.affiliation: School of Life Sciences, University of Warwick, Coventry, UK.
authors.forename: David J
authors.initials: DJ
authors.lastname: Scanlan
authors.affiliation: School of Life Sciences, University of Warwick, Coventry, UK.
authors.forename: Yin
authors.initials: Y
authors.lastname: Chen
mesh_terms: D020561:Alphaproteobacteria / Q000378:metabolism*; D016695:Glycosyltransferases / Q000378:metabolism; D052836:Heterotrophic Processes; D008522:Mediterranean Sea; D009792:Oceans and Seas; D010710:Phosphates / Q000737:chemistry; D010740:Phospholipases / Q000378:metabolism; D010743:Phospholipids / Q000737:chemistry*; D010758:Phosphorus / Q000737:chemistry*; D010802:Phylogeny; D010839:Phytoplankton / Q000378:metabolism*; D012623:Seawater / Q000382:microbiology*; D014871:Water Microbiology
chemical_list: D010710:Phosphates; D010743:Phospholipids; D010758:Phosphorus; D016695:Glycosyltransferases; D010740:Phospholipases