Sollich Miriam, Yoshinaga Marcos Y, Häusler Stefan, Price Roy E, Hinrichs Kai-Uwe, Bühring Solveig I
University of Bremen, MARUM Center for Marine Environmental SciencesBremen, Germany.
Institute of Chemistry, University of São PauloSão Paulo, Brazil.
Front Microbiol. 2017 Aug 22;8:1550. doi: 10.3389/fmicb.2017.01550. eCollection 2017.
Temperature exerts a first-order control on microbial populations, which constantly adjust the fluidity and permeability of their cell membrane lipids to minimize loss of energy by ion diffusion across the membrane. Analytical advances in liquid chromatography coupled to mass spectrometry have allowed the detection of a stunning diversity of bacterial and archaeal lipids in extreme environments such as hot springs, hydrothermal vents and deep subsurface marine sediments. Here, we investigated a thermal gradient from 18 to 101°C across a marine sediment field and tested the hypothesis that cell membrane lipids provide a major biochemical basis for the bioenergetics of archaea and bacteria under heat stress. This paper features a detailed lipidomics approach with the focus on membrane lipid structure-function. Membrane lipids analyzed here include polar lipids of bacteria and polar and core lipids of archaea. Reflecting the low permeability of their ether-linked isoprenoids, we found that archaeal polar lipids generally dominate over bacterial lipids in deep layers of the sediments influenced by hydrothermal fluids. A close examination of archaeal and bacterial lipids revealed a membrane quandary: not only low permeability, but also increased fluidity of membranes are required as a unified property of microbial membranes for energy conservation under heat stress. For instance, bacterial fatty acids were composed of longer chain lengths in concert with higher degree of unsaturation while archaea modified their tetraethers by incorporation of additional methyl groups at elevated sediment temperatures. It is possible that these configurations toward a more fluidized membrane at elevated temperatures are counterbalanced by the high abundance of archaeal glycolipids and bacterial sphingolipids, which could reduce membrane permeability through strong intermolecular hydrogen bonding. Our results provide a new angle for interpreting membrane lipid structure-function enabling archaea and bacteria to survive and grow in hydrothermal systems.
温度对微生物种群发挥着一级控制作用，微生物会不断调整其细胞膜脂质的流动性和通透性，以尽量减少因离子跨膜扩散而导致的能量损失。液相色谱与质谱联用技术的分析进展，使得人们能够在温泉、热液喷口和深海海底沉积物等极端环境中检测到种类惊人的细菌和古菌脂质。在此，我们研究了一个横跨海洋沉积区域、温度范围从18°C到101°C的热梯度，并验证了以下假设：在热应激条件下，细胞膜脂质为古菌和细菌的生物能量学提供了主要的生化基础。本文采用了一种详细的脂质组学方法，重点关注膜脂质的结构与功能。此处分析的膜脂质包括细菌的极性脂质以及古菌的极性脂质和核心脂质。受热液影响的沉积物深层中，古菌的极性脂质通常比细菌脂质占主导地位，这反映出其醚键连接的类异戊二烯具有较低的通透性。对古菌和细菌脂质的仔细研究揭示了一个膜困境：作为微生物膜在热应激下进行能量守恒的统一特性，不仅需要低通透性，还需要增加膜的流动性。例如，细菌脂肪酸由更长的链长度和更高程度的不饱和度组成，而古菌在沉积物温度升高时通过掺入额外的甲基来修饰其四醚。在高温下，这些使膜更具流动性的构型可能会被大量的古菌糖脂和细菌鞘脂所抵消，这些糖脂和鞘脂可通过强大的分子间氢键作用降低膜的通透性。我们的研究结果为解释膜脂质的结构与功能提供了一个新视角，使古菌和细菌能够在热液系统中生存和生长。
