NIOZ Royal Netherlands Institute for Sea Research, Department of Marine Microbiology and Biogeochemistry, Utrecht University, P.O. Box 59, 1797AB, Den Burg, Texel, The Netherlands.
Faculty of Geosciences, Department of Earth Sciences, Utrecht University, P.O. Box 80.021, 3508 TA, Utrecht, The Netherlands.
ISME J. 2021 Jan;15(1):168-182. doi: 10.1038/s41396-020-00772-2. Epub 2020 Sep 14.
Archaea synthesize membranes of isoprenoid lipids that are ether-linked to glycerol-1-phosphate (G1P), while Bacteria/Eukarya produce membranes consisting of fatty acids ester-bound to glycerol-3-phosphate (G3P). This dichotomy in membrane lipid composition (i.e., the 'lipid divide') is believed to have arisen after the Last Universal Common Ancestor (LUCA). A leading hypothesis is that LUCA possessed a heterochiral 'mixed archaeal/bacterial membrane'. However, no natural microbial representatives supporting this scenario have been shown to exist today. Here, we demonstrate that bacteria of the Fibrobacteres-Chlorobi-Bacteroidetes (FCB) group superphylum encode a putative archaeal pathway for ether-bound isoprenoid membrane lipids in addition to the bacterial fatty acid membrane pathway. Key genes were expressed in the environment and their recombinant expression in Escherichia coli resulted in the formation of a 'mixed archaeal/bacterial membrane'. Genomic evidence and biochemical assays suggest that the archaeal-like lipids of members of the FCB group could possess either a G1P or G3P stereochemistry. Our results support the existence of 'mixed membranes' in natural environments and their stability over a long period in evolutionary history, thereby bridging a once-thought fundamental divide in biology.
古菌合成醚键连接甘油-1-磷酸(G1P)的异戊烯脂质膜,而细菌/真核生物则产生脂肪酸酯键连接甘油-3-磷酸(G3P)的膜。这种膜脂组成的二分法(即“脂质鸿沟”)被认为是在最后共同祖先(LUCA)之后出现的。一个主要假设是 LUCA 拥有一个杂合的“混合古菌/细菌膜”。然而,目前还没有显示出任何支持这种情况的天然微生物代表存在。在这里,我们证明了纤维杆菌-绿菌-拟杆菌(FCB)超门的细菌除了具有细菌脂肪酸膜途径外,还编码一种用于醚键结合的异戊烯类膜脂的假定古菌途径。关键基因在环境中表达,其在大肠杆菌中的重组表达导致形成“混合古菌/细菌膜”。基因组证据和生化分析表明,FCB 组成员的类似古菌的脂质可能具有 G1P 或 G3P 立体化学。我们的结果支持在自然环境中存在“混合膜”及其在进化历史上长时间保持稳定的观点,从而弥合了生物学中曾经认为的一个基本鸿沟。