Sebastián Marta, Smith Alastair F, González José M, Fredricks Helen F, Van Mooy Benjamin, Koblížek Michal, Brandsma Joost, Koster Grielof, Mestre Mireia, Mostajir Behzad, Pitta Paraskevi, Postle Anthony D, Sánchez Pablo, Gasol Josep M, Scanlan David J, Chen Yin
Departament de Biologia Marina i Oceanografia, Institut de Ciències del Mar, CSIC, Barcelona, Spain.
School of Life Sciences, University of Warwick, Coventry, UK.
ISME J. 2016 Apr;10(4):968-78. doi: 10.1038/ismej.2015.172. Epub 2015 Nov 13.
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.
在缺磷情况下,海洋浮游植物通过用替代性非磷脂质取代膜磷脂来降低对磷的需求。最近有研究表明,一种SAR11分离株在培养中磷酸盐缺乏时也具有这种能力。然而,这一过程在其他海洋异养细菌以及自然环境中的发生程度尚不清楚。在此,我们证明,膜磷脂被多种非磷脂质取代是系统发育上不同的海洋异养细菌(包括α-变形菌和黄杆菌成员)对磷缺乏的一种保守反应。通过在模式海洋细菌费氏杆菌属Phaeobacter sp. MED193中进行缺失诱变和互补实验,以及在重组大肠杆菌中进行异源表达,我们证实了磷脂酶C(PlcP)和糖基转移酶在脂质重塑中的作用。对全球海洋采样和塔拉海洋宏基因组数据集的分析表明,PlcP在磷酸盐浓度低的区域特别丰富。此外,我们表明脂质重塑在季节性发生,并对地中海自然微生物群落中不断变化的营养条件作出反应。总之,我们的结果表明脂质替代作为一种适应性策略,使异养细菌能够在海洋中广阔的贫磷区域中生存,发挥着关键作用。